Phylogeny and Generic Limits in the Sister Tribes Psychotrieae and Palicoureeae (Rubiaceae): Evolution of Schizocarps in Psychotria and Origins of Bacterial Leaf Nodules of the Malagasy Species

Birgitta Bremer

Dissotis has long been regarded as the most species-rich genus of African Melastomataceae, yet its diagnostic characters have never been examined in an explicitly phylogenetic context. In a previous study, we recovered a large clade consisting of "Dissotis and allies" but with poorly understood generic limits. Here we present a nearly complete phylogeny of African Melastomateae with focus on Dissotis and allies using sequences generated from two nuclear (nrETS, nrITS) and two plastid markers (ndhF, psbK-psbL), sampling 94 accessions representing 69 species including outgroups. We infer phylogenetic relationships using maximum likelihood, parsimony and Bayesian approaches and propose a revised generic classification of Dissotis and allies based on our molecular trees. In addition, we reconstruct the ancestral state of 20 important morphological characters of African Melastomateae. Dissotis and Antherotoma as previously circumscribed are polyphyletic, while all four of the previously recognised sections of Dissotis subg. Dissotis are monophyletic (i.e., sections Dissotis, Macrocarpae, Sessilifoliae and Squamulosae). We also recovered a clade consisting of D. congolensis, A. sene-gambiensis, A. clandestina and Nerophila gentianoides plus the species earlier treated in African Osbeckia. Ancestral character reconstruction indicates there are no unambiguous morphological synapomorphies for Dissotis s.l. In particular, the character of staminal dimorphism is shown to be homoplasious. However, the individual clades making up Dissotis and allies are each diagnosed by one to several morphological characters. In view of these results, we propose the following changes for the classification of African Melasto-mateae: (1) five new genera are described, Almedanthus (for Dissotis pachytricha), Eleotis (for D. sect. Sessilifoliae), Feliciotis (for D. sect. Macrocarpae), Pyrotis (for D. gilgiana) and Rosettea (for D. sect. Squamulosae); (2) the genus Nerophila is reinstated with an expanded circumscription to include Antherotoma senegambiensis, A. clandestina, D. congolensis, D. pauciflora and three species earlier treated in African Osbeckia; (3) circumscription of Dissotis s.str. is reduced to six species; (4) the monospecific genus Derosiphia is reinstated; and (5) two species previously placed in Dissotis are transferred to Antherotoma. To complete our generic realignment, 12 new synonyms and 58 new combinations are effected at or below the species level. A total of 40 lecto-or neotypes are designated. A revised key is provided for African Melastomateae, including all nine genera presently recognised in Dissotis and allies. Dissotis leo-nensis (type and only species of D. subg. Paleodissotis) together with the monospecific Cailliella and Dionychastrum remain unsampled.

Melastomateae are the most species-rich (185 spp./13 gen.) and morphologically diverse tribe within the African Melastomataceae. In this study we present the first in-depth phylogenetic analysis of African Melastomateae using sequences generated from one nuclear (nrITS) and two plastid spacers (accD-psaI, psbK-psbL) sampling 183 accessions representing 75 African, 10 Madagascan and 7 Asian species and a broad outgroup sampling. We infer phylogenetic relationships using maximum likelihood, maximum parsimony and Bayesian approaches and propose a revised generic classification of African Melastomateae based on our molecular trees in combination with a careful reassessment of morphological variation. Our phylogenetic analyses support the monophyly of Old World Melastomateae except Dinophora which clearly falls outside Melastomateae. Asian and Madagascan endemic genera of Melastomateae are nested among the African genera. Of the African genera only two monophyletic groups, Dichaetanthera and Tristemma, are recovered in addition to the monospecific Pseudosbeckia lineage, while Antherotoma, Dissotis and Heterotis as currently circumscribed are polyphyletic. However, the subgenera and sections of these genera are mostly recovered as morphologically distinct and molecularly well-supported clades. Isomorphism versus dimorphism of the stamens is found to be an unreliable character when delimiting genera in Melastomateae. We propose the reinstatement of Argyrella and Dupineta, a new status at generic rank for Dissotis subg. Dissotidendron, a broadened circumscription of Guyonia (to include the species previously placed in Heterotis sect. Cyclostemma), and description of a new, monospecific genus Anaheterotis for the Heterotis pobeguinii lineage. Heterotis is maintained at generic rank but with a narrower circumscription in comparison to earlier treatments. We accommodate the rare Osbeckia porteresii lineage from Mt. Nimba (Guinea) within an expanded Melastomastrum. To complete our generic realignment, a total of 42 new combinations are effected at the species level and below, and a key is provided for the 12 genera presently recognised in African Melastomateae. Denser taxonomic sampling and sequencing of more loci will be needed to resolve relationships within the large clade of Dissotis s.str. and allies (including Antherotoma as well as three West African species erroneously placed in the otherwise Asian Osbeckia).

American Journal of Botany 101(7): 1102–1126, 2014. PHYLOGENY AND GENERIC LIMITS IN THE SISTER TRIBES PSYCHOTRIEAE AND PALICOUREEAE (RUBIACEAE): EVOLUTION OF SCHIZOCARPS IN PSYCHOTRIA AND ORIGINS OF BACTERIAL LEAF NODULES OF THE MALAGASY SPECIES1 SYLVAIN G. RAZAFIMANDIMBISON2,5, CHARLOTTE M. TAYLOR3, NIKLAS WIKSTRÖM2, THIERRY PAILLER4, ANBAR KHODABANDEH2, AND BIRGITTA BREMER2 2The Bergius Foundation at The Royal Swedish Academy of Sciences and Department of Ecology, Environment and Plant Sciences, Stockholm University, SE-106 91 Stockholm, Sweden; 3Missouri Botanical Garden, P. O. Box 299, St. Louis, Missouri 63166-0299 USA; and 4UMR C53, Peuplements végétaux et Bioagresseurs en milieu tropical, Faculté des Sciences et Technologies, Université de La Réunion, 15 Avenue Réné Cassin, BP 7151 97715 Saint-Denis Cedex 9, La Réunion, France • Premise of the study: The pantropical, species-rich Psychotrieae and Palicoureeae are sister tribes of mostly drupe-bearing and nonbacterial leaf-nodulating species with problematic generic limits. This problem is more complicated in Psychotrieae due to the paraphyly of the genus Psychotria, the lack of diagnostic characters for some major lineages, and the poor sampling from some biodiversity hotspots. Schizocarps and bacterial leaf nodules have been used for recognizing formal groups in Psychotrieae, but their evolution and taxonomic value have not been studied using a robust phylogeny of the tribe. • Methods: We analyzed 287 samples from the entire ranges of the tribes, with particular emphasis on the Western Indian Ocean region, with the Bayesian Markov chain Monte Carlo method. • Key results: All allied Psychotria genera investigated are nested within a paraphyletic Psychotria. Schizocarps evolved independently two times within Psychotria, and one reversal back to the drupaceous condition is inferred. The Malagasy leafnodulated Psychotrieae (except Apomuria bullata) and the Comorian non-leaf-nodulated Psychotria conocarpa are nested within the (African) leaf-nodulated clade. Within Palicoureeae, Chassalia is paraphyletic with respect to Geophila sensu stricto, and the Malagasy Geophila gerrardii and the African Hymenocoleus are closely related. • Conclusions: A widely circumscribed Psychotria encompassing the entire Psychotrieae is supported. Within Psychotria, two separate origins of schizocarps from drupes, one reversal back to the drupaceous condition, and two independent origins of the Malagasy leafnodulated species are inferred. A new genus Puffia is described to accommodate Geophila gerrardii, and a narrow circumscription of Chassalia is adopted. Thirty-two new combinations, two lectotypifications, and 25 new names are presented. Key words: bacterial nodules; Madagascar; Psychotrieae alliance; Rubiaceae; schizocarp; systematics; taxonomy; Western Indian Ocean region. The Psychotrieae alliance as defined by Razafimandimbison et al. (2008) belongs to the subfamily Rubioideae of the coffee family (Rubiaceae) and is a species-rich pantropical group. Our understanding of the systematics of the group has progressed greatly (e.g., Bremer and Manen, 2000; Robbrecht and Manen, 2006; Rydin et al., 2008). The current circumscription of the alliance sensu Razafimandimbison et al. (2008) contains about 3400 species of predominantly woody plants, which are formally classified in nine morphologically distinct tribes: Craterispermeae Verdc., Gaertnereae Bremek. ex Darwin, Mitchelleae 1 Manuscript received 25 February 2014; revision accepted 22 May 2014. The authors thank the following herbaria staff for allowing access to their collections: BR, GB, K, MAU, MO, NOU, P, S, SEY, TAN, TEF, and UPS; the DGF (Direction Générale des Forêts) and MNP (Madagascar National Parks) in Madagascar for issuing collecting and exportation permits for S.G.R.; the Missouri Botanical Garden, Madagascar Program for logistical support; the Parc Botanique et Zoologique de Tsimbazaza and the Missouri Botanical Garden, Madagascar Program (F. Lantoarisoa) for arranging collecting and exportation permits for S.G.R.; the Mauritian, Reunionese, and Seychellois authorities for approving our research proposals to collect Rubiaceae in their respective countries; C. Baider and V. Florens for kindly organizing our field collecting on Mauritius; K. Beaver for arranging a collecting permit for S.G.R. and B.B.; B. Senterre and C. Kaiser-Bunbury for their precious help to find Razafim. & B.Bremer, Morindeae Miq., Palicoureeae Robbr. & Manen, Prismatomerideae Ruan, Psychotrieae Cham. & Schltdl., Schizocoleeae C.Rydin & B.Bremer, and Schradereae Bremek. The tribes Palicoureeae and Psychotrieae include about 91% of the species of the Psychotrieae alliance and about 24% of Rubiaceae as a whole. Members of these groups of plants are very important components of various terrestrial ecosystems throughout the tropics. Their fleshy, drupaceous fruits are an important resource for many frugivorous, tropical birds and mammals, and a considerable variation in fruit texture and color Rubiaceae on Mahé (Seychelles); the Seychelle National Herbarium (SEY) at the Natural History Museum (Mahé, Seychelles); L. Barrabé, A. Davis, and A. Mouly for kindly providing material (DNA and/or leaf fragments); S. Malcomber for sharing a photo of Chassalia sp.-ck25; K. Kainulainen for technical help and comments on an earlier version of the manuscript; two anonymous reviewers and the Associate Editor (M. Simmons) for their constructive comments on an early version of the paper; and the Swedish Research Council and the Knut and Alice Wallenberg Foundation for financial support to B.B. and the Royal Swedish Academy of Sciences (FOA13H099-A) to S.G.R. 5 Author for correspondence (e-mail: sylvain@bergianska.se) doi:10.3732/ajb.1400076 American Journal of Botany 101(7): 1102–1126, 2014; http://www.amjbot.org/ © 2014 Botanical Society of America 1102 July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE attracts different animal dispersers (Herrera, 1989). On the other hand, relationships between most members of these tribes are still unknown partly due to the poor or lack of sampling from some biodiversity hotspots. Schizocarpous fruits and bacterial nodules have been used for recognizing formal groups in the mostly drupe-bearing and non-leaf-nodulated Psychotrieae. However, the evolution and taxonomic value of these characters have not been addressed based on a broadened sampling of the tribe. This study presents a robust phylogenetic framework for establishing new generic circumscriptions of the sister tribes. It allows us to have a better understanding of the evolution of schizocarpous fruits from fleshy, drupaceous fruits (or vice versa) and also sheds light on the origins of bacterial leaf nodules of the Malagasy Psychotria species. Earlier circumscriptions of Psychotrieae were all mainly based on morphological characters (Hooker, 1873; Müller, 1881; Schumann, 1891; Verdcourt, 1958; Petit, 1964, 1966; Bremekamp, 1934, 1966; Steyermark, 1972; Robbrecht, 1988; Taylor, 1996); however, none of these circumscriptions are supported as monophyletic by molecular data (Andersson and Rova, 1999; Bremer and Manen, 2000; Robbrecht and Manen, 2006; Bremer and Eriksson, 2009; Barrabé et al., 2014). The tribe has generally been characterized within Rubiaceae by the presence of raphides in tissues; usually bilobed stipules; corolla lobes valvate in bud; ovules that are solitary, anatropous, and basal in each locule; and fleshy, drupaceous fruits with each of the pyrenes being 1-seeded. Recently, Psychotrieae have been more narrowly delimited because a number of genera traditionally associated with the tribe, mainly because of their fleshy drupaceous fruits, have been found to be more closely related to genera of other tribes in Rubioideae. As a result, many genera have been excluded from Psychotrieae: Lasianthus Jack, Ronabea Aubl., and their allied genera with more than seven locules were transferred to the tribe Lasiantheae Bremer & Manen (Bremer and Manen, 2000; Taylor, 2004); Damnacanthus F.C.Gaertn. and Mitchella L. with campylotropous ovules to Mitchelleae (Razafimandimbison et al., 2008); Morinda L. and its allied genera with two ovules in each locule and mostly multiple fruits to Morindeae (Bremer and Manen, 2000; Razafimandimbison et al., 2009); Colletoecema E.M.A.Petit with axillary inflorescences to Colletoecemateae Rydin & B.Bremer (Rydin et al., 2008); and Gaetrnera Lam. and Pagamea Aubl. with inferior ovaries to Gaertnereae (Bremer and Manen, 2000). The transfer of these genera reduced the variation in the morphological characters of Psychotrieae, leaving a clade that is well supported by molecular data (e.g., Robbrecht and Manen, 2006; Bremer and Eriksson, 2009). Molecular phylogenetic analyses have generally resolved the members of this recircumscribed Psychotrieae into two species-rich sister lineages, both morphologically distinct and with pantropical distributions (e.g., Andersson and Rova, 1999; Nepokroeff et al., 1999; Robbrecht and Manen, 2006). These groups have informally been called the Psychotria complex or group and the Palicourea complex or group (Andersson and Rova, 1999; Nepokroeff et al., 1999; Andersson, 2002a) and formally treated as the tribes Psychotrieae and Palicoureeae (Robbrecht and Manen, 2006), respectively. When Palicoureeae is separated (Robbrecht and Manen, 2006), its sister tribe has sometimes been called Psychotrieae sensu stricto (Razafimandimbison et al., 2008). These sister tribes differ generally in their stipules, which are characteristically deciduous in Psychotrieae and persistent or marcescent in Palicoureeae; their pyrenes, entire vs. with various preformed germination slits (PGS), respectively; their seed 1103 coats, with an ethanol-soluble red pigment vs. without, respectively; and their drying color, characteristically brown to gray vs. green, respectively (Robbrecht and Manen, 2006). In addition to these morphological differences, Palicoureeae are apparently characterized biochemically by the presence of cyclotides. These are proteins known to have a wide range of biological activities, and although sampling so far has been limited, these cyclotides have not been found in Psychotrieae (Koehbach et al., 2013). Psychotrieae (sister to Palicoureeae) are mainly centered in the paleotropics and include at least 1600 species. The tribe is well delimited (e.g., Andersson, 2002b; Robbrecht and Manen, 2006; Razafimandimbison et al., 2008), but its generic limits remain unsettled. Some of the genera currently recognized, in particular Amaracarpus Blume, Calycosia A.Gray, Dolianthus C.H.Wright, Hedstromia A.C.Sm., and Hydnophytum Jack (and its closely related genera), have been shown to be nested within Psychotria L. (Nepokroeff et al., 1999; Andersson, 2002b; Robbrecht and Manen, 2006; Bremer and Eriksson, 2009; Barrabé et al., 2014), rendering the latter genus paraphyletic. Many lineages have been identified within Psychotrieae (Nepokroeff et al., 1999; Andersson, 2002b; Barrabé et al., 2014), but the lack of diagnostic characters or geographic separation for most of these groups is problematic. Furthermore, representatives of Psychotrieae from some of the world’s biodiversity hotspots (Davis et al., 2009), in particular Madagascar and its surrounding archipelagoes and the Indian subcontinent (from Afghanistan through India to Myanmar and Sri Lanka), have been sampled poorly, or not at all, in previous molecular phylogenetic studies. The relationships of these species are therefore unknown, and previous sampling of Psychotria is clearly inadequate to support conclusions about the whole genus. Beside the paraphyly of Psychotria, there is also controversy about whether the genus should be circumscribed in a narrow (Andersson, 2002b) or broad sense (e.g., Nepokroeff et al., 1999; Robbrecht and Manen, 2006). Many rubiaceous genera, including Camptopus Hook.f., Grumilea Gaertn., and Mapouria Aubl., have long been considered synonyms of Psychotria, and these taxonomic decisions have been supported by molecular data (e.g., Nepokroeff et al., 1999; Andersson, 2002b; Barrabé et al., 2014). On the other hand, the types of Camptopus (Camptopus mannii Hook.f., now Psychotria camptopus Verdc.) and Grumilea [Grumilea nigra Gaertn., now Psychotria nigra (Gaertn.) Alston] have not previously been included in molecular phylogenetic studies of Psychotrieae. Furthermore, the identity of the type of Psychotria was controversial, because Linnaeus’ (1759) description of his Psychotria asiatica L. was based on a mixture of two elements belonging to the Jamaican genus Psychotrophum P. Browne (Browne, 1756) (now Psychotria brownei Spreng.) and the Asian P. asiatica (e.g., Bremekamp, 1961; Petit, 1964; Davis et al., 2001). Petit (1964) clarified that P. asiatica is the type of Psychotria by designating the specimen Herb. Linn. No. 231.1 (LINN) as the lectotype of Psychotria. Davis et al. (2001) resolved the problem of the heterogeneous elements in P. asiatica by lectotypifying it on the Asian element (see Davis et al., 2001 for more details). The name Psychotria was conserved against the generic names Psychotrophum and Myrstiphyllum P. Browne (Browne, 1756). Palicoureeae, as delimited by Robbrecht and Manen (2006), have its center of diversity in the neotropics and include at least 1500 species currently classified in eight genera: the neotropical 1104 AMERICAN JOURNAL OF BOTANY genus Carapichea Aubl. with 23 species (Andersson, 2002a; Taylor and Gereau, 2013); the neotropical Notopleura (Hook.f.) Bremek. with ca. 210 species (e.g., Taylor, 2001); the neotropical Palicourea Aubl., which includes many of the species of Psychotria subgenus Heteropsychotria Steyerm. and Cephaelis Sw., with ca. 800 species (e.g., Taylor et al., 2010); the neotropical Rudgea Salisb. with at least 200 species; the paleotropical Chassalia Comm. ex Poir. with ca. 140 species (Bremekamp, 1962; Verdcourt, 1976 , 1983 ; Piesschaert et al., 1999a , b ; Lachenaud and Harris, 2010; Lachenaud et al., 2012; Govaerts et al., 2013); the African Hymenocoleus Robbr. with 13 species (Robbrecht, 1975, 1977); the pantropical Geophila D.Don with about 24 species (e.g., Bremekamp, 1963; Burger and Taylor, 1993; Dessein et al., 2011); and the pantropical Margaritopsis C.Wright (including the neotropical Chytropsia Bremek., the African Chazaliella E.M.A.Petit & Verdc., and the Fijian Readea Gillepsie) with about 80 species (Andersson, 2002a; Taylor, 2005; Barrabé et al., 2012). Palicoureeae sensu Robbrecht and Manen (2006) were supported by Barrabé et al. (2012) based on sequence data from five gene regions. That study mainly addressed the status of Margaritopsis and produced a fully resolved and well-supported phylogeny of the tribe, with the exception of a poorly supported sister-group relationship between Carapichea and Margaritopsis. The genus Chassalia was supported as monophyletic. However, their sampling was not consistently deep across the tribe, and the monophyly of the Palicoureeae genera has yet to be tested with a broadened sampling of the tribe. The Indian Ocean region encompasses many islands of various sizes and ages, with extraordinary levels of diversity and endemism of plants and animals (e.g., Agnarsson and Kuntner, 2012). Madagascar and the nearby Comore, Mascarene, and Seychelle archipelagoes are situated in the Western Indian Ocean region (WIOR), where Psychotrieae have twice as many species (Bremekamp, 1963; Friedmann, 1994) than Palicoureeae (represented by Chassalia with 68 species [Bremekamp, 