Skip to main content
Log in

Phylogenetic relationships of two Cuban spleenworts with unusual morphology: Asplenium (Schaffneria) nigripes and Asplenium pumilum (Aspleniaceae, leptosporangiate ferns)

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

The infrageneric classification of Asplenium, the most species-rich genus of ferns, is notoriously difficult as a result of extensive morphological homoplasy combined with exceptional morphological disparity. Besides a core Asplenium, 29 satellite genera have been described, but most of them have not been widely accepted. In recent years, molecular phylogenetic studies found most of these satellite genera to be nested in Asplenium, but several morphologically distinct taxa have not yet been included in such studies. One of these elements is the monospecific neotropical genus Schaffneria which is characterized by undivided suborbicular blades, lack of a costa, black stipes, netted veins and single or paired sori. Maximum likelihood and Bayesian phylogenetic inference based on the chloroplast DNA markers rbcL, rps4, rps4-trnS and trnL-trnF indicated a position of Schaffneria nigripes within Asplenium. We thus propose to treat Schaffneria as a synonym of Asplenium and adopt the name Asplenium nigripes. With the current sampling, Asplenium (Schaffneria) nigripes is placed sister to A. pumilum, the only species of Asplenium with whitish catenate hairs on its leaves. Despite considerable morphological differences, both species resemble each other in several features including filiform-lanceolate, mostly entire