1962; Verdcourt, 1983, 1989] and Geophila with two species [Bremekamp, 1963]). There are about 157 described species (mostly Malagasy endemics) of Psychotrieae in the WIOR, and these species have been classified in seven genera (Bremekamp, 1958, 1960, 1963; Verdcourt, 1983, 1989; Friedmann, 1994; Davis et al., 2007): Psychotria (44 species); Mapouria (67 species); the Malagasy-Comorian-Eastern African Apomuria Bremek. (13 species); the Malagasy-Comorian-New Caledonian Cremocarpon Boiv. ex Baill. (10 species); the MalagasyMascarene-Seychellois Psathura Comm. ex Poir. (8 species); the Malagasy Pyragra Bremek. (2 species); and the MalagasyComorian Trigonopyren Bremek. (9 species). Davis et al. (2007) transferred all of Bremekamp’s (1963) Mapouria species from Madagascar and the Comores to Psychotria. Trigonopyren is diagnosed by its pyrenes with smooth surfaces and three-angled in cross section, while Apomuria can be recognized by its seeds with nonruminate endosperm and a T-shaped longitudinal intrusion on the adaxial face (Bremekamp, 1963). Psathura is distinct by its ovaries and fruits with three to six locules and pyrenes (Bremekamp, 1963; Verdcourt, 1983, 1989; Friedmann, 1994). Cremocarpon and Pyragra differ from the other genera in the WIOR by their dry, schizocarpous fruits. Each schizocarp is formed by two mericarps, that disperse separately along with their covering mesocarps and endocarps, leaving behind a Y-shaped carpophore that becomes hardened and supports the mericarps from their adaxial surfaces. Pyragra is diagnosed by its markedly flatttened mericarps with [Vol. 101 the abaxial side deeply ridged and thin to winged margins as opposed to planoconvex to ellipsoid mericarps with the abaxial side weakly to markedly ridged and nonwinged margins in Cremocarpon (Bremekamp, 1958). The generic status of all these genera has been questioned by some authors (e.g., Piesschaert, 2001; Schatz, 2001; Davis et al., 2007), as they appear to fall within Psychotria’s limits based on their general morphology. Before this study less than 1% of Psychotrieae and Palicoureeae species from Madagascar had been included in previous molecular systematic studies (e.g., Andersson, 2002b; Lemaire et al., 2011, 2012a), and no species from the neighboring islands had been sequenced. More variation than recognized by Bremekamp (1958, 1963) in fruit characters has now been documented in Rubiaceae, in particular within the lineages and individual species of Psychotrieae (Piesschaert, 2001) and Palicoureeae (Piesschaert et al., 1998; Piesschaert, 2001; Taylor and Gereau, 2013). Schizocarps have evolved independently numerous times in different lineages of the angiosperms, e.g., Apiaceae, Araliaceae, Rosaceae, Rubiaceae. This type of dry fruit is presently known to occur in seven distantly related tribes of Rubiaceae: Naucleeae (Cephalanthus L., Razafimandimbison and Bremer, 2002); Sabiceeae (Hekistocarpa Hook.f., Khan et al., 2008); Trailliaedoceae (Trailliaedoxa W.W.Sm. & Forrest, Kainulainen et al., 2013); Knoxieae (Knoxia L., Kårehed and Bremer, 2007 ); Psychotrieae (Cremocarpon, Pyragra, Psychotria, Bremekamp, 1958; Barrabé et al., 2014); Rubieae (Galium L., Soza and Olmstead, 2010); and Spermacoceae [Diodella Small, Richardia Kunth., Diplophragma (Wight & Arn.) Meisn, Wikström et al., 2013 ]. This repeated pattern indicates multiple origins of schizocarpous fruits within the family. The occurrence of schizocarpous fruits within the mostly drupe-bearing Psychotrieae is interesting from an evolutionary standpoint. It has been shown by Andersson (2002b) and more recently by Barrabé et al. (2014) that the New Caledonian Cremocarpon rupicolum Baill. belongs in Psychotria (= Psychotria rupicola (Baill.)Schltr.) and that it is closely related to the New Caledonian Psychotria comptonii S.Moore and P. declieuxioides S.Moore (Barrabé et al., 2014). These latter species also have schizocarpous fruits but have consistently been classified in Psychotria. These findings imply that the generic status of Cremocarpon and Pyragra, which have been based on this fruit character (Bremekamp, 1958, 1963), needs a re-evalution. Schatz (2001, p. 338) recognized a broadly delimited Psychotria (including Cremocarpon and Pyragra), and argued that “…it might be more reasonable to accept the phenomenon of pyrenes drying and falling away separately as a secondary fruiting characteristic within Psychotria.” In other words, he considered Cremocarpon and Pyragra to be Psychotria with secondarily dehiscent fruits, in which initially fleshy drupaceous fruits ultimately dry out when they are fully mature. This hypothesis, if correct, would imply that the schizocarpous fruits of these genera have evolved from ancestors with fleshy, drupaceous fruits. A distinctive character that has not always been considered synapomorphic in Psychotria is the presence of bacterial leaf nodules (e.g., Hiern, 1877; Bremekamp, 1963). Bacterial symbiosis in the form of leaf nodules has been recorded in about 500 species of Rubiaceae and in the family Primulaceae (Miller, 1990). The symbionts are known to play an important role for the survival of their plant hosts (e.g., Lemaire et al., 2011, 2012a, b). Within Rubiaceae, all leaf-nodulated species belong to Psychotria and Apomuria (Psychotrieae) and the genera July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE Pavetta L. (tribe Pavetteeae) and Sericanthe Robbr. (tribe Coffeeae), both in the subfamily Ixoroideae (now Dialypetalanthoideae, Reveal, 2012) (Robbrecht, 1988; Lemaire et al., 2011, 2012a, b). The leaf-nodulated species of Rubiaceae are solely found in tropical Africa and the WIOR, with those of Psychotria (about 80 species, Lemaire et al., 2012b) distributed in tropical Africa, the Comores, and Madagascar (Bremekamp, 1960, 1963; Petit, 1964; Verdcourt, 1975, 1976). The bacterial nodules of the African and Comorian species are small and round to linear (Petit, 1964), while those of the species found in Madagascar vary from small and round to variously linear, branched, and/or reticulated (Bremekamp, 1960). Bremekamp (1960) studied a morphologically similar group of the leafnodulated Malagasy Psychotria species and postulated that these might represent a different genus, but never proposed a formal name for this group. Later, Bremekamp (1963) explicitly included an East African-Comorian leaf-nodulated species in Apomuria, A. punctata (Vatke) Bremek., and also added there a Malagasy leaf-nodulated species, A. bullata Bremek., though without noting its leaf nodules. Subsequently, Petit (1964) considered these leaf nodules an evolutionarily important character. The leaf-nodulated Psychotria species from continental Africa were then separated taxonomically in Psychotria subgenus Tetramerae (Hiern) E.M.A.Petit, without mention of the leaf-nodulated species from other areas (Psychotria subg. Tetramerae was based on Psychotria sect. Tetramerae Hiern, which was diagnosed by its four-merous flowers and included species both with and without bacterial nodules, while some species with bacterial nodules were classified by Hiern [1877] in other sections). The leaf-nodulated Psychotrieae species found in Madagascar are endemic to the island, and their placements in two different genera, Apomuria and Psychotria (Bremekamp, 1963), imply two independent origins of the Malagasy leafnodulated Psychotrieae. The objectives of this study are to produce an expanded, more robust phylogeny of the sister tribes Psychotrieae and Palicoureeae, and use this phylogeny to (1) test the generic status of the WIOR genera of Psychotrieae and re-assess the delimitation of Psychotria; (2) re-evaluate the generic limits and relationships within Palicoureeae, in particular Chassalia, Geophila, and Margaritopsis; (3) trace the evolution of schizocarpous fruits within Psychotria and evaluate its taxonomic value; and (4) test whether the Malagasy leaf-nodulated species of Psychotria and Apomuria evolved independently from their African counterparts. MATERIALS AND METHODS Taxon sampling—The present study included a total of 287 samples (see Appendix 1), of which 156 represent 135 species from Psychotrieae and 118 represent 107 species and eight genera from Palicoureeae. Taxa were selected to obtain a broad sampling of putative members of the two tribes across their respective geographic ranges, with particular emphasis on the WIOR. In total, we investigated about 105 species of the Psychotrieae and Palicoureeae genera found in the WIOR. The types of Camptopus (C. mannii = Psychotria camptopus) and Grumilea (G. nigra = Psychotria nigra) were also included. For Palicoureeae, 65 species of Chassalia (about 36 species from Madagascar, about 13 species from Africa, about 10 species from Asia, all the six species from Mauritius (including the type Chassalia capitata DC.), two species each from Reunion Island and the Comores), and seven species of Geophila (including the Malagasy Geophila gerrardii Baker) were sequenced. Eleven species from the remaining tribes of the Psychotrieae alliance were sampled, and two species from the Rubioideae tribes Colletoecemeae and Ophiorrhizeae were used as outgroup taxa to root the trees. 1105 DNA extraction, amplification, and sequencing—We used sequence data from the nuclear ribosomal nrETS and nrITS regions and the plastid atpB-rbcL, ndhF, rbcL, rps16, and trnT-F regions, as they were proven to be useful for inferring phylogenetic relationships within the Psychotrieae alliance (Razafimandimbison et al., 2008, 2009). Total DNA, extracted from leaves dried in silica gel (Chase and Hills, 1991) and/or herbarium material, was isolated following the mini-prep procedure outlined in Saghai-Maroof et al. (1984) and modified by Doyle and Doyle (1987). Isolated DNA was amplified and sequenced following the protocols outlined in the following articles: Razafimandimbison et al. (2009) for nrETS, Razafimandimbison et al. (2004) for nrITS, Rydin et al. (2008) for atpB-rbcL, Oxelman et al. (1997) for rps16, Olmstead and Reeves (1995) for ndhF, Bremer et al. (1995) for rbcL, and Razafimandimbison and Bremer (2002) for trnT-F. The same primers as for PCRs were used for sequencing reactions, which were sent to the Macrogen Europe (Amsterdam, Netherlands) for sequencing. Phylogenetic analyses—Sequence data were assembled using the Staden package v. 2.0.0b9 (Staden, 1996). For each marker, all newly generated sequences and published ones from GenBank were aligned with the computer program MUSCLE v.3.8.31 (Edgar, 2004). Manual adjustments were done following similarity criterion (Simmons, 2004) using the software SeAl v. 2.0 (Rambaut, 1996) for the atpB-rpcL, rps16, and trnT-F matrices. In all alignments, gaps were treated as missing data, and the aligned matrices were analyzed using Bayesian Markov chain Monte Carlo (MCMC) methods. Inferred indels/deletions were not coded as separate characters, and sites considered ambigously aligned in the rps16 and trnT-F regions were excluded from the analyses. We performed separate and combined Bayesian MCMC analyses (Yang and Rannala, 1997) of the data sets using MrBayes 3.1.2 (Huelsenbeck and Ronquist, 2001; Ronquist and Huelsenbeck, 2003). The combined plastid and nuclear matrix is available as supplemental data (Appendix S1, see Supplemental Data with the online version of this article). The best-fit nucleotide substitution models for each data set, the combined nuclear (nrETS+nrITS), the combined coding plastid (ndhF+rbcL), and the combined noncoding plastid (atpB-rbcL+rps16+trnT-F) data, were selected using the computer program MrAIC v. 1.4.4. (Nylander, 2004). We estimated the best performing evolutionary models under three different model selection criteria: Akaike information criterion (AIC) (Akaike, 1973), AICc (a second order AIC, necessary for small samples), and the Bayesian information criterion (BIC) (Schwarz, 1978). We performed two parallel runs of the Bayesian MCMC analyses of each data set and the combined nuclear and plastid data sets with six independent Markov chain runs (only four chains for the separate Bayesian MCMC analyses) for 20 × 106 Metropolis-coupled MCMC generations (only 5 × 106 generations for the separate Bayesian MCMC analyses), with tree sampling every 1 × 103 generations, and the temperature coefficient of the chain-heating scheme set to 0.20. For the combined Bayesian MCMC analysis, we divided the aligned sequence data from the seven markers in three partitions; therefore, we applied the GTR+G+I model to the combined coding plastid and the combined noncoding plastid data and the SYM+G+I model to the combined nuclear data. For all analyses, we checked stationary and convergence of runs and the correlation of split frequencies between the runs using the program AWTY (Nylander et al., 2008). The effective sample size (ESS) of parameters was also monitored using the program Tracer v. 1.5.0 (Rambaut and Drummond, 2009). Trees sampled before the Bayesian posterior probability (BPP) of splits stabilized were excluded as a burn-in phase. All saved trees from the two independent runs were subsequently pooled for a consensus tree. Ancestral state reconstruction—We reconstructed ancestral character states for the fruit types of Palicoureeae and Psychotrieae, which were coded as follows: fleshy, drupaceous fruits = 0 and schizocarpous fruits = 1. One thousand trees were randomly selected from postburn-in trees produced from the two parallel runs of the MrBayes analysis based on the combined nuclear and plastid data. Ancestral reconstruction states of the fruit types across these trees were inferred using the maximum likelihood Mk1 model (with equal probability of change between states), as implemented in the computer program Mesquite v2.74 (Maddison and Maddison, 2010). Results were subsequently plotted on the 50% Bayesian majority rule consensus tree generated from the combined data. RESULTS Information about all sequence data from the seven markers is summarized in Table 1. A total of 596 base pairs (bp) from the rps16 and trnT-F data sets were excluded, as they were 1106 [Vol. 101 AMERICAN JOURNAL OF BOTANY TABLE 1. Characteristics of the markers/data sets used, including statistics of alignments and evolutionary models suggested by MrAIC v.1.4.4. (Nylander, 2004). Data sets Number of taxa included in each matrix Number of sequences in the matrices Number of missing sequences in the matrices Number of new sequences in the matrices Length of aligned matrices (bp) Best-fit nucleotide substitution models Best-fit nucleotide substitution models nrETS nrITS ndhF rbcL atpB-rbcL rps16 trnT-F Combined data sets 287 204 83 287 260 27 287 237 50 287 230 57 287 215 72 287 267 20 287 256 31 287 1669 (83.08%) 340 (16.92%) 190 1509 GTR+G+I SYM+G+I 203 477 GTR+G+I 199 2118 GTR+G+I GTR+G+I 201 1353 GTR+G+I 193 774 HKY+G GTR+G+I 194 1635 HKY+G 201 2828 GTR+G 1381 (82.84%) 10 650 ambiguously aligned. The 50% Bayesian majority rule consensus trees generated from the separate Bayesian MCMC analyses of the seven data sets are presented as supplemental data (Appendices S2–S8, see online Supplemental Data). All plastid data sets resolve Psychotrieae and Palicoureae sensu Robbrecht and Manen (2006) as sisters (Appendices S2, S5–S8); however, Palicoureeae and the sister-group relationship between the two tribes collapse in both the ETS and ITS trees (Appendices S3, S4). A poorly supported clade formed by Rudgea and Palicourea sensu lato (BPP = 0.73) is sister to a poorly supported clade containing Psychotrieae and the remaining Palicoureeae (BPP = 0.8). In the ITS tree, Rudgea and the poorly supported clade formed by Carapichea and Palicourea sensu lato (BPP = 0.71) constitute a moderately supported clade with the strongly supported Psychotrieae (BPP = 0.87). We attribute these differences to the inability of the fast-evolving ETS and ITS regions to resolve deep nodes. Within Psychotrieae and Palicoureeae, the rps16, and trnT-F trees (Appendices S7, S8) are less resolved compared with the atpB-rbcL and rbcL trees (Appendices S2, S6). These latter two trees are in turn less resolved than the ndhF tree (Appendix S4). Both ETS and ITS data (Appendices S3, S4) provide a good resolution within Psychotrieae. Visual inspection of the seven trees (Appendices S2–S8) shows no strongly supported topological conflicts between them; accordingly, we merge the sequence data of these markers into a large combined matrix, which contains a total of 287 samples, 10 650 bp, and 1667 sequences. Of these, 1381 (82.84%) are new sequences published here (KJ804402–KJ805782, Appendix 1). A simplified Bayesian majority rule consensus tree generated from the combined nuclear and plastid data are depicted in Fig. 1, while the phylogenies of the tribes Psychotrieae and Palicoureeae from the same Bayesian tree are presented in Figs. 2 and 3, respectively. Within Psychotrieae, all allied genera of Psychotria investigated in this study (i.e., Amaracarpus, Calycosia, Dolianthus, Hydnophytum, and its satellite genera, Camptopus, represented by the type Camptopus mannii [= Psychotria camptopus, Fig. 2], Grumilea, including the type G. nigra [= Psychotria nigra, Fig. 2B], Mapouria, including the type M. guianensis Aubl. [= Psychotria mapourioides DC., Fig. 2G], and the WIOR genera Apomuria, Cremocarpon, Psathura, Pyragra, and Trigonopyren]) are nested within what would be a broadly defined Psychotria. In other words, Psychotria is highly paraphyletic if these genera are accepted (Fig. 2). This widely delimited Psychotria is resolved in seven highly major lineages Figs. 1, 2): the Pacific Psychotria clade (BPP = 1; = Pacific clade sensu Nepokroeff et al. [1999]); the Indian-Sri Lankan Psychotria clade (BPP = 1); the WIOR Psychotria clade (BPP = 1); the Australasian Psychotria clade (BPP = 1; = the Psychotria clade IV sensu Andersson [2002b]); the Afro-neotropical Psychotria clade (BPP = 1; = the Psychotria clade I sensu Andersson [2002b]); the AfroWIOR Psychotria clade or the leaf-nodulated Psychotria clade (BPP = 1; = the Psychotria clade II sensu Andersson [2002b]); and the Afro-Asian-WIOR-neotropical Psychotria clade (BPP = 1; = the Psychotria clade III sensu Andersson [2002b]). The phylogenetic relationships between these lineages are partly resolved. The Afro-neotropical Psychotria clade (Figs. 1E–2E) is resolved as sister to the Afro-WIOR Psychotria clade (Figs. 1F– 2F); the Afro-Asian-WIOR-neotropical Psychotria clade (Figs. 1G–2G) is in turn sister to a clade formed by the Afro-neotropical Psychotria and the Afro-WIOR Psychotria clades. The Pacific Psychotria clade (Fig. 2A) comprises all sequenced species of Calycosia, Hydnophytum, Myrmecodia, Dolianthus, and Amaracarpus, one Psychotria species from Caroline Island, and two Psychotria species from New Guinea. All sampled Sri Lankan and Indian species of Psychotria are grouped together in the Indian-Sri Lankan Psychotria clade (Fig. 2B). The WIOR Psychotria clade is resolved in three major groups (Fig. 2C): the Cremocarpon clade formed by the two recognized species of Pyragra and six sampled species of Cremocarpon, including the type C. boivinianum Baill. from the Comores (BPP = 0.88); a group comprising three samples of the Malagasy Cremocarpon lantzii (BPP = 1); and a large clade formed by species of Psychotria from Madagascar, the Comores, and the Seychelles, the leaf-nodulated Apomuria bullata, and the sampled species of Psathura, and Trigonopyren (BPP = 1). Within this large clade, Trigonopyren, represented by three species, is resolved as monophyletic, while Psathura, represented by six species, is not monophyletic. The Mascarene species of Psathura form a wellsupported clade, and the three Psychotria species from the Seychelles constitute another highly supported clade (Fig. 2C). Finally, all sequenced Malagasy and Comorian species of Psychotrieae are resolved in three distinct clades: the WIOR Psychotria clade (Fig. 2C), the Afro-WIOR Psychotria clade (Fig. 2F), and the Afro-Asian-WIOR-neotropical Psychotria clade (Fig. 2G). In contrast, all the species of Psychotrieae sampled from the Mascarenes and Seychelles are nested in the WIOR Psychotria clade (Fig. 2C). The Psychotrieae species from the neighboring islands of Madagascar (Comores, Mascarenes, and Seychelles) are closely related to their Malagasy counterparts. The only exceptions are the leaf-nodulated Apomuria punctata and the non-leaf-nodulated Psychotria conocarpa Bremek. from the Comores, which are nested within a well-supported African subclade (Psychotria leucopoda to Apomuria punctata-ai74, BPP = 1) of the Afro-WIOR Psychotria clade (Fig. 2F). Palicourea sensu lato (BPP = 1), the Notopleura-Rudgea clade (BPP = 1), Carapichea (BPP =1), and Margaritopsis July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE 1107 Fig. 1. A simplified Bayesian majority rule consensus tree of 287 samples from the sister tribes Palicoureeae and Psychotrieae based on combined data (without indels treated as missing data and all ambiguous sites from the rps16 and trnT-F data excluded) from five plastid (atpB-rbcL, ndhF, rbcL, rps16, and trnT-F) and two nuclear (nrETS and nrITS) gene regions, depicting the major lineages of the two tribes. COL = Colletoecemeae; CRA = Craterispermeae; GAE = Gaertnereae; MIT = Mitchelleae; MOR = Morindeae; OPH = Ophiorrhizeae; PRI = Prismatomerideae; SCHI = Schizocoleeae; SCHR = Schradereae. sensu lato (BPP =1), respectively, form a basal grade in the well-supported tribe Palicoureeae (BPP = 1). Within the Notopleura-Rudgea clade, both Notopleura and Rudgea form wellsupported monophyletic groups (BPP = 1). Margaritopsis as delimited by Andersson (2001), endorsed by Taylor (2005), and Barrabé et al. (2012), including Chazaliella and Readea, represented by the type Readea membranacea (= Margaritopsis membranacea (Gillepsie) L. Andersson, Fig. 3), receives high support and is resolved as sister to a large clade formed by Hymenocoleus, Geophila gerrardii, and Chassalia sensu lato (Fig. 3). The African Chazaliella is paraphyletic with respect to Margaritopsis. Geophila is not resolved as monophyletic, as the endemic Malagasy species G. gerrardii forms a strongly supported clade (BPP = 1) with the African genus Hymenocoleus, represented by two species [H. hirsutus (Benth.) Robbr. and H. scaphus (K.Schum.) Robbr.]. The remaining sampled species of Geophila form a highly supported monophyletic group (hereafter called Geophila sensu stricto, BPP = 1), which in turn is nested within a well-supported Chassalia (Fig. 3), rendering the latter paraphyletic. Geophila sensu stricto is resolved as sister to a large Chassalia clade (hereafter called Chassalia sensu stricto, Fig. 3) formed by all sampled Chassalia from the WIOR, tropical Asia (except Chassalia sp.-ck25), and tropical Africa, with the exceptions of the East African C. albiflora K.Krause, C. kenyensis Verdc., C. parvifolia K.Schum., C. subochreata (De Wild.) Robyns, and C. violacea K.Schum. var. violacea. These last five East African Chassalia species form a well-supported clade (hereafter called the East 1108 AMERICAN JOURNAL OF BOTANY [Vol. 101 Fig. 2. A detailed phylogeny of the tribe Psychotrieae, representing part of the 50% Bayesian majority rule consensus tree retrieved from the Bayesian MCMC analyses of the combined data sets of 287 samples from the sister tribes Palicoureeae and Psychotrieae. Values above nodes are Bayesian posterior probabilities. Taxa in boldface are types. Pie diagrams represent relative support for alternative character states. July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE 1109 Fig. 3. A detailed phylogeny of the tribe Palicoureeae, representing part of the 50% Bayesian majority rule consensus tree retrieved from the Bayesian MCMC analyses of the combined nuclear and plastid data of 287 samples from the sister tribes Palicoureeae and Psychotrieae. Values above nodes are Bayesian posterior probabilities. Taxa in boldface are types. 1110 AMERICAN JOURNAL OF BOTANY African Chassalia clade, Fig. 3), which is sister to a large Chassalia-Geophila clade formed by Geophila sensu stricto and Chassalia sensu stricto. Finally, the Southeast Asian Chassalia sp.-ck25, the East African Chassalia clade, and Geophila sensu stricto are successive sisters to Chassalia sensu stricto, and form a basal grade within a broadly delimited Chassalia (= Chassalia sensu lato, Fig. 3). Within Geophila sensu stricto, all sampled Geophila repens (L.) I.M.Johnst. var. repens from the paleotropics (Madagascar, Ethiopia, the Cook Islands, and New Caledonia) and Carinta repens (G. Forst.) L.B.Sm. & Downs var. comorensis Bremek. from the Comores together form a highly supported group (BPP = 1), while the neotropical C. repens (G. Forst.) L.B.Sm. & Downs var. americana Bremek. groups with the three neotropical species of Geophila [G. cordifolia Miq., G. macropoda (Ruiz. & Pav.) DC., and G. tenuis (Müll.Arg) Standl.]. Geophila repens var. repens as recognized by Bremekamp (1963) is paraphyletic with respect to C. repens var. comorensis, which forms a well-supported clade with G. repens var. repens from Madagascar (Fig. 3). Within Psychotrieae, schizocarpous fruits have evolved independently two times from fleshy, drupaceous fruits: (1) once in the WIOR Psychotria clade, followed by a single reversal back to the drupaceous condition (Fig. 2C); (2) once in the Australasian Psychotria clade (Fig. 2D). The Cremocarpon clade and Cremocarpon lantzii, which form a basal grade within the WIOR Psychotria clade and are characterized by schizocarpous fruits, are inferred to have ancestors with schizocarpous fruits (Fig. 2C). Within the Australasian Psychotria clade (Fig. 2D), the sampled species of New Caledonian Psychotria with schizocarps constitute a highly supported monophyletic group (BPP = 1). Finally, all sampled Malagasy leaf-nodulated species of Psychotria form a poorly supported monophyletic group (BPP = 0.77), which is deeply nested within the otherwise African leaf-nodulated Psychotria clade (= the Afro-WIOR Psychotria clade, Fig. 2F). The only Psychotria species without leaf nodules nested within this clade is the Comorian Psychotria conocarpa. The other leaf-nodulated species studied, Apomuria bullata, is nested in the WIOR Psychotria clade (Fig. 2C). DISCUSSION Generic limits and relationships in Psychotrieae— Paraphyly of Psychotria—Before the present study, two circumscriptions of Psychotria had been proposed based on molecular phylogenetic studies (Nepokroeff et al., 1999; Andersson, 2002b). Nepokroeff et al. (1999) favored a broadly circumscribed Psychotria including members of the subtribe Hydnophytinae (Huxley and Jebb, 1991) of the tribe Psychotrieae. These authors suggested the exclusion of the neotropical Psychotria subgen. Heteropsychotria and its Psychotria sect. Notopleura, which were shown to be more closely related to the neotropical Palicourea and its allied genera (now formally classified in Palicoureeae) than to Psychotria sensu Nepokroeff et al. (1999). Andersson (2002b), however, rejected the broad Psychotria sensu Nepokroeff et al. (1999) and instead proposed a delimitation of the genus that excluded Hydnophytinae and restricted Psychotria to only the members of the Psychotria clades I–IV (these clades correspond to the major lineages shown in Fig. 2D–2G). Andersson (2002b) formally merged the genera Cremocarpon, Pyragra, and Apomuria in Psychotria. However, no representative from the latter two genera were [Vol. 101 included in his study, and the phylogenetic position of Cremocarpon within his Psychotria was unresolved. Our analyses confirm the paraphyly of Psychotria, because the genera Amaracarpus, Calycosia, Camptopus, represented by its type C. mannii (= P. camptopus), Dolianthus, Hydnophytum, Grumilea Gaertn., represented by the type G. nigra (= Psychotria nigra), Mapouria, and all the WIOR genera (Apomuria, Cremocarpon, Psathura, Pyragra, and Trigonopyren) are nested within a broadly defined Psychotria. Apomuria, Cremocarpon, and Psathura are found here to be para- or polyphyletic, which implies that the fruit, pyrene, and seed characters used by Bremekamp (1958, 1963) to circumscribe these genera are homoplasious. Amaracarpus, Pyragra, and Trigonopyren appear to be monophyletic; however, they are deeply nested within Psychotria. Our findings support the decision of Schatz (2001) and Andersson (2002b) to merge Apomuria, Cremocarpon, Pyragra, and Trigonopyren into Psychotria. Psathura was not investigated by Andersson (2002b); however, our analyses and that of Barrabé et al. (2014) support its inclusion in Psychotria as well. The results of the present study, coupled with that of Nepokroeff et al. (1999), Schatz (2001), Andersson (2002b), and Barrabé et al. (2014), support a broad circumscription of Psychotria, which includes all of its allied genera and thus comprises the entire tribe Psychotrieae. The members of the WIOR genera have not been formally transferred to Psychotria; therefore, the transfer of these species is done here. Andersson’s (2002b) decision to keep the generic status of Amaracarpus, Calycosia, Dolianthus, Hedstromia, and Hydnophytum and its satellite genera received no support from Barrabé et al. (2014) or this present study, because it does not render Psychotria monophyletic. Psychotria as broadly defined in this study contains at least 1600 described species and numerous additional undescribed ones. Psychotria could also be rendered monophyletic by restricting it to include solely the members of the Afro-Asian-WIORneotropical Psychotria clade (Figs. 1G–2G), to which the type P. asiatica belongs (Davis et al., 2001), and recognizing each of the other six major lineages (Figs. 1A–F, 2A–F) at the generic level. This solution is attractive given the size of Psychotria and the availability of generic names for several of the lineages: Hydnophytum for the Pacific Psychotria clade (Figs. 1A–2A), Grumilea for the Indian-Sri Lankan Psychotria clade (Figs. 1B–2B), Psathura for the WIOR Psychotria clade (Figs. 1C– 2C), and Psychotria for the Afro-Asian-WIOR-neotropical Psychotria clade (Figs. 1G–2G). Three new generic names would have to be described to accommodate the members of the Australasian Psychotria clade (Figs. 1D–2D), the Afroneotropical Psychotria clade (Figs. 1E–2E), and the Afro-WIOR Psychotria clade (= the leaf-nodulated Psychotria clade, Figs. 1F–2F). We are not in favor of this alternative, because finding characters to circumscribe some of the major lineages is very difficult, and dividing this large genus into multiple, also large genera would cause tremendous nomenclatural instability. Furthermore, the phylogenetic relationships among the major lineages of Psychotria are only partly resolved in this study and continue to be a major challenge. The Pacific Psychotria clade (BPP = 1, Figs. 1A–2A) is predominantly distributed in the Pacific (with the exception of New Caledonia, Barrabé et al., 2014), but also found in Thailand, the Indo-Malesian region, New Guinea, and Australia. This group contains more than 340 species (Barrabé, 2013; Barrabé et al., 2014), with a number of Psychotria species from Fiji, Hawaii, and New Guinea (Nepokroeff et al., 1999; Andersson, July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE 2002b; present study) plus a large number of species in the Pacific in Amaracarpus, Calycosia, Straussia (DC.) A. Gray, Hydnophytum and its allied genera, Dolyanthus, Eumorphanthus A.C.Sm., Hedstromia, and Streblosa Korth. The Indian-Sri Lankan Psychotria clade (BPP = 1, Figs. 1B–2B) comprises one species of Psychotria from India and two species from Sri Lanka, one of them the type of Grumilea (= Psychotria nigra). It is likely that many species of Psychotria from the Indian subcontinent belong to this group. The WIOR Psychotria clade (BPP = 1, Figs. 1C–2C) contains species from the Malagasy-Comorian Trigonopyren, the Malagasy-Comorian species of Cremocarpon, the Malagasy-Mascarene-Seychelles Psathura, the Malagasy genus Pyragra, the Malagasy, leafnodulated Apomuria bullata, many species of the Malagasy Psychotria, two Seychellois Psychotria species, and one Comorian species of Psychotria. The group contains about 90 species and has its center of species diversity in Madagascar. The Australasian Psychotria clade (BPP = 1, Figs. 1D–2D) is distributed in the Indo-Malesian region, the Pacific islands, and Australia (absent on New Zealand), and contains at least 140 species of erect shrubs and climbers with adventitious roots (Barrabé, 2013). The Afro-neotropical clade (BPP = 1, Figs. 1E–2E) has its center of species diversity in tropical Africa and the neotropics, but does not include all neotropical species of Psychotria. The Afro-WIOR Psychotria clade or the leafnodulated Psychotria clade (BPP = 1, Figs. 1F–2F) contains all remaining leaf-nodulated species of Psychotria sampled and the non-leaf-nodulated P. conocarpa from the Comores. Finally, the Afro-Asian-WIOR-neotropical Psychotria clade (BPP = 1, Figs. 1G–2G) is resolved in two major groups: a moderately supported group formed by some African, Asian, and neotropical species of Psychotria (including P. asiatica and P. mapourioides) and a well-supported group containing some Malagasy Psychotria species, one Comorian Psychotria species, and one African Psychotria species. The species in this latter group all have yellow flowers and are very diverse in Madagascar. Generic limits and relationships between and within the genera of Palicoureeae— In contrast to Psychotrieae, the current circumscription of Palicoureeae sensu Robbrecht and Manen (2006) that contains eight genera (Carapichea, Chassalia, Geophila, Hymenocoleus, Margaritopsis, Notopleura, Palicourea, and Rudgea) has been widely accepted (e.g., Gruber et al., 2008; Koehbach et al., 2013; Taylor and Gereau, 2013). On the other hand, this study clearly demonstrates that the monophyly and delimitations of these genera need to be rigorously tested with a robust phylogeny of the tribe based on a broadened sampling. Polyphyly of Geophila—Geophila is a pantropical genus of about 24 species (Piesschaert et al., 1998; Taylor et al., 2004; Dessein et al., 2011; Govaerts et al., 2013), which is characterized by creeping, stoloniferous, and herbaceous habit; cordate leaves; and red or black drupaceous fruits. Most species are found in tropical Africa and the neotropics; each region contains nine species. Five species occur in tropical Asia and one species, G. gerrardii, is endemic to Madagascar. The generic status of Geophila has never been questioned; however, its monophyly has not previously been tested with molecular data. The present study investigated seven species of Geophila (including the Malagasy G. gerrardii, and G. repens, represented by three varieties (var. repens, var. comorensis, and var. americana). Our analyses show that Geophila is monophyletic 1111 if the Malagasy G. gerrardii is excluded. This Malagasy plant forms a strongly supported clade with the African Hymenocoleus, and this clade is well separated from Geophila sensu stricto (Fig. 3). This relationship, although unexpected, is supported by morphological data. Both are creeping stoloniferous herbs that are rooted at nodes, bear 2–6 pairs of leaves on the erect short stems, and have bifid stipules, bifid stigmas, and orange (sometimes red or black in Hymenocoleus) drupaceous fruits. Geophila and Hymenocoleus were separated by Robbrecht (1975, 1977) based on the membranous sheaths inside the stipules of the latter, a feature also lacking in G. gerrardii. Geophila gerrardii and Geophila sensu stricto have isostylous flowers (e.g., Verdcourt, 1976; Burger and Taylor, 1993; Taylor et al., 2004), while Hymenocoleus has heterodistylous flowers (Robbrecht, 1975). Finally, G. gerrardii has orange fruits as opposed to red or black fruits in Geophila sensu stricto. As a consequence, we describe the new genus Puffia Razafim. & B.Bremer to accommodate the Malagasy G. gerrardii (see below). This genus is restricted to the littoral forests of southeastern Madagascar, whereas Hymenocoleus is exclusively tropical African. Paraphyly of Chassalia—Chassalia is a paleotropical genus comprising about 140 species of shrubs and small trees, along with a few lianas, and epiphytes (Bremekamp, 1962; Piesschaert et al., 1999a, b; Lachenaud and Harris, 2010; Lachenaud et al., 2012; Govaerts et al., 2013). There are at least 10 new undescribed species in Madagascar alone, making the WIOR one of the centers of species diversity of Chassalia with about 50% of its species (60 in Madagascar, six on Mauritius, and two species each on Reunion and the Comores). About 45 of the species described are restricted to the African mainland and 29 species to tropical Asia. Only one species is endemic to New Guinea. Chassalia is characterized by its persistent, indurated stipules; fleshy, brightly colored or white inflorescences axes; slightly curved corollas that are often winged in bud; pyrenes mostly with a large ventral excavation; and large porate or colpate pollen grains (Bremekamp, 1962; Piesschaert et al., 1999a, b). Within Palicoureeae, Chassalia has been previously shown to be closely related to Geophila and Hymenocoleus (Bremer, 1996; Andersson and Rova, 1999; Nepokroeff et al., 1999; Barrabé et al., 2012). However, only a very limited number of Chassalia species was investigated: one species each by Bremer (1996), Andersson and Rova (1999), and Razafimandimbison et al., 2008; three species each by Andersson (2001) and Robbrecht and Manen (2006); six species by Barrabé et al., (2012). Chassalia appeared to be highly polyphyletic in Robbrecht and Manen (2006), whereas the genus was resolved as monophyletic in Barrabé et al. (2012) (BS = 90; BPP = 1). These conflicting results render the monophyly of Chassalia as currently delimited questionable. Piesschaert (2001) reported four distinct types of pyrenes in Chassalia, raising doubts based on this about the monophyly of the genus. Chassalia as presently circumscribed is found to be paraphyletic in our analysis with respect to Geophila sensu stricto (G. gerrardii excluded) (BPP = 1). The Southeast Asian Chassalia sp.-ck25, the East African Chassalia clade, and Geophila sensu stricto, respectively, form a basal grade within what could be considered Chassalia in a broad sense (= Chassalia sensu lato, Fig. 3). Geophila sensu stricto is in turn sister to Chassalia sensu stricto (including C. capitata to which the type specimen of Chassalia belongs, Bremekamp, 1962). Therefore, the current circumscription of Chassalia cannot be retained. There are at 1112 AMERICAN JOURNAL OF BOTANY least two alternatives to render the genus monophyletic. One is to merge Geophila in Chassalia (= Chassalia sensu lato, Fig. 3), which would make Chassalia morphologically heterogeneous and therefore difficult to circumscribe. Geophila sensu stricto can be recognized by creeping stoloniferous habit rooted at nodes; pyrenes with one central or several adaxial ribs that are straight or twisted; and the absence of preformed germination slits (Piesschaert et al., 1999c) on the pyrenes. In contrast, Chassalia is distinct by its arborescent habit (rarely epiphytes or climbers); four distinct types of pyrenes (open type with an open ventral excavation, closed type with a ventral excavation largely covered by the endocarp, flat type with ventral excavation lacking, and grooved type with two ventral grooves separated by a median crest, Piesschaert, 2001); and basal median preformed germination slits located at the dorsal side of the pyrene (Barrabé et al., 2012). Another argument against a merger of Geophila in Chassalia is that Geophila is a wellknown genus, firmly rooted in the Rubiaceae literature and therefore deserves to retain its current generic status. The second alternative is to circumscribe Chassalia in a narrow sense (Chassalia sensu stricto), sister to Geophila sensu stricto (Fig. 3). A consequence of choosing this second alternative is that the Southeast Asian Chassalia sp.-ck25 and the East African Chassalia clade both have to be recognized at the generic level. We find this last scenario more useful, especially if these two latter clades possess distinct features, which would allow them to be recognized from Chassalia sensu stricto. Interestingly, the grooved type of pyrenes and 3–4 porate pollen are so far only known from C. parvifolia and C. subochreata belonging in the Eastern African Chassalia clade (Fig. 3); whether the same type of pyrenes and pollen also occur in C. albifolia, C. kenyensis, and C. violacea remains to be seen. Here, we adopt the narrowly delimited Chassalia, which is characterized mostly by the open type of pyrene and 3–4 colpate pollen (Piesschaert, 2001). All sampled species of Chassalia from the WIOR, tropical Asia (with the exception of Chassalia sp.-ck25), and tropical Africa (with the exceptions of C. albiflora, C. kenyensis, C. parvifolia, C. subochreata, and C. violacea) belong to Chassalia sensu stricto. We refrain from proposing new circumscriptions for the East African Chassalia clade and the South East Asian Chassalia lineage (represented by Chassalia sp.ck25), pending further studies (see later under Perspectives). Phylogenetic relationships between and within the genera of Palicoureeae—The neotropical genera Carapichea and Margaritopsis are resolved as successive sisters to a well-supported clade formed by the paleotropical Hymenocoleus-Geophila gerrardii clade and Chassalia sensu lato (Fig. 3). Palicourea sensu lato, the Notopleura-Rudgea clade, Carapichea, all from the neotropics, and the pantropical Margaritopsis sensu lato, respectively, form a basal grade within Palicoureeae. On the other hand, the monophyly of the large clade formed by Margaritopsis sensu lato, the Hymenocoleus-Geophila gerrardii clade, and Chassalia sensu lato is not strongly supported (BPP = 0.94) in our analyses (Fig. 3). Our analyses indicate that the African genus Chazaliella as defined by Verdcourt (1975, 1977) is paraphyletic with respect to Margaritopsis [including the Fijian genus Readea, represented by Margaritopsis membranacea (Gillepsie) L.Andersson, and the neotropical genus Chytropsia Bremek., represented by Margaritopsis astrellantha (Wernh.) L. Andersson] (Fig. 3). The Chazaliella-Margaritopsis clade (corresponding to Margaritopsis sensu lato) receives high support in our analyses, and [Vol. 101 this lineage can be recognized by the presence of two basal, marginal, preformed germination slits on the ventral side of the pyrene. Therefore, we support the inclusion of Chazaliella in Margaritopsis as done by Andersson (2001) and endorsed by Taylor (2005) and Barrabé et al. (2012). Andersson (2001) nomenclaturally transferred only the type species of the genera that he synonymized with Margaritopsis. The remaining species of Chazaliella are therefore transferred to Margaritopsis here. All species of Palicoureeae are regional endemics, with the exception of Geophila repens (L.) I.M.Johnst., which has been considered pantropical. Five varieties of G. repens have been described. Bremekamp (1963) described two of these varieties: Carinta repens var. americana, which is restricted to the neotropics, and Carinta repens var. comorensis, which is confined to the Comores (he considered Geophila synonym of the genus Carinta W.Wight, but Geophila D.Don was conserved [Hepper, 1960] against Carinta). The remaining three varieties are paleotropical. Bremekamp (1963) and Piesschaert et al. (1999c) found C. repens var. americana distinct from the paleotropical varieties based on flower number and carpological data; they questioned the inclusion of this variety within in Geophila repens, but did not recognize it as a separate species. The neotropical Carinta (= Geophila) repens var. americana does not group with the paleotropical C. repens var. comorensis and G. repens var. repens in our analyses, but forms a clade with the three sampled neotropical Geophila species. This finding supports the exclusion of C. repens var. americana from the paleotropical G. repens (see later under Geophila taxonomy) and is consistent with Bremekamp (1963) and Piesschaert et al. (1999c), who suggested its recognition at the species level based on carpological and palynological data. Furthermore, the Comorian C. repens var. comorensis and G. repens var. repens from Madagascar form a strongly monophyletic group, which in turn constitutes a well-supported clade with the African and Pacific G. repens var. repens clade. Therefore, the current varietal status of C. repens var. comorensis cannot be maintained. Evolution of Schizocarpous fruits in Psychotria— Our results (Fig. 2C, 2D) demonstrate that schizocarpous fruits have evolved independently at least two times from ancestors with fleshy, drupaceous fruits within Psychotrieae, a group that ancestrally has fleshy drupes (Fig. 2): once within the WIOR Psychotria clade (Fig. 2C) and once in the Australasian Psychotria clade (Fig. 2D). In this latter group, all sampled species of Psychotria with schizocarps are endemic to New Caledonia and form a monophyletic clade (BPP = 1), consistent with the results of Barrabé et al. (2014). The other species with schizocarpous fruits are members of the mostly Malagasy Cremocarpon clade and the Malagasy clade with only Cremocarpon lantzii, which form a basal grade within the WIOR Psychotria clade; C. lantzii is resolved with high support as sister to a strongly supported group of the mostly Malagasy Psychotria with drupaceous fruits (Fig. 2C). Our findings support Schatz’s (2001) hypothesis that considers Cremocarpon and Pyragra to be Psychotria with secondarily dehiscent fruits (schizocarps) evolved from ancestors with fleshy, drupaceous fruits. Furthermore, our character state reconstruction indicates that the Cremocarpon clade and C. lantzii had ancestors with schizocarpous fruits and suggests a single reversal of schizocarpous fruits back to the drupaceous condition (Fig. 2). Dissections of mature drupaceous fruits of many of these Malagasy species reveal the presence of Y-shaped vascular bundles along the July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE septa, which are morphologically similar to the carpophores of the schizocarps of Cremocarpon and Pyragra. These structures were previously noted by Capuron (1973) in some Malagasy Psychotria species and thus may be generally present in this drupe-bearing group. The Y-shaped vascular bundles of drupaceous fruits apparently do not have all the same functions as the carpophores of the schizocarpous fruits; however, their occurrence in fleshy, drupaceous fruits seems to corroborate the hypothesis of an evolutionary reversal of schizocarpous fruits back to drupaceous fruits within the WIOR Psychotria clade (Fig. 2C). On the other hand, this latter conclusion is ambiguous based on Fitch (1971) optimization; furthermore, the support for the Cremocarpon clade is low (BPP = 0.88), and thus the monophyly of a group formed by all Malagasy and Comorian Cremocarpon and the Malagasy Pyragra cannot be ruled out. Origins of the Malagasy leaf-nodulated species of Psychotria— Bremekamp’s (1963) postulation that the Malagasy leaf-nodulated species he (Bremekamp, 1960) included in Psychotria may represent a distinct genus is not supported by our analyses. All leaf-nodulated species of Psychotria sampled from Madagascar form a poorly supported group (BPP = 0.77), which is deeply nested within the otherwise African nodulated Psychotria clade (= the Afro-WIOR Psychotria clade, Fig. 2F). Two independent origins of the Malagasy leaf-nodulated species of Psychotria are supported by our results. The Malagasy leaf-nodulated Apomuria bullata (= Psychotria armandii Razafim. & B.Bremer, present study) is nested in the non-leafnodulated Psychotria WIOR clade (Fig. 2C). Thus, our analysis rejects a single origin of the leaf-nodulated species of Psychotria, inconsistent with Andersson (2002b) and Lemaire et al. (2012a). Our results indicate an African origin of the Malagasy leaf-nodulated species of Psychotria recognized by Bremekamp (1960), with a single long-distance dispersal event from Africa to Madagascar. In contrast, the Malagasy A. bullata appears to have evolved from a non-leaf-nodulated ancestor from Madagascar. Furthermore, the Comorian, leaf-nodulated Apomuria punctata and the Eastern African A. punctata form a poorly supported clade, which is deeply nested within the otherwise African leaf-nodulated Psychotria clade (Fig. 2F); therefore, the Comorian A. punctata seems to have reached the Comores from East Africa. The placement of the Comorian non-leaf-nodulated Psychotria conocarpa in the otherwise leafnodulated Psychotria clade (Fig. 2F) indicates that there has been at least one secondary loss of bacterial nodules. Taxonomic treatments— The results of this study have taxonomic implications for the infratribal classifications of the sister tribes Psychotrieae and Palicoureeae. Adoption of the broad circumscription of Psychotria as defined in this study requires the formal transfer of the species of the WIOR genera Apomuria, Cremocarpon, Psathura, Pyragra, and Trigonopyren to Psychotria. In total, we present 13 new combinations, 25 new names, and two lectotypifications in Psychotria. The inclusion of the following genera in Psychotria as defined here has been supported by previous molecular phylogenetic studies and/or this study: Camptopus (Barrabé et al., 2014; this study); Hydnophytum and its allied genera (Nepokroeff et al., 1999; Andersson, 2002b); Straussia (Nepokroeff et al., 1999; Andersson, 2002b); Amaracarpus, Calycosia, Dolianthus (Nepokroeff et al., 1999; Andersson, 2002b; Barrabé et al., 2014, this study); 1113 Heidstromia (Barrabé et al., 2014); and Streblosa (Andersson and Rova, 1999; Lemaire et al., 2012a). To render Geophila monophyletic, we describe the new genus Puffia Razafim. & B.Bremer to accommodate the Malagasy Geophila gerrardii; this genus is named in memory of the Austrian botanist and Rubiaceae specialist Professor Christian Puff, who recently passed away, for his important contributions to the knowledge of the Malagasy Rubiaceae. The inclusion of the African genus Chazaliella (Verdcourt, 1975, 1977) in Margaritopsis sensu lato (Andersson, 2001; Taylor, 2005; Barrabé et al., 2012) requires 19 new combinations. New combinations and names in Psychotria—Psychotria L., Syst. Nat. ed. 10, 2: 929 (1759), nom. cons. Type. Psychotria asiatica L. Myrstiphyllum P.Browne, Civ. Nat. Hist. Jamaica 152 (1756), nom. rej. Type. Psychotria myrstiphyllum Sw. Psychotrophum P.Browne, Nat. Hist. Jamaica 160 (1756), nom. rej. Type. Psychotria brownei Spreng. Mapouria Aubl., Hist. Pl. Guiane 1: 175 (1775). Type. Mapouria guianensis Aubl. = Psychotria mapourioides DC. Grumilea Gaertn., Fruct. 1: 138 (1788). Type. Grumilea nigra Gaertn. = Psychotria nigra (Gaertn.) Alston. Psathura Comm. ex Juss., Gen. Pl. 206 (1789). Type. Psathura borbonica J.F.Gmel., syn. nov. = Psychotria borbonica (J.F.Gmel.) Razafim. & B.Bremer. Hydnophytum Jack, Trans. Linn. Soc. London 14: 124 (1823). Type. Hydnophytum formicarum Jack ≡ Lasiostoma formicarum (Jack) Spreng., syn. nov. Myrmecodia Jack, Trans. Linn. Soc. London 144: 122 (1823). Type. Myrmecodia tuberosa Jack ≡ Lasiostoma tuberosa (Jack) Spreng., syn. nov. Amaracarpus Blume, Bijdr. 945 (1826–1827). Type Amaracarpus pubescens Blume, syn. nov. Streblosa Korth., Ned Kruidk. Arch. 2(2): 245 (1851). Type. Psychotria tortilis Blume ≡ Streblosa tortilis (Blume) Korth., syn. nov. Calycosia A.Gray, Proc. Amer. Acad. Arts. Sci. 4: 47 (1858). Type. Calycosia petiolata A.Gray, syn. nov. Straussia (DC.) A.Gray, Proc. Amer. Acad. Arts Sci. 4: 42 (1858). Type. Coffea kaduana Cham. & Schltdl. ≡ Coffea sect. Straussia DC., Prod. 4: 502 (1830) ≡Straussia kaduana (Cham. & Schltdl.) A.Gray = Psychotria kaduana (Cham. & Schltdl.) Forb. Camptopus Hook.f., Bot. Mag. t. 5755 (1869). Type. Camptopus mannii Hook.f. (not Psychotria mannii Hiern) = Psychotria camptopus Verdc. Cremocarpon Boiv. ex Baill., Bull. Mens. Soc. Linn. Paris 1: 192 (1879). Type. Cremocarpon boivinianum Baill. = Psychotria boiviniana (Baill.) Razafim. & B.Bremer. Myrmephytum Becc., Malesia 2: 92 (1884). Type. Myrmephytum selebicum Becc., syn. nov. Myrmedoma Becc., Malesia 2: 94 (1884). Type. Myrmedoma arfakiana Becc., syn. nov. Squamellaria Becc., Malesia 2: 228 (1886). Type. Myrmecodia imberbis A.Gray = Squamellaria imberbis (A.Gray) Becc., syn. nov. Dolianthus C.H.Wright, Bull. Misc. Inform. Kew 1899: 106 (1899). Type. Dolianthus vaccinioides C.H.Wright, syn. nov. Megalopus K.Schum., Bot. Jahrb. Syst. 28: 491 (1900). Type. Megalopsus goetzei K.Schum. = Psychotria megalopus Verdc. Hedstromia A.C.Sm., Bernice P. Bishop Mus. Bull. 141: 146 (1936). Type. Hedstromia latifolia A.C.Sm., syn. nov. 1114 AMERICAN JOURNAL OF BOTANY Pyragra Bremek., Candollea 16: 174 (1958). Type. Pyragra obtusifolia Bremek. = Psychotria antakaranensis Razafim. & B.Bremer. Apomuria Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54(5): 88 (1963). Type. Apomuria mollis Bremek. = Psychotria sylvieana Razafim. & B.Bremer. Trigonopyren Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54(5): 105, 106 (1963). Type. Trigonopyren pauciflorus Bremek. = Psychotria alaotrensis Razafim. & B.Bremer. Anthorrhiza C.R.Huxley & Jebb, Bull. Jard. Bot. Nat. Belgium 60: 420 (1990). Type. Anthorrhiza echinella Huxley & Jebb., syn. nov. [Vol. 101 Note. This species is named after the local tribe Antakarana that occupies the area, where the type specimen was collected. 6. Psychotria armandii Razafim. & B.Bremer, nom. nov. Replaced name. Apomuria bullata Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 102 (1963), not Psychotria bullata Seem., 1866. Type. Madagascar, limite des Domaines de l’Est et du Centre, fôret d’Analamazaotra, alt. 800 m, Perrier de la Bâthie 6926 (Holotype, P!). Note. This species is named in memory of the Malagasy botanist Armand Rakotozafy. 1. Psychotria abrahamii Razafim. & B.Bremer, nom. nov. 7. Psychotria atsinanana Razafim. & B.Bremer, nom. nov. Replaced name. Psathura lutescens Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 174 (1963), not Psychotria lutescens Craib, 1932. Type. Madagascar, Domaine de l’Est, Réserve Naturelle I, Betampona, poste Rendrirendry, sommet de Vohimarangitra, alt. 1200 m, Cours 2567 (Holotype, P!; isotype, P!). Replaced name. Psathura lancifolia Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 173 (1963), not Psychotria lanceifolia K.Schum., 1903. Type. Madagascar, Domaine de l’Est, District de Tamatave, Mangabé, Decary 16851 (Holotype, P!). Note. This species is named in memory of the Malagasy botanist Jean Prosper Abraham. 2. Psychotria alaotra Razafim. & B.Bremer, nom. nov. Note. This species is named after the Region Atsinanana (meaning east). 8. Psychotria batopedina (Verdc.) Razafim. & B.Bremer, comb. nov. Replaced name. Trigonopyren pauciflorus Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 108 (1963), not Psychotria pauciflora Bartl. ex DC., 1830. Type. Madagascar, Domaine du Centre, Lac Alaotra, Herb. Jard. Bot. Tanan. 3853 (Holotype, P!). Basionym. Psathura polyantha Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 174 (1963), hom. illeg.; Psathura badopedina Verdc., Kew Bull. 37: 128 (1992). Type. Madagascar, Domaine de l’Est, District de Brickaville, Canton d’Ambalarondra, Andranampony, alt. 300 m, Cours 4520 (Holotype, P!). Note. This species is named after Alaotra Lake, where the type specimen was collected. 9. Psychotria bealananensis Razafim. & B.Bremer, nom. nov. 3. Psychotria andasibeensis, Razafim. & B.Bremer, nom. nov. Replaced name. Trigonopyren sambiranensis Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 113 (1963), not Psychotria sambiranensis Bremek., 1963. Type. Madagascar, Domaine du Centre (Nort-Est), District Bealanana, Canton Mandrindrano, Réserve Naturelle IV, Rababoto RN 5231 (Holotype, P!). Replaced name. Trigonopyren nitidulus Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 112 (1963), not Psychotria nitidula Cham. & Schltdl., 1829. Type. Madagascar, limites des Domaines de l’Est et du Centre, Analamazaotra, Herb. Jard. Bot. Tanan. 3783 (Holotype, P!). Note. This species is named after Commune Andasibe, where the type specimen was collected. 4. Psychotria ankarensis (Bremek.) Razafim. & B.Bremer, comb. nov. Basionym. Pyragra ankarensis Bremek. Candollea 16: 177 (1958). Type. Madagascar, Province Diego Suarez, plateaux calcaires de l’Ankarana du Nord, entre Ambilobe et Anivorano (secteur Nord du Domaine de l’Ouest), alt. 200–350 m, fôret tropophile sur calcaire jurassique, Humbert et Capuron 25480 (Holotype, P!). Note. This species is named after District Bealanana, where the type specimen was collected. 10. Psychotria belamboi Razafim. & B.Bremer, nom. nov. Replaced name. Trigonopyren capituliflorus Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 110 (1963), not Psychotria capituliflora (Müll.Arg.) Standl., 1936. Type. Madagascar, Domaine du Centre, Ampandrandava, fôret de Belambo, vers 1200 m, Seyrig 489 (Holotype, P!). Note. This species is named after the forest of Belambo, where the type specimen was collected. 5. Psychotria antakaranensis Razafim. & B.Bremer, nom. nov. 11. Psychotria bemarahensis Razafim. & B.Bremer, nom. nov. Replaced name. Pyragra obtusifolia Bremek. Candollea 16: 175–176 (1958), not Psychotria obtusifolia Lam. ex Poir., 1804. Type. Madagascar, collines et plateaux calcaires de l’Analamera (secteur Nord du Domaine de l’Ouest), alt. 50– 400 m, fôret tropophile, Humbert 19122 (Holotype, P!). Replaced name. Trigonopyren angustifolius Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 109 (1963), not Psychotria angustifolia Poir., 1804. Type. Madagascar, Domaine de l’ouest, Tsingy du Bemahara, Réserve Naturelle IX, près de Tsiandro, Leandri 828 (Holotype, P!). July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE 1115 Note. This species is named after the National Park Bemaraha, where the type specimen was collected. Domaine de l’Ouest, Ambongo, bords du Kapilosa, Perrier de la Bâthie 1614 (Holotype, P!). 12. Psychotria bernierii (Bremek.) Razafim. & B.Bremer, comb. nov. Basionym. Cremocarpon bernieri Bremek., Candollea 16: 165–166 (1958). Type. Madagascar (Nord), Ling-vatour (probablement l’Anivato), Bernier 111 (Holotype, P!; isotype, K!). Note. This species is named after the Malagasy botanist Désiré Ravelonarivo. 13. Psychotria betotozafyi, Razafim. & B.Bremer, nom. nov. Basionym. Apomuria penduliflora Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 100 (1963), not Psychotria penduliflora Ridl., 1923. Type. Madagascar. Domaine de l’Ouest, Ankaladina sur la Betsiboka, Perrier de la Bâthie 3789 (Holotype, P!). Note. This species is named after the Malagasy botanist Be Totozafy Sylvain. 14. Psychotria biloba (Bremek.) Razafim. & B.Bremer., comb. nov. Basionym. Apomuria biloba Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 97 (1963). Type. Madagascar, Domaine de l’Ouest, Tsiandro, Behandrao, alt. 550–600 m, Leandri 1986 (Holotype, P!). 15. Psychotria boiviniana (Baill.) Razafim. & B.Bremer, comb. nov. Basionym. Cremocarpon boivinianum Baill., Hist. Pl. 7: 399 (1880). Type. Comores, probablement Mayotte, Boivin 3165 (Holotype, P!; isotype, K!). 16. Psychotria borbonica (J.F.Gmel.) Razafim. & B.Bremer, comb. nov. Basionym. Psathura borbonica J.F.Gmel., Syst. Nat. ed. 13, 2: 577 (1791). Type. La Réunion, Commerson s.n. (Lectotype, designated by Verdcourt (1983: 108), P-JU 9975; isolectotype, P!). 17. Psychotria charlotteana Razafim. & B.Bremer, nom. nov. Replaced name. Apomuria perrieri Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 95 (1963), not Psychotria perrieri Bremek., 1963. Type. Madagascar, Domaine de l’Ouest, Haut Bemarivo (Boena), Perrier de la Bâthie 4564 (Holotype, P!). Note. This species is named after the Malagasy botanist and palynologist Professor Charlotte Rajeriarison. 18. Psychotria crispulifolia (Bremek.) Razafim. & B.Bremer, comb. nov. Basionym. Apomuria crispulifolia Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 99 (1963). Type. Madagascar, Domaine de l’Ouest, près d’Anjabona (Boena), Perrier de la Bâthie 3791 (Holotype, P!). 19. Psychotria desirei Razafim. & B.Bremer, nom. nov. Replaced name. Apomuria angustifolia Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 99 (1963), not Psychotria angustifolia Poir., 1804. Type. Madagascar, 20. Psychotria faramalala Razafim. & B.Bremer, nom. nov. Replaced name. Apomuria falcata Bremek., Verh. Konink. Nederl. Akad., Wetensch., Natuurk., Tweede Reeks 54: 98 (1963), not Psychotria falcata Rusby, 1893. Type. Madagascar, Domaine de l’Ouest, Ankarafantsika, Perrier de la Bâthie 3981 (Holotype, P!). Note. This species is named after the Malagasy botanist Professor Faramalala Miadana. 21. Psychotria fissicorne (Bremek.) Razafim. & B.Bremer, comb. nov. Basionym. Cremocarpon fissicorne Bremek., Candollea 16: 163 (1958). Type. Madagascar, Plateau d’Ankara, Kamakama, Perrier de la Bâthie 1015 (Holotype, P!). 22. Psychotria hanta Razafim. & B.Bremer, nom. nov. Replaced name. Cremocarpon tenuifolium Bremek., Candollea 16: 164 (1958), not Psychotria tenuifolia Sw., 1788. Type. Madagascar (Nord), Diego Suarez, Montagne des Français, Perrier de la Bâthie 17512 (Holotype, P!). Note. This species is named after the Malagasy botanist Hanta Razafindraibe. 23. Psychotria hymenodes (Bremek.) Razafim. & B.Bremer, comb. nov. Basionym. Apomuria hymenodes Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 94 (1963). Type. Madagascar, Domaine de l’Ouest, Tsarasaotra, Perrier de la Bâthie 384 (Holotype, P!). 24. Psychotria kentii Razafim. & B.Bremer, nom. nov. Replaced name. Psathura myriantha Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 175 (1963), not Psychotria myriantha Müll.Arg., 1876. Type. Madagascar, Domaine de l’Est, vallée de la Lokoho, près d’Ambalavaniho, alt. 75–300 m, Humbert et Cours 22803 (Holotype, P!). Note. This species is named after of the Swedish botanist and Rubiaceae specialist Dr. Kent Kainulainen. 25. Psychotria labatii Razafim. & B.Bremer, nom. nov. Replaced name. Trigonopyren comorensis Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 107 (1963), not Psychotria comorensis Bremek., 1963. Type. Comores, Mayotte, bois du Chongui, de Moussa Péré au Qualey, Boivin 3172 (Holotype, P!). Note. This species is named in memory of the late French botanist Professor Jean-Noël Labat for his important contributions to the Comorian and Malagasy floras. 26. Psychotria lantzii (Bremek.) Razafim. & B.Bremer, comb. nov. 1116 AMERICAN JOURNAL OF BOTANY Basionym. Cremocarpon lantzii Bremek., Candollea 16: 168 (1958). Type. Madagascar (Sud-Est), Benanoremana, Lantz s.n. (holotype, P!). 27. Psychotria madagascariensis Razafim. & B.Bremer, nom. nov. Replaced name. Apomuria melanosticta Bremek., Verh. Konink. Nederl. Akad., Wetensch., Natuurk., Tweende Reeks 2, 54: 95 (1963), not Psychotria melanosticta K.Schum., 1894. Madagascar, Domaine de l’Ouest, route de Tananarive à Majunga, km 285, alt. 350 m (environs d’Antsiafabositra), Capuron SF125 (Holotype, P!). 28. Psychotria moramangensis (Bremek.) Razafim. & B. Bremer, comb. nov. Basionym. Apomuria moramangensis Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 101 (1963). Type. Madagascar, limite des Domaines de l’Est et du Centre, entre Anosibe et Moramanga (km 18), SF 9469 (Holotype, P!). 29. Psychotria moratii Razafim. & B.Bremer, nom. nov. Replaced name. Psathura myrtifolia A.Rich. ex DC., Prodr. 4: 463 (1830), not Psychotria myrtifolium St.-Lag, 1880. Type. Mauritius, Michaux s.n. (Holotype, P!). Note. This species is named after the French botanist Professor Philippe Morat. 30. Psychotria papanga Razafim. & B.Bremer, nom. nov. Replaced name. Cremocarpon floribundum Bremek., Candollea 16: 171 (1958), not Psychotria floribunda Kunth, 1820. Type. Madagascar (Sud-Est), Massif de Beampingaratra, Mt. Papanga, alt. 1400–1525 m, fôret et brousse éricoide du sommet, Humbert 6350 (Holotype, P!). Note. This species is named after the Mountain Papanga, where the type specimen was collected. 31. Psychotria puffii Razafim. & B.Bremer, nom. nov. Replaced name. Apomuria parvifolia Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 93 (1963), not Psychotria parvifolia Benth., 1853. Type. Madagascar, Domaine du Centre, montagnes à l’ouest d’Itremo (Ouest Betsileo), pentes occidentales, alt. 1500–1700 m, Humbert 30041 (Holotype, P!). Note. This species is named in memory of the late Austrian botanist and Rubiaceae specialist Professor Christian Puff. 32. Psychotria pulchristipula (Bremek.) Razafim. & B. Bremer, comb. nov. [Vol. 101 Galeotti, 1844. Type. Madagascar. Montagne d’Ambohitsi, Hildebrandt 3888b (holotype, P!). Note. This species is named after the American botanist Dr. George Schatz for his important contributions to the knowledge of the Malagasy flora. 34. Psychotria sylvieana Razafim. & B.Bremer, nom. nov. Replaced name. Apomuria mollis Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 92 (1963), not Psychotria mollis Poir., 1804. Type. Madagascar, Domaine de l’Ouest, Morataitra, rive droite du Betsiboka en amont de son confluent avec l’Ikopa, Perrier de la Bâthie 805 (Holotype, P!). Note. This species is named after the Malagasy botanist Dr. Sylvie Andriambololonera. 35. Psychotria terniflora (A.Rich. ex DC.) Razafim. & B. Bremer, comb. nov. Basionym. Psathura terniflora A.Rich. ex DC., Prod. 4: 413 (1830). Type. Mauritius, Michaux s.n. (Holotype, P!). 36. Psychotria tsiandroi Razafim. & B.Bremer, nom. nov. Replaced name. Trigonopyren albicostatus Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 111 (1963), not Psychotria albicostata Rusby, 1920. Type. Madagascar, Domaine de l’Ouest, Tsiandro, fôret de Behandrao, alt. 550–600 m, Capuron, Leandri et Razafindrakoto 1949 (Holotype, P!). Note. This species is named after the region, where the type specimen was collected. 37. Psychotria tsimihetensis Razafim. & B.Bremer, nom. nov. Replaced name. Trigonopyren multiflorus Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 112 (1963), not Psychotria multiflora Schumach. & Thonn., 1827. Type. Madagascar, limite des Domaines de l’Est et du Centre, Massif d’Anjanaharibe, à l’Ouest d’Andapa (haute Andramonta, bassin de la Lokoho), alt. 750 m, Humbert, Capuron, Cours 24501 (Holotype, P!). Note. This species is named after the local tribe that occupies the area, where the type specimen was collected. 38. Psychotria vololoniaina Razafim. & B.Bremer, nom. nov. Replaced name. Trigonopyren ovalifolius Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Reeks 54: 109 (1963), not Psychotria ovalifolia Rusby, 1907. Type. Madagascar, Domaine de l’Ouest, Tsingy du Bemaraha, Réserve Naturelle IX, Rakotovao RN 5122 (Holotype, P!). Basionym. Cremocarpon pulchristipulum Bremek., Candollea 16: 166 (1958). Type. Madagascar (Centre), Bassin du Bemarivo, fôret d’Analamahitso, alt. 800 m, Perrier de la Bâthie 3725 (Holotype, P!; isotype, K!). Note. This species is named after the Malagasy botanist Professor Vololoniaina Harimanga Jeannoda. 33. Psychotria schatzii Razafim. & B.Bremer, nom. nov. Type. Puffia gerrardii (Baker) Razafim. & B.Bremer, comb. nov. Basionym. Geophila gerrardii Baker, J. Linn. Soc. 21: 413 (1885); Carinta gerrardii (Baker) Bremek., Verh. Konink. Replaced name. Cremocarpon sessilifolium Bremek., Candollea 16: 162 (1958), not Psychotria sessifolia M.Martens & Puffia Razafim. & B.Bremer, gen. nov. July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE 1117 Nederl. Akad., Natuurk., Tweede Reeks 54: 120 (1963). Type. Madagascar, Gerrard 102 (Lectotype, designated by Bremekamp (1963: 121), K!). Creeping, stoloniferous herbs with 2 pairs of leaves on the flowering stem, rooted at nodes, entirely pubescent. Leaves petiolate, dark green and glabrous above, brownish and pubescent underneath, secondary veins less prominent above and more prominent below; stipules simple, deltoid and shallowly bifid, green and glabrous on both sides. Inflorescence terminal, capitate formed by 5–7 flowers, subtended by involucral bracts. Flowers 4–6-merous, actinomorphic, white, isostylous; calyx green; corolla white; style exserted, white; stigma bifid, white; anthers included. Fruits globose, fleshy, drupaceous, orange when fully mature. Pyrenes verrucate, 6-costate. Diagnostic characters. Puffia is distinct from Geophila sensu stricto by its orange fruits. It differs from the African genus Hymenocoleus in having isostylous flowers, verrucate and sightly ribbed pyrenes (instead of heterodistylous and with smooth pyrenes; Robbrecht, 1975, 1977). The persistent, membranous sheaths lying inside the stipules, a potential morphological synapomorphy of the latter, are absent in the former. Furthermore, Puffia is confined to southeastern Madagascar, while Hymenocoleus is restricted to tropical Africa. Number of species: one. For a detailed description, see Baker (1887) and Bremekamp (1963). Distribution and habitat. Puffia gerrardii is restricted to the littoral forests of southeastern Madagascar between the Masoala National Park (District Maroantsetra, Region Atsinanana, Province Toamasina) and the Manombo National Park (District Farafangana, Region Atsimo-Atsinanana, Province Fianarantsoa). The species also occurs on the Island of Nosy Mangabe (National Park of Nosy Mangabe). 2. Margaritopsis coffeosperma (K.Schum.) Razafim. & B. Bremer, comb. nov. New combinations in Margaritopsis—Margaritopsis C.Wright, in Sauvalle Anales. Acad. Ci. Méd. Habana 6: 146 (1869), nom. cons. (Taxon 62: 1069–1070). Type. Margaritopsis acuifolia C.Wright. Eumachia Dc., Prod. 4: 478–479 (1830), nom. rej. Type. Eumachia carnea (G. Forst.) DC. ≡ Petesia carnea G. Forst. = Psychotria carnea (G. Forst.) A.C. Sm. Margaris Griseb., Cat. Pl. Cub.: 134 (1866), hom. illeg., not Margaris DC., 1830. Type. Margaris nudiflora Griseb. = Margaritopsis acuifolia C.Wright. Readea Gillespie, Bernice P. Bishop Mus. Bull. 74: 35 (1930). Type. Readea membranacea Gillespie. = Margaritopsis membranacea (Gillespie) L.Andersson. Chytropsia Bremek., Rec. Trav. Bot. Néerl. 31: 291 (1934). Type. Psychotria astrellantha Wernham ≡ Chytropsia astrellantha (Wernham) Bremek. = Margaritopsis astrellantha (Wernham) L.Andersson. Chazaliella E.M.A.Petit & Verdc., Kew Bull. 31: 268 (1975). Type. Psychotria abrupta Hiern ≡ Chazaliella abrupta (Hiern) E.M.A.Petit & Verdc. = Margaritopsis abrupta (Hiern) L. Andersson. Basionym. Psychotria insidens Hiern, Fl. Trop. Afr. 3: 208 (1877); Chazaliella insidens (Hiern) E.M.A.Petit & Verdc., Kew Bull. 30: 269 (1975). Type. Fernando Po, alt. 300 m, Mann 310 & 1155 (syntypes, K!). 1. Margaritopsis anacamptopus (K.Schum.) Razafim. & B. Bremer, comb. nov. Basionym. Psychotria anacamptopus K.Schum., Bot. Jahrb. Syst. 33: 360 (1903); Chazaliella anacamptopus (K.Schum.) E.M.A.Petit & Verdc. Type Cameroun, Bipindi, Comanchio, Zenker 984 (Holotype, B†). Basionym. Psychotria coffeosperma K.Schum., Bot. Jahrb. Syst. 33: 363 (1903); Chazaliella coffeosperma (K.Schum.) Verdc., Kew Bull. 31: 813 (1977). Type. Cameroun, Lolodorf, Staudt 141 (Holotype, B†; isotypes, K!, P!). 3. Margaritopsis cupulicalyx (Verdc.) Razafim. & B.Bremer, comb. nov. Basionym. Chazaliella cupulicalyx Verdc., Kew Bull. 31: 799 (1977). Type. Liberia, Cooper 360 (Holotype, K!; isotype, K!). 4. Margaritopsis domatiicola (De Wild.) Razafim. & B. Bremer, comb. nov. Basionym. Psychotria domatiicola De Wild., Pl. Bequaert. 2: 362 (1924); Chazaliella domatiicola (De Wild.) E.M.A.Petit & Verdc., Kew Bull. 30: 269 (1975). Type. Zaïre (R. D. Congo), between Bolobo and Sandy Beach, Bequaert 874 (Holotype, BR!; isotype, BR!). 5. Margaritopsis gossweileri (Cavaco) Razafim. & B. Bremer, comb. nov. Basionym. Grumilea gossweileri Cavaco, Bull. Mus. Natl. Hist. Nat., sér. 2 II, 29: 515 (1958); Chazaliella gossweileri (Cavaco) E.M.A.Petit & Verdc., Kew Bull. 30: 269 (1975). Type. Angola, NE Lunda, Dundo, proximum flumen Luacimo, Gossweiler 13799 (Holotype, P!; isotype, K!). 6. Margaritopsis insidens (Hiern) Razafim. & B.Bremer, comb. nov. 7. Margaritopsis longistylis (Hiern) Razafim. & B.Bremer, comb. nov. Basionym. Psychotria longistylis Hiern, Fl. Trop Afr. 3: 209 (1877); Chazaliella longistylis (Hiern) E.M.A.Petit & Verdc., Kew Bull. 30: 269 (1975). Type. Gabon, Gaboon River, Mann 987 (Holotype, K!). 8. Margaritopsis lophoclada (Hiern) Razafim. & B.Bremer, comb. nov. Basionym. Psychotria lophoclada Hiern, Fl. Trop. Afr. 3: 197 (1877); Chazaliella lophoclada (Hiern) E.M.A.Petit & Verdc., Kew Bull. 30: 269 (1975). Type. Sierra Leone, Sugar Loaf Mountain, Barter s.n. (Lectotype, K!, here designated by Razafimandimbison and B.Bremer). Note. We selected the specimen Barter s.n. (K!) as lectotype among the three syntypes, because it is in better condition than the other syntypes, Afzelius s.n. and G. Don s.n. (BM!). 9. Margaritopsis macrocarpa (Verdc.) Razafim. & B.Bremer, comb. nov. Basionym. Chazaliella macrocarpa Verdc., Kew Bull. 31: 794 (1977). Type. Zaïre (R. D. Congo), Louis 3463 (Holotype, BR!). 1118 AMERICAN JOURNAL OF BOTANY [Vol. 101 10. Margaritopsis obanensis (Wernham) Razafim. & B. Bremer, comb. nov. 18. Margaritopsis viridicalyx (R.D.Good) Razafim. & B. Bremer, comb. nov. Basionym. Psychotria obanensis Wernham, Cat. Pl. Oban.: 53 (1913); Chazaliella obanensis (Wernham) E.M.A.Petit & Verdc., Kew Bull. 30: 269 (1975). Type. Nigeria, Oban, Talbot 244 (Holotype, BM!). Basionym. Psychotria viridicalyx R.D.Good, J. Bot. 64, Suppl. 2: 33 (1926), as “viridocalyx”; Chazaliella viridicalyx (R.D.Good) Verdc., Kew Bull. 31: 816 (1977). Type. Angola, Cabinda, Mayumbe, Buco Zau, Gossweiler s.n. (Holotype, BM!). 11. Margaritopsis obovoidea (Verdc.) Razafim. & B.Bremer, comb. nov. 19. Margaritopsis wildemanniana (Th.Dur. ex De Wild.) Razafim. & B.Bremer, comb. nov. Basionym. Chazaliella obovoidea Verdc., Kew Bull. 31: 803 (1977). Type. Zaïre (R. D. Congo), Toussaint 2270 (Holotype, BR!; isotype, BR!). Basionym. Psychotria wildemanniana Th.Dur. ex De Wild., Ann. Mus. Congo, Bot. sér. 5, 2: 349 (1908); Chazaliella wildemanniana (Th.Dur. ex De Wild.) E.M.A.Petit & Verdc., Kew Bull. 30: 270 (1975). Type. Zaïre (R. D. Congo), Djuma Valley, Gillet Justin 2738, 2762 & 2768, & Gentil s.n. (syntypes, BR!). 12. Margaritopsis oddonii (De Wild.) Razafim. & B.Bremer, comb. nov. Basionym. Psychotria oddonii De Wild., Ann. Mus. Congo Belge, Bot. sér. 5, 2: 187, t. XLIV (1907); Chazaliella oddonii (De Wild.) E.M.A.Petit & Verdc., Kew Bull 30: 269 (1975). Type. Zaïre (R. D. Congo), Sanda, A. Oddon 3001 & 3746 (syntypes, BR!). 13. Margaritopsis pilosula (De Wild.) Razafim. & B.Bremer, comb. nov. Basionym. Psychotria pilosula De Wild., Pl. Bequaert. 2: 403 (1924); Chazaliella pilosula (De Wild.) E.M.A. & Verdc., Kew Bull. 30: 269 (1975); Type. Zaïre (R. D. Congo), between Walikale and Lobutu, Bequaert 6588 (Holotype, BR!). 14. Margaritopsis poggei (K.Schum.) Razafim. & B.Bremer, comb. nov. Basionym. Psychotria poggei K.Schum., Bot. Jahrb. Syst. 28: 97 (1899); Chazaliella poggei (K.Schum.) E.M.A.Petit. & Verdc., Kew Bull. 30: 269 (1975). Type. Zaïre (R. D. Congo), near Mukenge, Pogge 1039, 1095 & 1251 (syntypes, B†). 15. Margaritopsis ramisulca (Verdc.) Razafim. & B.Bremer, comb. nov. Basionym. Chazaliella ramisulca Verdc., Kew Bull 31: 814 (1977). Type. Zaïre (R. D. Congo), Donis 1625 (Holotype, BR!). 16. Margaritopsis rotundifolia (R.D.Good) Razafim. & B.Bremer, comb. nov. Basionym. Psychotria rotundifolia R.D.Good, J. Bot. 64, Suppl. 2: 32 (1926); Chazaliella rotundifolia (R.D.Good) E.M.A.Petit & Verdc., Kew Bull. 30: 270 (1975). Type. “Portuguese Congo”, Buco Zau, Mayumbe, Gossweiler 6812 (Holotype, BM!). 17. Margaritopsis sciadephora (Hiern) Razafim. & B. Bremer, comb. nov. Basionym. Psychotria sciadephora Hiern, Fl. Trop. Afr. 3: 202 (1877); Chazalliella sciadephora (Hiern) E.M.A.Petit & Verdc., Kew Bull. 30: 270 (1975). Type. Cameroun Mt., Mann 1192 (Lectotype, here designated by Razafimandimbison & B.Bremer, K!; isolectotype, BR!). Note. We selected the specimen Mann 729 (K!) over Mann 1192 (K!), both syntypes, as the lectotype because it is in better condition and has flowers. Geophila taxonomy—Geophila repens (L.) I.M. Johnst., Sargentia 8: 281 (1949). Rondeletia repens L., Syst. Nat. (ed. 10) 2: 928 (1759). Psychotria repens (L.) L., Amoen Acad. 5: 377 (1759). Geophila herbacea K.Schum., Nat. Pflanzenfam. 4(1): 119 (1891), nom. superfl. illeg. Geocardia repens (L.) Baker f., Bekn. Fl. Java 144 (1956). Carinta repens (L.) L.B. Sm. & Downs, Sellowia 7: 88 (1956). Type. Jamaica, Sloane Herb. vol. 4: 111 (Lectotype, designated by Howard (1989: 416), BM ID 502, barcode BM000589966!). Geophila uniflora Hiern, Fl. Trop. Afr. 3: 221 (1877). Types. Niger, at Nupe, Barter s.n. (K n.v.), Sudan, Niamniamland, Nabambiso, Schweinfurth 3856 (Syntypes, BM n.v., K n.v.). Psychotria herbacea Jacq., Enum. Syst. Pl. 16 (1760), not Geophila herbacea K. Schum. (1891). Psychotrophum herbaceum (Jacq.) Crantz, Inst. Rei Herb. 2: 259 (1766). Cephaelis herbacea (Jacq.) Kurze, J. Asiat. Soc. Bengal, Pt. 2, Nat. Hist. 46(2): 140 (1877). Mapouria herbacea (Jacq.) Muell.Arg., Fl. Bras. 6(5): 427 (1881). Uragoga herbacea (Jacq.) Kuntze, Revis. Gen. Pl. 1: 300 (1891). Carinta herbacea (Jacq.) W.Wight, Contr. U.S. Natl. Herb. 9: 216 (1905). Carinta repens var. americana Bremek., Verh. Konink. Nederl. Akad., Natuurk., Tweede Sect. 54: 119 (1963). Type. Rheede, Hort. Malab. 10: tab. 21. Notes. Rondeletia repens L. was originally described based on two specimens, one from Jamaica and one from India. Bremekamp (1963) considered the type to be from India, but did not formally designate a lectotype. Later, Howard (1989) did designate a lectotype, and he chose the Jamaican plant. Thus, the name Geophila repens correctly applies to the neotropical plants. This situation has been confused taxonomically for some time. One of these confusions was that Bremekamp recognized some varieties of Geophila repens (as Carinta repens) and treated var. repens (incorrectly) to include the paleotropical plants and var. americana (incorrectly) to include the neotropical plants. His var. repens is however typified by the Jamaican lectotype specimen and thus actually includes to the neotropical plants. Bremekamp’s var. americana was not described as a new variety but was based on a previously described name, Psychotria herbacea Jacq., and Bremekamp seems not to have noticed that Jacquin’s name was based on and is thus typified by an illustration and description by Rheede in Rheede Hort. Mal. 10: 41, t. 21 (1689), which is based on a plant from India. Thus, Bremekamp’s var. americana actually applies to the paleotropical plants. The name Psychotria herbacea Jacq. does apply to the paleotropical plants that have been included in Geophila repens, July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE however this is not the same species as Geophila herbacea K.Schum., so Jacquin’s name cannot now be transferred into Geophila; unfortunately, Schumann’s name was a replacement name for Rondeletia repens L., so it is an illegitimate superfluous later name for Geophila repens, which has also generated taxonomic confusion in this group. The oldest validly published name for the paleotropical plants that have been included in Geophila repens appears to be Geophila uniflora Hiern, which is here adopted as the accepted name; further study of Geophila in southeast Asia may show that an earlier name exists but is outside the scope of this present work. CONCLUSIONS A broadly circumscribed Psychotria that includes all its allied genera is proposed, rendering the tribe Psychotrieae monogeneric. In Palicoureeae, the new genus Puffia is decribed to accommodate the Malagasy Geophila gerrardii that is more closely related to the African genus Hymenocoleus than to Geophila sensus stricto. Geophila repens is now exclusively neotropical with no varieties recognized and the accepted name for the paleotropical plants of Geophila repens is Geophila uniflora. Chassalia is paraphyletic with respect to Geophila sensu stricto, and we propose a narrow circumscription of Chassalia that excludes the Eastern African Chassalia clade and the Southeast Asian Chassalia clade (represented by Chassalia sp.-ck25), successive sisters to the clade formed by Geophila sensu stricto and Chassalia sensu stricto. Schizocarpous fruits evolved independently two times from drupaceous fruits within the broadly circumscribed Psychotria and we report one reversal back to the drupaceous condition in the WIOR Psychotria clade. Finally, two independent origins of the bacterial-nodulated Psychotria are inferred. The Malagasy leaf-nodulated species of Psychotria recognized by Bremekamp (1960) evolved from a single leaf-nodulated ancestor from mainland Africa, while the Malagasy leaf-nodulated Apomuria bullata (now Psychotria armandii Razafim. & B.Bremer) evolved from a non-leaf-nodulated ancestor from Madagascar. One secondary loss of leaf nodules within the African-WIOR leaf-nodulated Psychotria clade is reported. PERSPECTIVES The results of the molecular phylogenetic analyses presented in this study allow us to establish improved classifications of the sister tribes Psychotrieae and Palicoureeae. This study, coupled with the results of previous molecular studies, demonstrates that the genera Amaracarpus, Calycosia, Dolianthus, Heidstromia, Hydnophytum and its allied genera, and Streblosa all belong to this broadly delimited Psychotria, and therefore should formally be transferred to the latter genus. The phylogenetic relationships between the seven major lineages of Psychotria identified are only partly resolved. We hope to investigate more species of Psychotrieae and Palicoureeae from the Indian subcontinent (especially the Western Ghats, a hill range along the west coast of India, and Sri Lanka), continental Asia (in particular Thailand), Southeast Asia (particularly the Indonesian-Malesian region), which are poorly represented in our analyses. Also, a much broader sampling of Chassalia from tropical Asia (especially the Indonesian-Malesian region), tropical Africa (particularly Southern and Eastern Africa) is needed before we can formally circumscribe the Eastern African Chassalia clade and the Southeast Asian Chassalia clade excluded from Chassalia. This should be 1119 coupled with morphological, palynological, and carpological studies of the members of these two clades. Finally, the new phylogeny of the sister tribes Psychotrieae and Palicoureeae reveals some interesting biogeographic patterns, which we will test using a broadened sampling of the Psychotrieae alliance. LITERATURE CITED AGNARSSON, I., AND M. KUNTNER. 2012. The generation of biodiversity hotspot: Biogeography and phylogeography of the Western Indian Ocean islands. In K. Anamthawat-Jonsson [ed.], Current topics in phylogenetics and phylogeography of terrestrial and aquatic systems, 33–82. Tech Publishers, Rijeka, Croatia. AKAIKE, H. 1973. Information theory as an extension of the maximum likelihood principle. In B. N. Petrov and F. Csaki [eds.], Second International Symposium on Information Theory, 267–281. Akademia Kiado, Budapest, Hungary. ANDERSSON, L. 2001. Margaritopsis (Rubiaceae, Psychotrieae) is a pantropical genus. Systematics and Geography of Plants 71: 73–85. ANDERSSON, L. 2002a. Re-establishment of Carapichea (Rubiaceae, Psychotrieae). Kew Bulletin 57: 363–374. ANDERSSON, L. 2002b. Relationships and generic circumscriptions in the Psychotria complex (Rubiaceae, Psychotrieae). Systematics and Geography of Plants 72: 167–202. ANDERSSON, L., AND J. H. E. ROVA. 1999. The rps16 intron and the phylogeny of the Rubioideae (Rubiaceae). Plant Systematics and Evolution 214: 161–186. BACKLUND, M., B. OXELMAN, AND B. BREMER. 2000. Phylogenetic relationships within the Gentianales based on ndhF and rbcL sequences, with particular reference to the Loganiaceae. American Journal of Botany 87: 1029–1043. BAKER, J. G. 1887. Further contributions to the Flora of Madagascar. – Second and final part. Journal of the Linnean Society of London, Botany 22: 441–472. BARRABÉ, L. 2013. Systématique et évolution du genre Psychotria (Rubiaceae) en Nouvelle Calédonie. Thèse de doctorat, Université de La Nouvelle Calédonie, New Caledonia. BARRABÉ, L., S. BUERKI, A. MOULY, A. P. DAVIS, J. MUNZINGER, AND L. MAGGIA. 2012. Delimitation of the genus Margaritopsis (Rubiaceae) in the Asian, Australasian and Pacific region, based on molecular phylogenetic inference and morphology. Taxon 61: 1251–1268. BARRABÉ, L., L. MAGGIA, Y. PILLON, F. RIGAULT, A. MOULY, A. P. DAVIS, AND S. BUERKI. 2014. New Caledonian lineages of Psychotria (Rubiaceae) reveal different evolutionary histories and the largest documented plant radiation for the archipelago. Molecular Phylogenetics and Evolution 71: 15–35. BREMEKAMP, C. E. B. 1934. Notes on the Rubiaceae of Surinam. Receuil des Travaux Botaniques Néerlandais 31: 248–308. BREMEKAMP, C. E. B. 1958. Monographie des genres Cremocarpon Boiv. ex Baill. et Pyragra Brem. (Rubiacées). Candollea 16: 147–177. BREMEKAMP, C. E. B. 1960. Les “Psychotria” bactériophiles de Madagascar. Notulae Systematicae 16: 41–54. BREMEKAMP, C. E. B. 1961. On the identity of the genera Mapouria Aubl. and Grumilea Gaertn. (Rubiaceae, Psychotrieae). Acta Botanica Neerlandica 10: 307–319. BREMEKAMP, C. E. B. 1962. Révision des Chassalia de Madagascar. Candollea 18: 195–238. BREMEKAMP, C. E. B. 1963. Sur quelques genres de Psychotriées (Rubiacées) et sur leurs répresentants Malgaches et Comoriens. Verhandelingen der Koninklijke Akademie van Wetenschappen, Afdeeling Natuurkunde. Section 2: 1–181. BREMEKAMP, C. E. B. 1966. Remarks on the position, the delimitation and the subdivision of the Rubiaceae. Acta Botanica Neerlandica 15: 1–33. BREMER, B. 1996. Phylogenetic studies within Rubiaceae and relationships to other families based molecular data. Opera Botanica of Belgica 7: 33–50. BREMER, B., K. ANDREASEN, AND D. OLSSON. 1995. Subfamilial, and tribal relationships in the Rubiaceae based on rbcL sequence data. Annals of the Missouri Botanical Garden 82: 383–397. 1120 AMERICAN JOURNAL OF BOTANY BREMER, B., AND T. ERIKSSON. 2009. Time tree of Rubiaceae: Phylogeny and dating of the family, subfamilies, and tribes. International Journal of Plant Sciences 170: 766–793. BREMER, B., R. J. JANSEN, B. OXELMAN, M. BACKLUND, H. LANTZ, AND K.J. KIM. 1999. More characters or more taxa for a robust phylogeny – case study from the coffee family (Rubiaceae). Systematic Biology 48: 413–435. BREMER, B., AND J.-F. MANEN. 2000. Phylogeny and classification of the subfamily Rubioideae. Plant Systematics and Evolution 225: 43–72. BREMER, B., AND M. THULIN. 1998. Collapse of Isertieae, re-establishment of Mussaendeae, and a new genus of Sabiceae; phylogenetic relationships based on rbcL data. Plant Systematics and Evolution 211: 71–92. BROWNE, P. 1756. The civil and natural history of Jamaica. Publisher unknown, London, UK. BURGER, W., AND C. M. TAYLOR. 1993. Family # 202 Rubiaceae. In W. Burger [ed.], Flora costaricensis. Fieldiana Botany 33: 1–333. CAPURON, R. 1973. Révision des Rubiacées de Madagascar et des Comores. Unpublished manuscript: Notes regroupées et mises en forme par J. Bosser, dactylographiées par F. Chauvet. Laboratoire Phanérogamie, Paris, France. CHASE, M. W., AND H. H. HILLS. 1991. Silica gel: An ideal material for preservation of leaf samples for DNA studies. Taxon 40: 215–220. DAVIS, A. P., D. BRIDSON, C. JARVIS, AND R. GOVAERTS. 2001. The typification and characterization of the genus Psychotria L. Botanical Journal of the Linnean Society 135: 35–42. DAVIS, A. P., R. GOVAERTS, D. M. BRIDSON, M. RUSHSAM, J. MOAT, AND N. A. BRUMMITT. 2009. A global assessment of distribution, diversity, endemism, and taxonomic effort in the Rubiaceae. Annals of the Missouri Botanical Garden 96: 68–78. DAVIS, A. P., R. GOVAERTS, AND M. BRIGGS. 2007. Indian Ocean Mapouria species transferred to Psychotria (Rubiaceae-Psychotrieae). Blumea 52: 245–262. DESSEIN, S., S. VANTHOURNOUT, AND F. NIYONGABO. 2011. Geophila erythrocarpa (Rubiaceae), a new species from D. R. Congo and Zambia. Blumea 56: 149–152. DOYLE, J. J., AND J. L. DOYLE. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin 19: 11–15. EDGAR, R. C. 2004. MUSCLE: Multiple alignment with high acuracy and high throughput. Nucleic Acids Research 32: 1792–1797. FITCH, W. M. 1971. Toward defining the course of evolution: Minimum change for a specific tree topology. Systematic Zoology 20: 406–416. FRIEDMANN, F. 1994. Rubiacées. In Flore des Seychelles: Dicotylédones, 573–678. Édition de l’ORSTOM, Institut Français de Recherche Scientifique pour le Développement en Coopération, Paris, France. GOVAERTS, R., L. ANDERSSON, E. ROBBRECHT, D. BRIDSON, D. DAVIS, I. SCHANZER, AND B. SONKÉ. 2013. World Checklist of Rubiaceae. The Board of Trustees of the Royal Botanic Gardens, Kew, England. GRUBER, C. W., A. G. ELLIOTT, D. C. IRELAND, P. G. DELPRETE, S. DESSEIN, U. GÖRABSSON, M. TRABI, ET AL. 2008. Distribution and evolution of circular miniproteins in flowering plants. Plant Cell 20: 2471–2483. HEPPER, F. N. 1960. (71) Proposal for the conservation of the generic Name Geophila D. Don (Rubiaceae) Fl. Nep.136 (1825) versus Geophila Bergeret (Liliaceae) Fl. Basses-Pyrén. 2: 184 (1803), 2nd ed., 306(1909), and rejection of the substitute names Carinta W. F. Wight in Contrib. U.S. Nat. Herb.9: 216 (1905) and Geocardia Standley in Contrib. U.S. Nat. Herb. 17: 444 (1914). Taxon 9: 88–89. HERRERA, C. M. 1989. Seed dispersal by animals: A role in angiosperm diversification. American Naturalist 133: 309–322. HIERN, W. P. 1877. Order LXX. Rubiaceae. In D. Oliver [ed.], Flora of tropical Africa, vol. 3. 249–280, Reeve, London, UK. HOOKER, J. D. 1873. Rubiaceae. In G. Bentham and J. D. Hooker [eds.], Genera plantarum 2, 7–151. Reeve & Co., London, UK. HOWARD, R. A. 1989. Flora of the Lesser Antilles: Dicotyledonae, vol. 6, part 3. Arnold Arboretum, Havard University, Boston, USA. HUELSENBECK, J., AND F. RONQUIST. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. HUXLEY, C. R., AND M. H. P. JEBB. 1991. The tuberous epiphytes of the Rubiaceae 1: A new subtribe—The Hydnophytinae. Blumea 36: 1–20. JACQUIN, N. J. 1760. Enumeratio systematica plantarum, quas in insulis Caribaeis vicinaque continente detexit novas, aut jam cognitas [Vol. 101 emedavit. Apud Theodorum Haak, Lugduni Batavorum (Leiden), Netherlands. KAINULAINEN, K., S. G. RAZAFIMANDIMBISON, AND B. BREMER. 2013. Phylogenetic relationships and new tribal delimitations in Ixoroideae (Rubiaceae). Botanical Journal of the Linnean Society 173: 387–408. KÅREHED, J., AND B. BREMER. 2007. The systematics of Knoxieae (Rubiaceae)—Molecular data and their taxonomic consequences. Taxon 56: 1051–1076. KHAN, S. A., S. G. RAZAFIMANDIMBISON, B. BREMER, AND S. LIEDE-SCHUMANN. 2008. Sabiceeae and Virectarieae (Rubiaceae, Ixoroideae): One or two tribes? New tribal and generic circumscriptions of Sabiceeae and biogeography of Sabicea s.l. Taxon 57: 7–23. KOEHBACH, J., A. F. ATTAH, A. BERGER, R. HELLINGER, T. M. KUTCHAN, E. J. CARPENTER, ET AL. 2013. Cyclotide discovery in Gentianales revisited: Identification and characterization of cyclic cystine-knot peptides and their phylogenetic distribution in Rubiaceae plants. Biopolymers 100: 438–452 (Peptide Sciences). KRÜGER, Å., S. G. RAZAFIMANDIMBISON, AND B. BREMER. 2012. Molecular phylogeny of the tribe Danaideae (Rubiaceae, Rubioideae). Another example of out-of-Madagascar dispersal. Taxon 61: 629–636. LACHENAUD, O., AND D. J. HARRIS. 2010. Three new species of Chassalia and Psychotria (Rubiaceae) from Central Africa. Edinburgh Journal of Botany 67: 219–233. LACHENAUD, O., Q. LUKE, B. TCHIENGUÉ, AND B. BYTEBIER. 2012. Chassalia magnificens sp. nov. and C. chrysoclada comb. nov. (Rubiaceae) from Central Africa. Nordic Journal of Botany 30: 129–135. LEMAIRE, B., O. LACHENAUD, C. PERSSON, E. SMETS, AND S. DESSEIN. 2012a. Screening for leaf-associated endophytes in the genus Psychotria (Rubiaceae). FEMS Microbiology Ecology 81: 364–372. LEMAIRE, B., S. V. OEVELEN, P. DE BLOCK, B. VERSTRAETE, E. SMETS, E. PRINSEN, AND S. DESSEIN. 2012b. Identification of the bacterial endosymbionts in leaf nodules of Pavetta (Rubiaceae). International Journal of Systematic and Evolutionary Microbiology 62: 202–209. LEMAIRE, B., P. VANDAMME, V. MERCKX, E. SMETS, AND D. DESSEIN. 2011. Bacterial leaf symbiosis in angiosperms: Host specificity without co-speciation. PLoS ONE 6(9): e24430. doi:10.1371/journal. pone.0024430. LINNAEUS, C. 1759. Systema naturae, 10th ed., vol. 2. Holmiae. Impensis direct, Laurentii Salvii, Stockholm, Sweden. MADDISON, W. P., AND D. R. MADDISON. 2010. Mesquite: A modular system for evolutionary analysis, version 2.72 [computer program]. Website http://mesquiteproject.org [accessed December 2013]. MILLER, I. M. 1990. Bacterial nodule symbiosis. Advances in Botanical Research 17: 163–234. MÜLLER, J. 1881. Rubiaceae. In C. von Martius [ed.], Flora braziliensis 6, part 5. Lipsiae Apud frid. Fleischer in comm. NEPOKROEFF, M., B. BREMER, AND K. J. SYSTMA. 1999. Reorganization of the genus Psychotria and tribe Psychotrieae (Rubiaceae) inferred from ITS and rbcL sequence data. Systematic Botany 24: 5–27. NOVOTNY, V., Y. BASSET, S. E. MILLER, G. D. WEIBLEN, B. BREMER, L. CIZEK, AND P. DROZD. 2002. Low host specificity of herbivorous insects in a tropical forest. Nature 416: 841–844. NYLANDER, J. 2004. MrAIC.pl. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden. NYLANDER, J. A. A., J. C. WILGENBUSCH, D. L. WARREN, AND D. L. SWOFORD. 2008. AWTY (Are We There Yet?): A system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics (Oxford, England) 24: 581–583. OLIVEIRA, L. O. DE, A. A. ROSSI, E. R. MARTINS, F. R. BATISTA, AND S. R. SILVA. 2010. Molecular phylogeography of Carapichea ipecacuanha, an amphitropical shrub that occurs in the understory of both semideciduous and evergreen forests. Molecular Ecology 19: 1410–1422. OLMSTEAD, R. G., AND P. A. REEVES. 1995. Evidence for the polyphyly of Scrophulariaceae based on chloroplast rbcL and ndhF sequences. Annals of the Missouri Botanical Garden 82: 176–193. OXELMAN, B., M. LIDÉN, AND D. BERGLUND. 1997. Chloroplast rps16 intron phylogeny of the tribe Sileneae (Carophyllaceae). Plant Systematics and Evolution 206: 393–410. July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE PEI, N., J.-Y. LIAN, D. L. ERICKSON, N. G. SWENSSON, W. J. KRESS, W.-H. YE, AND X.-J. GE. 2011. Exploring tree-habitat associations in a Chinese subtropical forest plot using a molecular phylogeny generated from DNA barcode loci. PLoS ONE 6(6): e21273. doi:10.1371/journal.pone.0021273 PETIT, E. 1964. Les espèces africaines du genre Psychotria L. (Rubiaceae) – I. Bulletin du Jardin Botanique d’État, Bruxelles 34: 1–229. PETIT, E. 1966. Les espèces africaines du genre Psychotria L. (Rubiaceae) – II (suite). Bulletin du Jardin Botanique d’État, Bruxelles 36: 65–146. PIESSCHAERT, F. 2001. Carpology and pollen morphology of Psychotrieae (Rubiaceae-Rubioideae). Towards a new tribal and generic delimitation. Doctoral thesis, Katholieke Universiteit Leuven, Faculteit Wetenschappen, Institut voor Plantkunde en Microbiologie, Laboratorium voor Systematiek, Leuven, Belgium. PIESSCHAERT, F., L. ANDERSSON, S. JANSEN, S. DESSEIN, E. ROBBRECHT, AND E. SMETS. 2000. Searching for the taxonomic position of the African genus Colletoecema (Rubiaceae): morphology and anatomy compared with an rps16-intron analysis of the Rubioideae. Canadian Journal of Botany 78: 288–304. PIESSCHAERT, F., S. JANSEN, S. HUYSMANS, E. SMETS, AND E. ROBBRECHT. 1999a. Chassalia petitiana (Rubiaceae—Psychotrieae), an overlooked epiphytic species hidden in the African canopy. Systematic Botany 24: 315–322. PIESSCHAERT, F., E. ROBBRECHT, A. D. POULSEN, AND E. SMETS. 1998. The tropical African Geophila ingens (Rubiaceae-Psychotrieae) reinvestigated. Nordic Journal of Botany 19: 87–92. PIESSCHAERT, F., E. ROBBRECHT, A. D. POULSEN, AND E. SMETS. 1999b. Pyrene and pollen observations in the pantropical genus Geophila (Rubiaceae-Psychotrieae). Nordic Journal of Botany 19: 93–99. PIESSCHAERT, F., E. ROBBRECHT, AND S. SMETS. 1999c. Chassalia subcordifolia, a new combination in African Rubiaceae (Rubioideae, Psychotrieae). Systematics and Geography of Plants 69: 189–194. QUEIROZ, C. DE S., F. R. DE CARVALHO BATISTA, AND L. O. DE OLIVEIRA. 2011. Evolution of the 5.8S nrDNA gene and internal transcribed spacers in Carapichea ipecacuanha (Rubiaceae) within a phylogeographic context. Molecular Phylogenetics and Evolution 59: 293–302. RAMBAUT, A. 1996. Se-Al: Sequence alignment editor. Available from http://evolve.zoo.ox.ac.uk/ [accessed August 2013]. RAMBAUT, A., AND A. J. DRUMMOND. 2009. Tracer version 1.5. University of Edinburgh, Edinburgh, UK. Available from http://tree.bio.ed.ac. uk/software/tracer/ [accessed September 2013]. RAZAFIMANDIMBISON, S. G., AND B. BREMER. 2002. Phylogeny and classification of Naucleeae (Rubiaceae) inferred from molecular (nrITS, rbcL, and trnT-F) and morphological data. American Journal of Botany 89: 1027–1041. RAZAFIMANDIMBISON, S. G., E. A. KELLOGG, AND B. BREMER. 2004. Recent origin and phylogenetic utility of divergent nrITS putative pseudogenes: A case study from Naucleeae (Rubiaceae). Systematic Biology 53: 177–192. RAZAFIMANDIMBISON, S. G., H. LANTZ, A. MOULY, AND B. BREMER. 2009. Molecular phylogenetics and generic assessment in the tribe Morindeae (Rubiaceae-Rubioideae): How to circumscribe Morinda L. to be monophyletic? Molecular Phylogenetics and Evolution 52: 879–886. RAZAFIMANDIMBISON, S. G., C. RYDIN, AND B. BREMER. 2008. Evolution and trends in the Psychotrieae alliance (Rubiaceae)—A rarely reported evolutionary change of many-seeded carpels from one-seeded carpels. Molecular Phylogenetics and Evolution 48: 207–223. REVEAL, J. L. 2012. Newly required infrafamilial names mandated by changes in the code of nomenclature for algae, fungi, and plants. Phytoneuron 33: 1–32. ROBBRECHT, E. 1975. Hymenocoleus, a new genus of Psychotrieae (Rubiaceae) from tropical Africa. Bulletin du Jardin Botanique National de Belgique 45: 273–300. ROBBRECHT, E. 1977. The tropical African genus Hymenocoleus (Rubiaceae, Psychotrieae): additions. Bulletin du Jardin Botanique National de Belgique 47: 3–29. ROBBRECHT, E. 1988. Tropical woody Rubiaceae. Opera Botanica Belgica 1: 1–271. ROBBRECHT, E., AND J.-F. MANEN. 2006. The major evolutionary lineages of the coffee family (Rubiaceae, angiosperms). Combined analysis (nDNA and cpDNA) to infer the position of Coptosapelta and Luculia, and supertree construction based on rbcL, rps16, trnL-trnF, and 1121 atpB-rbcL data. A new classification in two subfamilies, Cinchonoideae and Rubioideae. Systematics and Geography of Plants 76: 85–146. RONQUIST, F., AND J. HUELSENBECK. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. ROVA, J. H. E., P. G. DELPRETE, L. ANDERSSON, AND V. A. ALBERT. 2002. A trnL-F cpDNA sequence study of the Condamineeae-RondeletieaeSipaneeae complex with implications on the phylogeny of the Rubiaceae. American Journal of Botany 89: 145–159. RYDIN, C., K. KAINULAINEN, S. G. RAZAFIMANDIMBISON, J. E. E. SMEDMARK, AND B. BREMER. 2009a. Deep divergences in the coffee family and the systematic position of Acranthera. Plant Systematics and Evolution 278: 101–123. RYDIN, C., S. G. RAZAFIMANDIMBISON, AND B. BREMER. 2008. Rare and enigmatic genera (Dunnia, Schizocolea, Colletoecema), sisters to species-rich clades: Phylogeny and aspects of conservation biology in the coffee family. Molecular Phylogenetics and Evolution 48: 74–83. RYDIN, C., S. G. RAZAFIMANDIMBISON, A. KHODABANDEH, AND B. BREMER. 2009b. Evolutionary relationships in the Spermacoceae alliance (Rubiaceae) using information from six loci: Insights into systematic affinities of Neohymenopogon and Mouretia. Taxon 58: 793–810. SAGHAI-MAROOF, K. M., M. SOLIMAN, R. A. JORGENSEN, AND R. W. ALLARD. 1984. Ribosomal DNA spacer length polymorphism in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proceedings of the National Academy of Sciences, USA 81: 8014–8018. SCHATZ, G. E. 2001. Generic tree flora of Madagascar. Cromwell Press, Trowbridge, UK. SCHUMANN, K. 1891. Rubiaceae. In A. Engler and K. Prantl [eds.], Die natürlichen Pfanzenfamilien IV, vol. 4, 1–156. Whilhem Englelmann. Leipzig, Germany. SCHWARZ, G. 1978. Estimating the dimensions of a model. Annals of Statistics 6: 461–464. SIMMONS, M. P. 2004. Independence of alignment and tree search. Molecular Phylogenetics and Evolution 31: 874–879. SONKÉ, B., S. DESSEIN, H. TAEDOUMG, I. GROENINCKX, AND E. ROBBRECHT. 2008. A new species of Colletoecema (Rubiaceae) from Soputh Cameroon with a discussion of relationships among basal Rubioideae. Blumea 53: 533–547. SOZA, V. L., AND R. G. OLMSTEAD. 2010. Evolution of breeding systems and fruits in New world Galium and relatives (Rubiaceae). American Journal of Botany 97: 1630–1646. STADEN, R. 1996. The Staden sequence analysis package. Molecular Biotechnology 5: 233–241. STEYERMARK, J. A. 1972. Rubiaceae. In B. Marguire et al. [ed.], The botany of the Guyana highland—Part IX. Memoire New York Botanical Garden 23: 277–832. TAYLOR, C. M. 1996. Overview of the Psychotrieae (Rubiaceae) in the Neotropics. Opera Botanica Belgica 7: 261–270. TAYLOR, C. M. 2001. Overview of the Neotropical genus Notopleura (Rubiaceae, Psychotrieae), with the description of some new species. Annals of the Missouri Botanical Garden 88: 478–515. TAYLOR, C. M. 2004. The Neotropical Ronabea (Rubiaceae, Lasiantheae). Systematics and Geography of Plants 74: 35–42. TAYLOR, C. M. 2005. Margaritopsis (Rubiaceae, Psychotrieae) in the Neotropics. Systematics and Geography of Plants 75: 161–177. TAYLOR, C. M., AND R. E. G EREAU . 2013. The genus Carapichea (Rubiaceae, Psychotrieae). Annals of the Missouri Botanical Garden 99: 100–127. TAYLOR, C. M., D. H. LORENCE, AND R. E. GEREAU. 2010. Rubiacearum americanum magna hama pars XXV: The nocturnally flowering Psychotria domingensis-Coussarea hondensis group plus three other Mesoamerican Psychotria species transfer to Palicourea. Novon 20: 481–492. TAYLOR, C. M., J. A. STEYERMARK, P. G. DELPRETE, A. VINCENTINI, R. CORTÉS, D. ZAPPI, C. PERSSON, ET AL. 2004. Rubiaceae. In J. A. Steyermark, P. E. Berry, K. Yatskievych, and B. K. Holst [eds.], Flora of the Venezualan Guyana, 497–848. Missouri Botanical Garden Press, St. Louis, Missouri, USA. VERDCOURT, B. 1958. Remarks on the classification of the Rubiaceae. Bulletin du Jardin d’État 28: 209–281. 1122 AMERICAN JOURNAL OF BOTANY VERDCOURT, B. 1975. Studies in the Rubiaceae: Rubiaceae for the “Flora of tropical East Africa”: I. Kew Bulletin 30: 247–326. VERDCOURT, B. 1976. Rubiaceae (part 1). In R. M. Polhill [ed.], Flora of tropical East Africa. 1–414. Whitefriars Press, London, UK. VERDCOURT, B. 1977. A synopsis of the genus Chazaliella (Rubiaceae, Psychotrieae). Kew Bulletin 31: 785–818. VERDCOURT, B. 1983. Notes on Mascarenes Rubiaceae. Kew Bulletin 37: 521–570. VERDCOURT, B. 1989. 108. Rubiacées. In J. Bosser, T. Cadet, J. Guého, and W. Marais [eds.], Flore des Mascareignes, La Réunion, Maurice, Rodrigues, 1–135. M.S.I.R.I., O.R.S.T.O.M. & Kew, Port Louis, Mauritius. [Vol. 101 WIKSTRÖM, N., S. NEUPANE, J. KÅREHED, T. J. MOTLEY, AND B. BREMER. 2013. Phylogeny of Hedyotis L. (Rubiaceae: Spermacoceae): Redefining a complex Asian-Pacific assemblage. Taxon 62: 357–374. YANG, Z., AND B. RANNALA. 1997. Bayesian phylogenetic inference using DNA sequences: A Markov chain Monte Carlo method. Molecular Biology and Evolution 14: 717–724. YOKOYAMA, J., T. FUKUDA, AND H. TSUKAYA. 2003. Morphological and molecular variation in Mitchella undulata, with special reference to the systematic treatment of the dwarf form from Yakushima. Journal of Plant Research 116: 309–315. APPENDIX 1. Origins of the taxa used in the study and GenBank accession numbers. “....” = missing sequences; 1 Barrabé et al. (2012); 2 Queiroz et al. (2011); 3 Nepokroeff et al. (1999); 4 Oliveira et al. (2010); 5 Unpublished GenBank; 6 Andersson (2001); 7 Lemaire et al. (2012); 8 Andersson and Rova (1999); 9 Rydin et al. (2008); 10 Piesschaert et al. (2000); 11 Bremer and Manen (2000); 12 Razafimandimbison et al. (2008); 13 Andersson (2002b); 14 Bremer and Eriksson (2009); 15 Bremer (1996); 16 Yokoyama et al. (2003); 17 Razafimandimbison et al. (2009); 18 Sonké te al. (2008); 19 Bremer et al. (1999); 20 Bremer et al. (1995); 21 Bremer and Thulin (1998); 22 Backlund et al. (2000); 23 Rova et al. (2002); 24 Krüger et al. (2012); 25 Rydin et al. (2009a); 26 Rydin et al. (2009b); 27 Pei et al. (2011); 28 Barrabé et al. (2014); 29 Novotny et al. (2002); and 30 Andersson (2002a). Taxon, tribal classification, voucher information, country origins, accession numbers: nrETS, nrITS, atpB-rbcL, ndhF, rbcL, rps16, and trnT-F sequences. Amaracarpus nematopodus (F. Muell.) P.I. Forst., Psychotrieae, Barrabé et al. 1030 (NOU), Australia, ...., JX1550601, ...., JX1551051, ...., JX1551521, JX1550111; Amaracarpus novoguineensis (Warb. ex Boerl.) Valeton, Psychotrieae, Erik Nymann 479 (S), New Guinea, ...., KJ804785, ...., ...., ...., ...., KJ805381; Amaracarpus pubescens Blume var. sechellarum F.Friedmann, Psychotrieae, Senterre 5380 (SEY), Seychelles, KJ804599, KJ804786, KJ804402, KJ804988, KJ805582, KJ805187, KJ805382; Amaracarpus sp.-bu36, Psychotrieae, Drozd & Molem s.n. (PSF), New Guinea, KJ804596, KJ804787, KJ804403, KJ804989, KJ805583, KJ805188, KJ805383; Amaracarpus sp.-v74, Psychotrieae, Prodz & Molem s.n., New Guinea, KJ804597, KJ804788, ...., KJ804990, KJ805584, KJ805189, KJ805384; Apomuria bullata Bremek., Psychotrieae, Kårehed et al. 308 (S), Madagascar, KJ804598, KJ804789, KJ804404, KJ804991, KJ805585, KJ805190, KJ805385; Apomuria punctata Vatke-ai74, Psychotrieae, Luke 9021 (UPS), Kenya, ...., KJ804790, KJ804992, KJ804405, KJ805586, KJ805192, KJ805386; Apomuria punctata Vatke-ch22, Psychotrieae, Mouly 697 (P), Mayotte (Comores), KJ804599, KJ804791, KJ804406, KJ804993, KJ805587, KJ805192, KJ805387; Apomuria sp.-ck24, Psychotrieae, Randrianasolo 1118 (MO), Madagascar, KJ804600, KJ804792, KJ804407, KJ804994, KJ805588, KJ805193, KJ805388; Appunia guatemalensis Donn.Sm., Morindeae, Lundell 6675 (S), Sine loc., FJ90710417, AM94519112, AJ23400911, AM94525212, AJ28859311, AM94530612, AM94533212; Calycosia aff. lageniformis (Gillespie) A.C.Sm., Psychotrieae, Callmander et al. 962 (S), Fiji, KJ804601, KJ804793, KJ804408, KJ804995, KJ805589, KJ805194, KJ805389; Calycosia macrocyatha Fosberg, Psychotrieae, Rova and Gustavsson 2486 (GB), Fiji, ...., ...., ...., ...., ...., AF41067113, ....; Calycosia magnifica Gillespie, Psychotrieae, Smith 666 (S), Fiji, KJ804602, KJ804794, ...., ...., ...., ...., ....; Carapichea ipecacuantha (Brot.) L.Andersson, Palicoureeae, ...., HM9929242, DQ1317735, ....., AJ0021843, AF37004030, GU3850334; Carapichea ligularis (Rudge) Delprete, Palicoureeae, ...., AF1493905, ...., ...., ...., AF1475676, ....; Carinta repens (G. Forst.) L.B.Sm. & Downs var. americana Bremek., Palicoureeae, Balslev et al. 97211 (AAU), Ecuador, ...., AF41068613, ...., ....., ...., AF3698466, ....; Carinta repens (G. Forst.) L.B.Sm. & Downs var. comorensis Bremek., Palicoureeae, Mouly 653 (P), Comores, KJ804603, KJ804795, ...., KJ804996, KJ805590, KJ805195, KJ805390; Chassalia aff. gaertneroides (Cordem.)Verdc., Palicoureeae, Razafimandimbison et al. 1224 (S), Reunion, KJ804604, KJ804796, ...., KJ804797, KJ805591, KJ805196, KJ805191; Chassalia albiflora K.Krausse, Palicoureeae, Farkas et al. 89282 (UPS), Tanzania, KJ804605, KJ804797, KJ804409, KJ804998, KJ805592, KJ805197, KJ805392; Chassalia betsilensis Bremek., Palicoureeae, Razakamalala 6452 (S), Madagascar, KJ804606, KJ804798, KJ804410, KJ804999, KJ805593, KJ805198, KJ805393; Chassalia bojeri Bremek.-cg45, Palicoureeae, Bremer et al. 5250 (S), Madagascar, KJ804607, KJ804799, KJ804427, KJ805000, KJ805494, KJ805199, KJ805394; Chassalia bojeri Bremek.-cm25, Palicoureeae, Razafimandimbison et al. 1195 (S), Madagascar, KJ804608, KJ804800, ...., KJ805001, KJ805595, KJ805200, KJ805395; Chassalia boryana DC., Palicoureeae, Krüger et al. 45 (S), Mauritius, KJ804609, KJ804801, KJ804411, KJ805002, KJ805596, KJ805201, KJ805396; Chassalia bosseri Verdc., Palicoureeae, Joel Dupont s.n. (REU), Reunion, KJ804610, KJ804802, ...., KJ805003, KJ805597, KJ805202, KJ805397; Chassalia capitata DC., Palicoureeae, Razafimandimbison et al. 858 (S), Mauritius, KJ804611, KJ804803, KJ804412, KJ805004, KJ805598, KJ805203, KJ805398; Chassalia comorensis Bremek., Palicoureeae, Mouly 665 (P), Mayotte (Comores), KJ804612, KJ804804, KJ804413, KJ805005, KJ805599, KJ805204, KJ805399; Chassalia coralloides (Cordem.) Verdc., Palicoureeae, Razafimandimbison et al. 1219 (S), Reunion, KJ804613, KJ804805, ...., KJ805006, KJ805600, KJ805205, KJ805400; Chassalia coriacea Verdc. var. coriacea, Palicoureeae, Razafimandimbison et al. 842 (S), Mauritius, KJ804614, KJ804806, KJ804414, KJ805007, KJ805601, KJ805206, .....; Chassalia coriacea Verdc. var. johnstonii Verdc., Palicoureeae, Krüger & Razafimandimbison 54 (S), Mauritius, KJ804615, KJ804807, KJ804415, KJ805008, KJ805602, KJ805207, KJ805401; Chassalia cristata (Hiern) Bremek., Palicoureeae, R.A.M.Geesteranus 6228 (S), Kenya, ...., KJ804808, ...., KJ805009, KJ805603, KJ805209, KJ805402; Chassalia discolor K.Schum.-cl20, Palicoureeae, Lundgreen 324 (UPS), Tanzania, KJ804616, KJ804809, KJ804416, KJ805010, KJ805604, KJ805209, KJ805403; Chassalia discolor K.Schum.-cl21, Palicoureeae, Thulin and Mhoro 3205 (UPS), Tanzania, KJ804617, KJ804810, KJ804417, KJ805011, KJ805605, KJ805210, KJ805404; Chassalia eurybotrya Bremek., Palicoureeae, Razakamalala 6179 (S), Madagascar, KJ804618, KJ804811, ...., KJ805012, KJ805606, KJ805211, KJ805405; Chassalia gaertneroides (Cordem.) Verdc., Palicoureeae, Razafimandimbison et al. 1223 (S), Reunion, KJ804619, KJ804812, ...., KJ805013, KJ805607, KJ805212, KJ805406; Chassalia grandifolia DC., Palicoureeae, Razafimandimbison & Krüger 825 (S), Mauritius, KJ804620, KJ804813, KJ804418, KJ805014, KJ805608, KJ805213, KJ805407; Chassalia kenyensis Verdc., Palicoureeae, A. Hemp 5260 (S), Tanzania, ...., KJ804814, ...., KJ805015, KJ805609, KJ805214, KJ805408; Chassalia kolly (Schumach.) Hepper, Palicoureeae, Jongkind and Noyes 1283 (UPS), Ghana, KJ804621, KJ804815, KJ804419, KJ805016, KJ805610, KJ805215, KJ805409; Chassalia lanceolata (Poir.) A.Chev., Palicoureeae, Razafimandimbison et al. 814 (S), Mauritius, KJ804622, KJ804816, KJ804420, KJ805017, KJ805611, KJ805216, KJ805410; Chassalia macrodiscus K.Schum., Palicoureeae, Dessein et al. 1823 (BR), Gabon, ...., ...., ...., ...., ...., JN6431097, JN6433877; Chassalia magnifolia Bremek., Palicoureeae, Razakamalala 6528 (S), Madagascar, KJ804624, KJ804817, KJ804421, KJ805018, KJ805612, KJ805217, KJ805411; Chassalia parvifolia K.Schum.-bo34, Palicoureeae, Luke 9107 (UPS), Tanzania, KJ804624, KJ804818, KJ804422, KJ805019, KJ805613, KJ805218, KJ805412; Chassalia parvifolia K.Schum.-cl22, Palicoureeae, Thulin and Mhoro 3194 (UPS), Tanzania, KJ804625, KJ804819, KJ804423, KJ805020, KJ805614, KJ805219, KJ805413; Chassalia petrinensis Verdc., Palicoureeae, Razafimandimbison & Krüger 853 (S), Mauritius, KJ804626, KJ804820, KJ804424, KJ805021, KJ805615, KJ805220, KJ805414; Chassalia sp.1-VIET, Palicoureeae, HNK 610 (K), Vietnam, ...., JX1550871, ...., JX1551321, ...., JX1551771, July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE JX1550391; Chassalia sp.2-VIET, Palicoureeae, Briggs 114 (K), Vietnam, ...., JX1550901, ...., JX1551351, ...., JX1551791, JX1550421; Chassalia sp.-ac52, Palicoureeae, Davis 2580 (K), Madagascar, KJ804627, KJ804821, KJ804425, KJ805022, KJ805616, KJ805221, KJ805415; Chassalia sp.-bk67, Palicoureeae, Razafimandimbison 554 (UPS), Madagascar, KJ804628, KJ804822, KJ804426, ...., KJ805617, KJ805222, KJ805416; Chassalia sp.-ch19, Palicoureeae, Mouly 594 (P), Mayotte (Comores), KJ804629, KJ804823, KJ804428, KJ805023, KJ805618, KJ805223, KJ805417; Chassalia sp.-ck25, Palicoureeae, Malcomber 3035 (MO), Malaysia, ...., KJ804824, KJ804429, KJ805024, KJ805619, KJ805224, KJ805418; Chassalia sp.-ck26, Palicoureeae, Malcomber 3014 (MO), Brunei, KJ804630, KJ804825, KJ804430, KJ805025, KJ805620, KJ805225, KJ805419; Chassalia sp.-ck28, Palicoureeae, Malcomber & Hemingway 3005 (MO), Brunei, KJ804631, KJ804826, KJ804431, KJ805026, KJ805621, KJ805226, KJ805420; Chassalia sp.ck30, Palicoureeae, Kainulainen et al. 008 (S), Vietnam, KJ804632, KJ804827, KJ804432, KJ805027, KJ805622, KJ805227, KJ805421; Chassalia sp.-ck31, Palicoureeae, Kainulainen et al. 33 (S), Vietnam, KJ804633, KJ804828, KJ804433, KJ805028, KJ805623, KJ805228, KJ805422; Chassalia sp.-ck32, Palicoureeae, Razafimandimbison et al. 743 (S), Vietnam, KJ804634, KJ804829, KJ804434, KJ805029, KJ805624, KJ805229, KJ805423; Chassalia sp.-ck33, Palicoureeae, Kainulainen et al. 007 (S), Vietnam, KJ804635, KJ804830, KJ804435, KJ805030, KJ805625, KJ805230, KJ805424; Chassalia sp.-ck34, Palicoureeae, Razafimandimbison et al. 790 (S), Vietnam, KJ804636, KJ804831, KJ804436, KJ805031, KJ805626, KJ805231, KJ805425; Chassalia sp.-ck35, Palicoureeae, Krüger et al. 002 (S), Vietnam, KJ804637, KJ804832 KJ804437, KJ805032, KJ805627, KJ805232, KJ805426; Chassalia sp.-ck36, Palicoureeae, Krüger et al. 007 (S), Vietnam, KJ804638, KJ804833, KJ804438, KJ805033, KJ805628, KJ805233, KJ805427; Chassalia sp.-ck39, Palicoureeae, Razakamalala 6247 (S), Madagascar, KJ804639, KJ804834, KJ804439, KJ805034, KJ805629, KJ805234, KJ805428; Chassalia sp.-ck40, Palicoureeae, Razafimandimbison et al. 1138 (S), Madagascar, KJ804640, KJ804835, KJ804440, KJ805035, KJ805630, KJ805235, KJ805429; Chassalia sp.ck42, Palicoureeae, Kainulainen et al. 120 (S), Madagascar, KJ804641, KJ804836, ...., KJ805036, KJ805631, KJ805236, KJ805430; Chassalia sp.-ck43, Palicoureeae, Kainulainen et al. 142 (S), Madagascar, KJ804642, KJ804837, KJ804441, KJ805037, KJ805632, KJ805237, KJ805431; Chassalia sp.-ck44, Palicoureeae, Razafimandimbison et al. 1145 (S), Madagascar, KJ804643, KJ804838, KJ804442, KJ805038, KJ805633, KJ805238, KJ805432; Chassalia sp.-cl17, Palicoureeae, Iversen and Mziray 87184 (UPS), Tanzania, KJ804644, ...., KJ804443, KJ805039, ...., KJ805239, KJ805433; Chassalia sp.-cl19, Palicoureeae, J. G. Adam s,n, (UPS), Liberia, KJ804645, KJ804839, ...., KJ805040, KJ805634, KJ805240, KJ805434; Chassalia sp.-cm17, Palicoureeae, Razafimandimbison et al. 1108 (S), Madagascar, KJ804646, KJ804840, KJ804444, KJ805041, KJ805635, KJ805241, KJ805435; Chassalia sp.cm18, Palicoureeae, Razafimandimbison et al. 1092 (S), Madagascar, KJ804647, KJ804841, KJ804445, KJ805042, KJ805636, KJ805242, KJ805436; Chassalia sp.-cm24, Palicoureeae, Razafimandimbison et al. 1126 (S), Madagascar, ...., KJ804842, KJ804426, KJ805043, KJ805637, KJ805243, KJ805437; Chassalia sp.-cm26, Palicoureeae, Kainulainen et al. 71 (S), Madagascar, KJ804648, KJ804843, ...., KJ805044, KJ805638, KJ805244, KJ805438; Chassalia sp.-cm47, Palicoureeae, Razafimandimbison et al. 1224a (S), Madagascar, KJ804649, KJ804844, KJ804447, KJ805045, KJ805639, KJ805245, KJ805439; Chassalia sp.cm62, Palicoureeae, Kainulainen et al. 203 (S), Madagascar, KJ804650, KJ804845, KJ804448, KJ805046, KJ805640, KJ805246, 5440; Chassalia sp.-cm64, Palicoureeae, Kainulainen et al. 217 (S), Madagascar, ...., KJ804846,...., KJ805047, KJ805641, KJ805247, KJ805441; Chassalia sp.SUMA, Palicoureeae, De Kok 1297 (K), Sumatra (Indonesia), ...., JX1550881, ...., JX1551331, ...., JX1551781, JX1550401; Chassalia subcordatifolia (De Wild.) Piesschaert, Palicoureeae, ...., AF41068313, ...., ...., ....., AF3698406, ....; Chassalia subochreata (De Wild.) Robyns,, Palicoureeae, Frimodt-Møller 2 (C), Tanzania, ...., ...., ...., ...., ....., AF3698416, .....; Chassalia ternifolia (Baker) Bremek., Palicoureeae, Razakamalala 6484 (S), Madagascar, KJ804651, KJ804847, KJ804449, KJ805048, KJ805642, KJ805248, KJ805442; Chassalia umbraticola Vatke, Palicoureeae, Luke 8321 (UPS), Kenya, KJ804652, KJ804848, KJ804450, KJ805049, KJ805643, KJ805249, KJ805443; Chassalia vanderystii (De Wild.)Verdc., Palicoureeae, Walters and Niangadouma 1210 (MO), Gabon, KJ804653, KJ804849, KJ804451, KJ805050, 1123 KJ805644, KJ805250, KJ805444; Chassalia violacea K.Schum. var. violacea, Palicoureeae, Thulin and Mhoro 3195 (UPS), Tanzania, KJ804654, KJ804850, KJ804452, KJ805051, KJ805645, KJ805251, KJ805445; Chassalia zimmermannii Verdc., Palicoureeae, Borhidi et al. 85289 (UPS), Tanzania, KJ804655, KJ804851, KJ804453, KJ805052, KJ805646, KJ805252, KJ805446; Chazaliella abrupta (Hiern) E.M.A.Petit var. abrupta, Palicoureeae, Luke 10016 (UPS), Tanzania, KJ804656, KJ804852, KJ804454, KJ805053, KJ805647, ...., KJ805447; Chazaliella lophoclada (Hiern)E.M.A.Petit, Palicoureeae, J.G.Adam 28554 (UPS), Cameroon, KJ804657, KJ804854, ....., ...., ....., ...., ....; Chazaliella macrocarpa Verdc., Palicoureeae, Pierlot 2108 (BR), Republic Democratic of Congo, ...., ...., ...., ...., ...., AF3698426, ....; Chazaliella rotundifolia (R.D.Good) E.M.A.Petit, Palicoureeae, Staudt 119 (S), Cameroon, ...., KJ804855, ...., ...., ...., ...., ....; Chazaliella sciadephora (Hiern) E.M.A.Petit & Verdc., Palicoureeae, Andersson and Nilsson 2282 (GB), Gabon), ...., ...., ...., ...., ...., AF3698436, ....; Chazaliella sciadephora (Hiern)E.M.A.Petit & Verdc.-ck46, Palicoureeae, Gereau et al. 5596 (MO), Cameroon, KJ804658, KJ804856, KJ804455, KJ805054, KJ805648, KJ805253, KJ805448; Chazaliella sp., Palicoureeae, Cable et al. 1350 (K), Cameroon, ...., ...., ...., ...., ...., AF0013378, ....; Chazaliella sp.-cl95, Palicoureeae, Bipinde Urwardgeniet 4281 (S), Cameroon, ...., KJ804853, KJ804456, ...., ...., KJ805254, KJ805449; Coelospermum truncatum (Wall.)Baill., Morindeae, Razafimandimbison et al. 776 (S), Vietnam, KJ804659, KJ804857, KJ804457, KJ805055, KJ805649, KJ805255, KJ805450; Colletoecema dewevrei (De Wild.) E.M.A.Petit, Colletoecemeae, Lisowski 47195 (K), unknown, ...., KJ804858, DQ1317135, EU1454099, EU1454579, AF12927210, EU1455329; Craterispermum longipedunculatum Verdc., Craterispermeae, Luke 9196 (UPS), Tanzania, KJ804660, KJ804859, KJ804458, KJ805056, KJ805650, KJ805256, KJ805451; Cremocarpon boivinianum Baill., Psychotrieae, Mouly 696 (P), Mayotte (Comores), KF67579328, KF67590928, KJ80445928, KF67599728, KJ80565128, KF67608528, KF67617328; Cremocarpon fissicorne Bremek.-cd62, Psychotrieae, Davis 2540 (K), Madagascar, KJ804661, KJ804860, KJ804460, KJ805057, KJ805652, KJ805257, KJ805452; Cremocarpon fissicorne Bremek.-ck49, Psychotrieae, Kainulainen et al. 179 (S), Madagascar, KJ804662, ...., KJ804461, KJ805058, KJ805653, KJ805258, KJ805453; Cremocarpon floribundum Bremek., Psychotrieae, Razafimandimbison et al. 1269 (TAN), Madagascar, KJ804663, ...., KJ804462, KJ805059, KJ805654, KJ805259, KJ805454; Cremocarpon lantzii Bremek.-am69, Psychotrieae, Razafimandimbison 517 (UPS), Madagascar, KJ804664, KJ804861, KJ804463, KJ805060, AM11722214, AM11729614, AM11735614; Cremocarpon lantzii Bremek.-cd65, Psychotrieae, McPherson et al. 18327 (MO), Madagascar, KF67579428, KF67591028, KJ80446428, KF67599828, KJ805655, KF67608628, KF676174; Cremocarpon Lantzii Bremek.-ck47, Psychotrieae, Kainulainen et al. 84 (S), Madagascar, KJ804665, KJ804862, KJ804465, KJ805061, KJ805656, KJ805260, KJ805455; Cremocarpon pulchristipulum Bremek.-cd61, Psychotrieae, Ratovao et al. 2690 (K), Madagascar, KJ804666, KJ804863, KJ804466, KJ805062, KJ805657, KJ805261, KJ805456; Cremocarpon pulchristipulum Bremek.-ck48, Psychotrieae, Rakotovao et al. 2690 (MO), Madagascar, KJ804667, KJ804864, KJ804467, KJ805063, KJ805658, KJ805262, KJ805457; Cremocarpon sp.-cd63, Psychotrieae, Davis 2577 (K), Madagascar, KJ804668, KJ804865, KJ804468, KJ805064, KJ805659, KJ805263, KJ805458; Cremocarpon tenuifolium-cc44 Bremek., Psychotrieae, Bremer et al. 5104 (S), Madagascar, KJ804669, KJ804866, KJ804469, KJ805065, KJ805660, KJ805264, KJ805459; Cremocarpon tenuifolium Bremek.-cc45, Psychotrieae, Bremer et al. 5128 (S), Madagascar, KJ804670, KJ804867, KJ804470, KJ805066, KJ805661, KJ805265, KJ805460; Damnacanthus indicus C.F.Gaertn., Mitchelleae, Bremer 3107 (S), Sine loc., KJ804671, AY5140613, AJ23401511, AM94525612, Z6879315, AF3316473, AM94533512; Dolianthus vaccinioides C.H.Wright, Psychotrieae, ...., ...., ...., ....., ...., AF41068513, JN6433897; Gaertnera vaginata Lam., Gaertnereae, Razafimandimbison et al. 1216a (S), Reunion, KJ804672, KJ804868, KJ804471, KJ805067, KJ805662, KJ805266, KJ805461; Gentingia subsessilis (King & Gamble) J.T.Johanss., Prismatomerideae, Low and Wong s.n. (KLU), Malaysia, KJ804673, KJ804869, KJ804472, KJ805068, ...., ...., KJ805462; Geophila cordifolia Miq., Palicoureeae, Hammel 18062 (MO), Costa Rica, ...., AF0720153, ...., ...., ...., ...., ....; Geophila gerrardii Baker-cl49, Palicoureeae, Kainulainen et al. 81 (S), Madagascar, KJ804674, KJ804870, KJ804473, KJ805069, KJ805663, KJ805267, KJ805463; 1124 AMERICAN JOURNAL OF BOTANY Geophila gerrardii Baker-cm48, Palicoureeae, Razafimandimbison et al. 1230 (S), Madagascar, KJ804675, KJ804871, KJ804474, KJ805070, KJ805664, KJ805268, KJ805464; Geophila gerrardii Baker-cm50, Palicoureeae, Razafimandimbison et al. 1244 (S), Madagascar, KJ804676, KJ804872, KJ804475, KJ805071, KJ805665, KJ805269, KJ805465; Geophila ingens Wernham, Palicoureeae, Poulsen et al. 1252 (C), Uganda, ...., ...., ...., ...., ...., AF3698446, ....; Geophila macropoda (Ruiz & Pav.) DC., Palicoureeae, National Bot. Gard. Belgium, acc. 19841045, New World, ...., AF0720173, ...., ...., ...., ...., ....; Geophila obvallata Didr., Palicoureeae, Luke 9037 (UPS), Kenya, KJ804677, AM94519612, KJ804476, AM94525912, AM11722814, AF3698456, EU1455699; Geophila repens (L.) I.M.Johnst. var. repens, Palicoureeae, Munzinger 3649 (NOU), Vanuatu, ..., JX1550791, ...., JX1551241, ...., ...., JX1550311; Geophila repens L. var. repens-b65, Palicoureeae, Jonsson 2506 (UPS), Cook Islands, ...., KJ804873, KJ804477, KJ805072, KJ805666, KJ805270, KJ805466; Geophila repens (L.) I.M.Johnst. var. repens-cl10, Palicoureeae, Fries and Gilbert Vollesen 4127 (UPS), Ethiopia, KJ804678, ...., ...., KJ805073, KJ805667, KJ805271, KJ805467; Geophila repens (L.) I.M.Johnst. var. repens-cm53, Palicoureeae, Razafimandimbison et al. 1254 (S), Madagascar, KJ804679, KJ804874, KJ804478, KJ805074, KJ805668, KJ805272, KJ805468; Geophila tenuis (Mull.Arg.) Standl., Palicoureeae, ...., AF0720163, ...., ...., ...., AF0013388, ....; Gynochthodes kanalensis (Baill. ex Guillaumin) Razafim. & B.Bremer, Morindeae, Mouly 173 (P), New Caledonia, KJ804680, KJ804875, KJ804479, KJ805075, KJ805669, KJ805273, KJ805469; Hydnophytum grandiflorum Valeton, Psychotrieae, Rova 2445 (GB), Fiji, KJ804681, KJ804876, KJ804480, KJ805076, KJ805670, KJ805274, KJ805470; Hymenocoleus hirsutus (Benth.) Robbr., Palicoureeae, Malaisse 14528 (?), Cult. National Bot. Gard. Belgium, accession 1995116, KJ804682, AF0720183, KJ804481, KJ805077, AJ0021783, AF3698486, KJ805471; Hymenocoleus scaphus (K.Schum.) Robbr., Palicoureeae, ...., ...., ...., ...., ...., ...., ...., AF3698496, ....; Margaritopsis acuifolia C.Wright, Palicoureeae, Ekman 10248 (UPS), Cuba, KJ804683, AM94519812, AM94522512, KJ805078, AM11724714, AF0013408, KJ805472; Margaritopsis astrellantha (Wernham) L. Andersson, Palicoureeae, Zappi 938 (K), Brazil, ...., JX1550961, ...., JX1551421, ...., JX1551851, JX155047-81; Margaritopsis boliviana (Standl.) C.M.Taylor, Palicoureeae, Zappi 973 (K), Brazil, ...., JX1550971, ...., JX1551431, ...., JX155186-71, JX155049-501; Margaritopsis guianensis (Bremek.) C.M.Taylor, Palicoureeae, Zappi 980 (K), Brazil, ...., JX1550981, ...., JX1551441, ...., JX1551881, JX155051-21; Margaritopsis kappleri (Miq.) C.M.Taylor, Palicoureeae, Zappi 921 (K), Brazil, ...., JX1550951, ...., JX1551411, ...., JX1551841, JX1550461; Margaritopsis membranacea (Gillespie) L.Andersson, Palicoureeae, Barrabé 1093 (S), Fiji, KJ804684, KJ804877, KJ804482, KJ805079, KJ805671, KJ805275, KJ805473; Margaritopsis microdon (DC.) C.M.Taylor, Palicoureeae, ...., AF0720133, ...., ...., JQ5937935, AF3698616, ....; Margaritopsis sp.1-VIET, Palicoureeae, Davis 4031 (K), Vietnam, ...., JX1550811, ...., JX1551261, ...., JX1551721, JX1550331; Margaritopsis sp.2-VIET, Palicoureeae, HNK 614 (K), Vietnam, ...., JX1550831,...., JX1551281, ...., JX1551731, JX1550351; Mitchella repens L., Mitchelleae, Petterson and Mayfield 7369 (MEXU), Mexico, KJ804685, AB10353516, AM94522312, AM94525812, Z6880515, AF0014418, AM94533712; Morinda buchii Urb., Morindeae, Ekman 2452 (S), Haiti, FJ90712017, FJ90705517, KJ804483, KJ805080, KJ805672, KJ805276, FJ90699217; Mymecodia tuberosa Jack., Psychotrieae, Andreasen 341 (UPS), Bergi. Bot Gard., KJ804686, KF67591328, KJ804484, KF67600128, KJ805673, KF67608928, KF67617728; Notopleura guadalupensis (DC.) C.M.Taylor, Palicoureeae, Howard 15644 (S), Puerto Rico, ...., AF1493845, ...., ...., ...., AF1475626, ....; Notopleura tapajozensis (Standl.) Bremek., Palicoureeae, Zappi 869 (K), Brazil, ...., JX1550941, ...., JX1551401, ...., JX1551831, JX1550451; Notopleura uliginosa (Sw.) Bremek., Palicoureeae, ...., AF1494085, ...., ...., ...., AF1475816, ....; Ophiorrhiza mungos L., Ophiorrhizeae, Bremer 3301 (S), Cult. Bot. Gard. Uppsala University, ...., ...., FJ22654118, AJ13083819, X8365620, AF0040646, DQ66215123; Palicourea alpina (Sw.) DC., Palicoureeae, Rova 2246 (GB), Cuba, KJ804687, KJ804878, KJ804485, KJ805081, KJ805674, KJ805277, KJ805474; Palicourea crocea (Sw.) Schult., Palicoureeae, Cordiero 2736 (SP), New World, KJ804688, AF1493225, AM94524712, AM94528012, AM11725314, AF1475105, AM94535912; Palicourea quadrilateralis C.M.Taylor, Palicoureeae, Alzate 229 (GB), Colombia, KJ804689, KJ804879, KJ804486, KJ805082, KJ805675, KJ805278, KJ805475; Palicourea triphylla DC., Palicoureeae, Persson & Gustafsson 310 (GB), [Vol. 101 Ecuador, ...., KJ804880, KJ804487, KJ805083, KJ805676, KJ805279, KJ805476; Psathura badopedina Verdc.-cm51, Psychotrieae, Razafimandimbison et al. 1249 (S), Madagascar, KJ804690, KJ804881, KJ804488, KJ805084, KJ805677, KJ805280, KJ805477; Psathura badopedina Verdc.-cm52, Psychotrieae, Razafimandimbison et al. 1250 (S), Madagascar, KJ804691, KJ804882, KJ804489, KJ805085, KJ805678, KJ805281, KJ805478; Psathura borbonica J.F.Gmel.-cc66, Psychotrieae, Razafimandimbison et al. 821 (S), Mauritius, KJ804693, KJ804884, KJ804491, KJ805087, KJ805680, KJ805283, KJ805480; Psathura borbonica J.F.Gmel-cl74, Psychotrieae, Razafimandimbison et al. 1221 (S), Reunion, KJ804692, KJ804883, KJ804490, KJ805086, KJ805679, KJ805282, KJ805479; Psathura lutescens Bremek., Psychotrieae, Razafimandimbison et al. 1059 (S), Madagascar, KJ804694, KJ804885, ...., KJ805088, KJ805681, KJ805284, KJ805481; Psathura myrtifolia A.Rich. ex DC., Psychotrieae, Razafimandimbison et al. 835 (S), Mauritius, KJ804695, KJ804886, KJ804493, KJ805089, KJ805682, KJ805285, KJ805482; Psathura sp.-ac50, Psychotrieae, Davis 2270 (K), Madagascar, KJ804696, KJ804887, KJ804494, KJ805090, KJ805683, KJ805286, KJ805483; Psathura terniflora A.Rich ex DC., Psychotrieae, Coode 4698 (K), Mauritius, KF67580128, KF67591428, KJ804495, KF67600228, KJ805684, KF67609028, KF67626028; Psychotria aff. augagneri Hochr., Psychotrieae, Razafimandimbison et al. 1180 (S), Madagascar, KJ804697, KJ804888, KJ804496, KJ805091, KJ805685, KJ805287, KJ805484; Psychotria aff. glaucifolia A.P.Davis & Govaerts, Psychotrieae, Razakamalala 6220 (S), Madagascar, KJ804698, KJ804889, KJ804497, KJ805092, KJ805686, KJ805288, KJ805485; Psychotria aff. iringensis Verdc., Psychotrieae, Kayombo 1896 (S), Tanzania, ...., KJ804890, KJ804498, KJ805093, KJ805687, KJ805289, KJ805486; Psychotria amboniana K.Schum., Psychotrieae, Luke 8344 (UPS), Kenya, KJ804699, AM94521512, AM94524812, AM94528112, AM94530212, AM94532812, AM94536012; Psychotria ammericola Guillaumin, Psychotrieae, McPherson & Munzinger 735 (UPS), New Caledonia, KJ804700, KJ804891, KJ804499, KJ805094, KJ805688, KJ805290, KJ805487; Psychotria anceps Kunth., Psychotrieae, ...., AF1493615, ...., ...., ...., AF14754413, JN0536507; Psychotria andapae A.P.Davis & Govaerts, Psychotrieae, Bremer et al. 5203 (S), Madagascar, KJ804701, KJ804892, KJ804500, KJ805095, KJ805689, KJ805291, KJ805488; Psychotria andevorantensis Bremek., Psychotrieae, Razakamalala 6537 (S), Madagascar, KJ804702, KJ804893, KJ804576, KJ805096, KJ805690, KJ805292, KJ805489; Psychotria ankafinensis (K.Schum.) A.P.Davis-ck62, Psychotrieae, Razakamalala 6489 (S), Madagascar, KJ804703, KJ804894, KJ804501, KJ805097, KJ805691, KJ805293, KJ805490; Psychotria ankafinensis (K.Schum.) A.P.Davis-ck67, Psychotrieae, Razakamalala 6568 (S), Madagascar, KJ804704, KJ804895, KJ804502, KJ805098, KJ805692, KJ805294, KJ805491; Psychotria asiatica L., Psychotrieae, ...., JX1550821, ...., JX1551271, JN4073735, AF3698546, JX1550341; Psychotria asiatica L., Psychotrieae, ...., FJ9803875, ...., ...., HQ41511927, ...., JN6435245; Psychotria asiatica L.-cm11, Psychotrieae, Kainulainen et al. 38 (S), Vietnam, ...., KJ804896, KJ804503, KJ805099, KJ805693, KJ805295, KJ805492; Psychotria asiatica L.-cm12, Psychotrieae, Razafimandimbison et al. 752 (S), Vietnam, KJ804705, KJ804897, KJ804504, KJ805100, KJ805694, KJ805296, KJ805493; Psychotria baviensis Pit., Psychotrieae, Krüger et al. 10 (S), Vietnam, KJ804706, KJ804898, KJ804505, KJ805101, KJ805695, KJ805297, KJ805494; Psychotria bullulata Bremek., Psychotrieae, Razakamalala 6542 (S), Madagascar, KJ804707, KJ804899, KJ804506, KJ805102, KJ805696, ...., KJ805495; Psychotria camerunensis E.M.A.Petit, Psychotrieae, JN0496897, JN0497437, ...., ....., ...., JN0538527, JN0539497; Psychotria camptopus Verdc., Psychotrieae, Maurin 38 (K), Cameroon, ...., JX1550841, ...., JX1551291, ...., JX1551741, JX1550361; Psychotria capensis (Eckl.) Vatke, Psychotrieae, Bremer 4264 (S), South Africa, KJ804708, AM94521312, AM94524512, AM94527712, AM94530112, AM94532612, AM94535712; Psychotria cephalophora Merr., Psychotrieae, Kainulainen et al. 10 (S), Vietnam, KJ804709, KJ804900, KJ804507, KJ805103, KJ805697, KJ805298, KJ805496; Psychotria cf. boivinii Bremek., Psychotrieae, Razakamalala 6272 (S), Madagascar, ...., ...., KJ804508, KJ805104, KJ805698, KJ805299, ....; Psychotria comorensis Bremek., Psychotrieae, Mouly 660 (P), Mayotte (Comores), KJ804710, KJ804901, KJ804509, KJ805105, KJ805699, KJ805300, KJ805497; Psychotria comptonii S.Moore, Psychotrieae, Barrabé & Rigault 1014 (NOU), New Caledonia, KF67582328, KF67592728, KJ804510, KF67601528, KJ805700, KF67610428, KF67619128; July 2014] RAZAFIMANDIMBISON ET AL.—EVOLUTION OF PSYCHOTRIEAE AND PALICOUREEAE Psychotria conocarpa Bremek., Psychotrieae, Mouly 712 (P), Mayotte (Comores), KJ804711, KJ804902, KJ804511, KJ805106, KJ805701, KJ805301, KJ805498; Psychotria cryptogrammata E.M.A.Petit, Psychotrieae, Luke 9128 (UPS), Tanzania, KJ804712, KJ804903, KJ804512, KJ805107, KJ805702, KJ805302, KJ805499; Psychotria cupularis (Mull.Arg.) Standl., Psychotrieae, ...., ...., ...., ...., ...., AF41071013, JN6434407; Psychotria cyanococca Seem. ex Dombrain (as P. Pittieri Standl.), Palicoureeae, J. Wright s.n., Panama, ...., AF0719983, ...., ...., ...., AF0027468, AF15261424; Psychotria dalzellii Hook.f., Psychotrieae, A. Meebold 6682 (S), India, ...., KJ804904, ...., ...., ...., KJ805303, KJ805500; Psychotria declieuxioides S.Moore, Psychotrieae, Barrabé & Nigote 937 (NOU), New Caledonia, KF67582828, KF67593228, KJ804513, KF67602028, KJ80570328, KF67610728, ....; Psychotria diversinodula (Verdc.) Verdc., Psychotrieae, Mwasumbi 16350 (S), Tanzania, ...., KJ804904, KJ804514, KJ805108, KJ805704, KJ805304, KJ805501; Psychotria faucicola K.Schum., Psychotrieae, Drummond 3198 (S), Kenya, KJ804713, KJ804907, KJ804516, KJ805109, KJ805705, KJ805305, KJ805502; Psychotria fractinervata E.M.A.Petit, Psychotrieae, Luke 8924 (UPS), Kenya, KJ804714, KJ804907, KJ804517, KJ805110, KJ805706, KJ805306, KJ805503; Psychotria gossweileri E.M.A.Petit, Psychotrieae, D.J. Harris 2685 (S), Cameroon, ...., KJ804908, KJ804518, KJ805111, KJ805707, KJ805307, KJ805504; Psychotria grandis Sw., Psychotrieae, Rova 2267 (GB), Cuba, KJ804715, KJ804909, KJ804519, KJ805112, KJ805708, KJ805308, KJ805505; Psychotria himanthophylla Bremek., Psychotrieae, Razafimandimbison et al. 1028 (S), Madagascar, ...., KJ804910, KJ804520, KJ805113, KJ805709, KJ805309, KJ805506; Psychotria hispidula Standl. ex Steyerm., Palicoureeae, L. Loredo 3881 (MO), Nicaragua, ...., ...., HQ3847705, HQ3848515, HQ3849135, HQ3851905, HQ4129695; Psychotria holtzii (K.Schum.) E.M.A.Petit, Psychotrieae, Luke 8342 (UPS), Kenya, KJ804716, AM94521712, AM94525012, KJ805114, AM94530412, AM94533012, AM94536212; Psychotria homolleae Bremek., Psychotrieae, Razakamalala 6414 (S), Madagascar, KJ804717, KJ804911, KJ804521, KJ805115, KJ805710, KJ805310, KJ805507; Psychotria kirkii Hiern, Psychotrieae, Bremer 3102 (UPS), Cult. Uppsala Univ. Bot. Gard., JQ72985424, AM94521412, AM94524612, AM94527812, X8366320, AM94532712, AM94535812; Psychotria kirkii Hiern-bp81, Psychotrieae, Bremer & Rydin 5002 (S), Tanzania, KJ804718, KJ804912, KJ804522, KJ805116, AY53846925, KJ805311, KJ805508; Psychotria lauracea (K.Schum.) E.M.A.Petit, Psychotrieae, Luke 8343 (UPS), Kenya, ...., ...., ...., ...., ...., KJ805312, KJ805509; Psychotria lavanchiei Bremek., Psychotrieae, Mouly 79 (P), Mayotte (Comores), KJ804719, KJ804913, KJ804523, KJ805117, KJ805711, KJ805313, KJ805510; Psychotria leptothyrsa Miq., Palicoureeae, Molem & Cizek s.n. (PSM), New Guinea, KF67584428, JX1551021, KJ804524, JX1551491, AJ31845229, AJ32008329, JX1550561; Psychotria leucopoda E.M.A.Petit, Psychotrieae, Luke 9458 (UPS), Tanzania, KJ804720, KJ804914, KJ804525, KJ805118, KJ805712, KJ805314, KJ805511; Psychotria lokohensis Bremek.-ck72, Psychotrieae, Razakamalala 6221 (S), Madagascar, KJ804721, KJ804915, KJ804526, KJ805119, KJ805713, ...., KJ805512; Psychotria lokohensis-ck75, Psychotrieae, Razafimandimbison et al. 1040 (S), Madagascar, KJ804722, KJ804916, KJ804515, KJ805120, KJ805714, KJ805315, KJ805513; Psychotria loniceroides Sieber ex DC., Psychotrieae, ...., AF0720343, ...., ...., ...., AF41073213, ....; Psychotria lucidula Baker-ck64, Psychotrieae, Razakamalala 6521 (S), Madagascar, ...., KJ804917, KJ804567, KJ805121, KJ805715, KJ805316, KJ805514; Psychotria macrochlamys (Bremek.) A.P.Davis-ch04, Psychotrieae, Bremer et al. 5338 (S), Madagascar, KJ804723, KJ804918, KJ804527, ...., KJ805716, KJ805317, KJ805515; Psychotria macrochlamys (Bremek.) A.P.Davis-ck61, Psychotrieae, Razakamalala 6485 (S), Madagascar, KJ804724, KJ804919, KJ804528, KJ805122, KJ805318, KJ805717, KJ805516; Psychotria mahonii C.H.Wright, Psychotrieae, Luke 8370 (S), Vietnam, KJ804725, KJ804920, KJ804529, ...., KJ805718, KJ805319, KJ805517; Psychotria mapourioides DC., Psychotrieae, ...., AF0720403, ...., ...., JQ6260795, AF0013538, JN6434987; Psychotria mariniana (Cham. & Schltdl.) Fosberg, Psychotrieae, ...., AF0349043, ...., ...., AJ0021853, AF0013548, ....; Psychotria marojejensis Bremek., Psychotrieae, Bremer et al. 5225 (S), Madagascar, KJ804726, KJ804921, KJ804530, KJ805123, KJ805719, KJ805320, KJ805518; Psychotria megalocarpa (Bremek.) A.P.Davis, Psychotrieae, Razakamalala 6523 (S), Madagascar, KJ804727, KJ804722, KJ804531, KJ805124, KJ805720, KJ805321, KJ805519; Psychotria menalohensis (Bremek.) A.P.Davis & Govaerts, Psychotrieae, Kårehed et al. 1125 288 (UPS), Madagascar, KJ804728, KJ804923, KJ804532, KJ805125, KJ805721, KJ805322, KJ805520; Psychotria micralabastra (Lauterb. & K.Schum.) Valeton, Psychotrieae, Molem & Cizek s.n. (PSM), New Guinea, KJ804729, KJ804924, KJ804533, KJ805126, AJ32008429, .....; KJ805521; Psychotria micrococca (Lauterb. & K.Schum.) Valeton, Psychotrieae, Molem & Cizek s.n. (PSM), New Guinea, KF67585328, KF67595128, KJ804534, KF67603828, AJ31845429, AJ32008529, KF67621528; Psychotria microglossa (Bail.) Baill. ex Guillaumin, Psychotrieae, McPherson & Munzinger 826 (UPS), New Caledonia, KJ804730, KJ804925, KJ804535, KJ805127, KJ805722, KJ805323, KJ805522; Psychotria montana Blume, Palicoureeae, Fagerlind s.n. (S), Indonesia, KJ804731, KJ804926, KJ804536, ...., ...., KJ805324, ....; Psychotria nervosa Benth., Psychotrieae, Rova 2249 (GB), Cuba, KJ804732, KJ804932, KJ804537, KJ805128, KJ805723, KJ805325, KJ805523; Psychotria nigra (Gaertn.) Alston, Psychotrieae, Klackenberg 216 (S), Sri Lanka, ...., KJ804929,...., ...., ...., ...., ....; Psychotria obtusifolia Lam ex Poir., Psychotrieae, Kainulainen et al. 88 (S), Madagascar, KJ804733, KJ804929, KJ804538, KJ805129, KJ805724, KJ805326, KJ805524; Psychotria ostreophora (Wernham) C.M.Taylor, Palicoureeae, Erik Asplemd 10657 (UPS), Colombia, KJ804734, KJ804930, KJ804539, ...., KJ805725, ...., ....; Psychotria pachygrammata Bremek., Psychotrieae, Razakamalala 6324 (S), Madagascar, ...., KJ804931, KJ804540, KJ805130, KJ805726, KJ805327, KJ805525; Psychotria peduncularis (Salisb.) Steyerm., Psychotrieae, ...., AF0720443, ...., ...., ...., AF41074213, JN0536547; Psychotria perrieri Bremek., Psychotrieae, Bremer et al. 5231 (S), Madagascar, KJ804735, KJ804932, KJ804492, KJ805131, KJ805727, KJ805328, KJ805526; Psychotria pervillei Baker-cl47, Psychotrieae, Bremer et al. 5406 (S), Seychelles, KJ804736, KJ804933, KJ804541, KJ805132, KJ805728, KJ805329, KJ805527; Psychotria pervillei Baker-cl48, Psychotrieae, Bremer et al. 5410 (S), Seychelles, KJ804737, KJ804934, KJ804542, KJ805133, KJ805729, KJ805330, KJ805528; Psychotria poeppigiana Mull.Arg., Palicoureeae, Gust O. Malme 1901b (UPS), Brazil, ...., ...., ...., ...., KJ805730, ...., KJ805529; Psychotria polygrammata Bremek., Psychotrieae, Bremer et al. 5083 (S), Madagascar, KJ804738, KJ804935, KJ804543, KJ805134, KJ805731, KJ805331, KJ805530; Psychotria psychotrioides (DC.) Roberty, Psychotrieae, Adoph 5414 (S), Ghana, ...., ...., KJ804544, KJ805135, KJ805732, KJ805332, KJ805531; Psychotria pyrrotricha (Bremek.) A.P.Davis & Govaerts, Psychotrieae, Razafimandimbison et al. 1262 (S), Madagascar, ...., KJ804936, KJ804545, KJ805136, KJ805733, KJ805333, KJ805532; Psychotria ramuensis Sohmer, Psychotrieae, Molem & Cizek s.n. (PSM), New Guinea, KJ804739, KJ804937, KJ804546, KJ805137, AJ31845529, AJ32008629, KJ805533; Psychotria remota Benth., Psychotrieae, ...., AF1494035, ...., ...., ...., AF1475765, JN6435197; Psychotria retusa (Bremek.) A.P.Davis & Govaerts, Psychotrieae, Razafimandimbison et al. 1137 (S), Madagascar, KJ804740, KJ804938, KJ804547, KJ805138, KJ805734, KJ805334, KJ805534; Psychotria rhombocarpa Kaneh., Psychotrieae, ...., AF0720313, ...., ...., ...., ...., ....; Psychotria rupicola (Baill.) Schltr.-cc43, Psychotrieae, Mouly 830 (P), New Caledonia, KJ804741, KJ804939, KJ804548, KJ805139, KJ805735, KJ805335, KJ805535; Psychotria rupicola (Baill.) Schltr.-cd58, Psychotrieae, Barrabé 547 (NOU), New Caledonia, KF67586328, KF67596128, KJ804549, KF67604828, KJ805736, KF67613628, KF67622528; Psychotria saltiensis (S.Moore) Guillaumin, Psychotrieae, McPherson & Munzinger 18065 (UPS), New Caledonia, KJ804542, KJ804940, KJ804550, KJ805140, KJ805737, KJ805336, KJ805536; Psychotria sarmentosa Blume, Psychotrieae, ...., ...., ...., ...., ...., AF41075113, JN6435307; Psychotria schliebenii E.M.A.Petit, Psychotrieae, Luke 8348 (UPS), Kenya, KJ804743, AM94521612, AM94524912, AM94528212, AM94530312, AM94532912, AM94536112; Psychotria scytophylla Bremek., Psychotrieae, Razakamalala 6188 (S), Madagascar, KJ804744, KJ804941, KJ804551, KJ805141, KJ805738, KJ805337, KJ805537; Psychotria serpens L., Psychotrieae,...., AF0720363, ...., ...., ...., AF1475775, JN6435337; Psychotria silhouettae F.Friedmann, Psychotrieae, Senterre 5681 (SEY), Seychelles, KJ804745, KJ804942, KJ804552, KJ805142, KJ805739, KJ805338, KJ805538; Psychotria simianensis A.P.Davis & Govaerts-cm56, Psychotrieae, Razafimandimbison et al. 1241 (S), Madagascar, KJ804746, KJ804943, KJ804553, KJ805143, KJ805740, KJ805339, KJ805539; Psychotria simianensis A.P.Davis & Govaerts-cm57, Psychotrieae, Razafimandimbison et al. 1238 (S), Madagascar, KJ804747, KJ804944, KJ804554, KJ805144, KJ805741, KJ805340, KJ805540; Psychotria simianensis A.P.Davis & Govaerts-cm59, 1126 AMERICAN JOURNAL OF BOTANY Psychotrieae, Razafimandimbison et al. 1251 (S), Madagascar, KJ804748, KJ804945, KJ804555, KJ805145, KJ805742, KJ805341, KJ805541; Psychotria sp.-b84, Psychotrieae, Cult. Bot. Gard. Meise, KJ804749, KJ804946, KJ804556, KJ805146, KJ805743, KJ805342, KJ805542; Psychotria sp.-bl02, Psychotrieae, Eriksson et al. 995 (S), Madagascar, KJ804750, KJ804947, ...., KJ805147, KJ805744, KJ805343, KJ805543; Psychotria sp.-bl30, Psychotrieae, Eriksson et al. 932 (S), Madagascar, KJ804751, KJ804948, KJ804557, KJ805148, KJ805745, KJ805344, KJ805544; Psychotria sp.-ce56, Psychotrieae, Bremer et al. 5055 (S), Madagascar, KJ804652, KJ804949, KJ804558, KJ805149, KJ805746, KJ805345, KJ805545; Psychotria sp.-ce98, Psychotrieae, Bremer et al. 5079 (S), Madagascar, KJ804753, KJ804950, KJ804559, KJ805150, KJ805747, KJ805346, KJ805546; Psychotria sp.-ce99, Psychotrieae, Bremer et al. 5080 (S), Madagascar, KJ804754, KJ804951, KJ804560, KJ805151, KJ805748, ...., KJ805547; Psychotria sp.-cf84, Psychotrieae, Bremer et al. 5180 (S), Madagascar, KJ804755, KJ804952, KJ804561, KJ805152, KJ805749, KJ805347, KJ805548; Psychotria sp.-ch18, Psychotrieae, Mouly 702 (P), Mayotte (Comores), KJ804756, KJ804953, KJ804562, KJ805153, KJ805750, KJ805348, KJ805549; Psychotria sp.-ck23, Psychotrieae, McPherson & Munzinger 18265 (MO), New Caledonia, KJ804757, KJ804954, KJ804563, KJ805154, ...., KJ805349, KJ805550; Psychotria sp.-ck27, Psychotrieae, Schmidt et al. 1677 (MO), Ghana, ...., KJ804955, KJ804564, KJ805155, KJ805751, KJ805350, KJ805551; Psychotria sp.-ck38, Psychotrieae, Razakamalala 6554 (S), Madagascar, KJ804758, KJ804956, KJ804565, KJ805156, KJ805752, KJ805351, KJ805552; Psychotria sp.-ck63, Psychotrieae, Razakamalala 6516 (S), Madagascar, KJ804759, KJ804957, KJ804566, KJ805157, KJ805753, KJ805352, KJ805553; Psychotria sp.-ck66, Psychotrieae, Razakamalala 6532 (S), Madagascar, KJ804760, KJ804958, KJ804568, KJ805158, KJ805754, KJ805353, KJ805554; Psychotria sp.-ck68, Psychotrieae, Razakamalala 6573 (S), Madagascar, KJ804761, KJ804959, KJ804569, KJ805159, KJ805755, KJ805354, KJ805555; Psychotria sp.-ck69, Psychotrieae, Razakamalala 6571 (S), Madagascar, KJ804762, KJ804960, KJ804570, KJ805160, KJ805756, KJ805355, KJ805556; Psychotria sp.-ck70, Psychotrieae, Razakamalala 6456 (S), Madagascar, KJ804763, KJ804961, KJ804571, KJ805161, KJ805757, KJ805356, KJ805557; Psychotria sp.-ck76, Psychotrieae, Razafimandimbison et al. 1065 (S), Madagascar, ...., KJ804962, KJ804572, KJ805162, KJ805758, KJ805357, KJ805558; Psychotria sp.-ck78, Psychotrieae, Razafimandimbison et al. 782 (S), Vietnam, KJ804764, KJ804963, KJ804573, KJ805163, KJ805759, KJ805358, KJ805559; Psychotria sp.ck79, Psychotrieae, Kainulainen et al. 11 (S), Vietnam, KJ804765, KJ804964, KJ804574, KJ805164, KJ805760, KJ805359, KJ805560; Psychotria sp.cm06, Psychotrieae, Razakamalala 6446 (S), Madagascar, ...., KJ804965, KJ804575, KJ805165, KJ805761, KJ805360, KJ805561; Psychotria sp.cm09, Psychotrieae, Razakamalala 6574 (S), Madagascar, ...., KJ804966, KJ804577, KJ805166, KJ805762, KJ805361, ....; Psychotria sp.-cm28, Psychotrieae, Razafimandimbison et al. 1130 (S), Madagascar, ...., KJ804967, KJ804578, KJ805167, KJ805763, KJ805362, KJ805562; Psychotria sp.cm30, Psychotrieae, Kainulainen et al. 69 (S), Madagascar, ...., KJ804968, KJ804579, KJ805168, KJ805764, KJ805363, KJ805563; Psychotria sp.cm32, Psychotrieae, Razafimandimbison et al. 1070 (S), Madagascar, ...., KJ804969, KJ804580, KJ805169, KJ805765, KJ805364, KJ805564; Psychotria sp.-cm33, Psychotrieae, Kainulainen et al. 119 (S), Madagascar, ...., KJ804970, ...., KJ805170, KJ805766, KJ805365, KJ805565; Psychotria sp.-cm46, Psychotrieae, Razafimandimbison et al. 1222 (S), Madagascar, KJ804766, KJ804971, KJ804581, KJ805171, KJ805767, KJ805366, KJ805566; Psychotria sp.-cm49, Psychotrieae, Razafimandimbison et al. 1242a (S), Madagascar, KJ804767, KJ804972, KJ804582, KJ805172, KJ805768, KJ805367, KJ805567; Psychotria sp.-cm54, Psychotrieae, Razafimandimbison et al. 1247 (S), Madagascar, KJ804768, KJ804973, KJ804583, KJ805173, KJ805769, KJ805368, KJ805568; Psychotria sp.cm55, Psychotrieae, Razafimandimbison et al. 1228 (S), Madagascar, KJ804769, KJ804974, KJ804584, KJ805174, KJ805770, KJ805369, KJ805569; Psychotria sp.-cm60, Psychotrieae, Razafimandimbison et al. 1219a (S), Madagascar, KJ804770, ...., KJ804585, KJ805175, KJ805771, KJ805370, KJ805570; Psychotria submontana Domin., Psychotrieae, ...., AF0720233, ...., ...., ...., ...., ....; Psychotria taxifolia Bremek., Psychotrieae, Razakamalala 6463 (S), Madagascar, KJ804771, KJ804975, KJ804586, KJ805176, KJ805772, KJ805371, KJ805571; Psychotria urbaniana Steyer., Palicoureeae, Wit and Holge 2400 (UPS), Brazil, KJ804772, KJ804976, ...., ...., KJ805774, ...., ....; Psychotria zeylanica Sohmer-cl81, Psychotrieae, Klackenberg 473 (S), Sri Lanka, KJ804773, KJ804977, KJ804587, KJ805177, KJ805774, KJ805372, KJ805572; Psychotria zeylanica Sohmer-cl82, Psychotrieae, Klackenberg 489 (S), Sri Lanka, KJ804774, KJ804978, KJ804588, KJ804978, KJ805775, KJ805373, KJ805573; Psychotria zombamontana (Kuntze) E.M.A.Petit, Psychotrieae, ...., ....., ....., ...., ...., AF41076613, JN6435557; Pyragra ankarensis Bremek., Psychotrieae, Razafimandimbison et al. 405 (UPS), Madagascar, KJ804775, KJ804979, KJ804589, KJ805179, KJ805776, KJ805374, KJ805574; Pyragra obtusifolia Bremek., Psychotrieae, SF23374 (P), Madagascar, KJ804776, KJ804980, KJ804590, KJ805180, KJ805777, KJ805375, KJ805575; Rudgea hostmanniana Benth., Palicoureeae, ..., AF0720143, ...., ...., ...., AF0036158, JN6435567; Rudgea loretensis Standl., Palicoureeae, Bremer 3346 (S), Ecuador, KJ804777, KJ804981, KJ804591, KJ805181, Z6882115, KJ805376, KJ805576; Rudgea panurensis Mull.Arg.-cl07, Palicoureeae, Bremer 3334 (UPS), Ecuador, KJ804778, KJ804982, ...., KJ805182, KJ805778, KJ805377, KJ805577; Rudgea stipulacea (DC.)Steyerm., Palicoureeae, Zappi 986 (K), Brazil, ...., JX1550991, ...., JX155145-61,...., JX1551891, JX1550531; Rudgea viburnoides (Cham.) Benth., Palicoureeae, Gust O. Malme 2550 (S), Brazil, KJ804779, KJ804983, ...., KJ805183, KJ805779, KJ805378, KJ805578; Schizocolea linderi (Hutch. & Daziel) Bremek., Schizocoleeae, Adam 20116 (UPS), Liberia, KJ804780, EU1453579, EU1453239, FJ69533526, AM11727214, EU1454989, EU1455469; Schradera stellata Benth., Schradereae, Clark & Watt 783 (QCNE), Ecuador, KJ804781, KJ804984, AJ23401411, AM94526412, Y1185921, AM94531312, AM94534312; Trigonopyren comorensis Bremek., Psychotrieae, Mouly 708 (P), Mayotte (Comores), KJ804782, KJ804985, KJ804592, KJ805184, KJ805780, KJ805379, KJ805579; Trigonopyren pauviflorus Bremek., Psychotrieae, Razakamalala 6541 (S), Madagascar, KJ804783, KJ804986, KJ804593, KJ805185, KJ805781, KJ805380, KJ805580; Trigonopyren sp.-ck81, Psychotrieae, Razakamalala 6548 (S), Madagascar, KJ804784, KJ804987, KJ804594, KJ805186, KJ805782, ...., KJ805581.

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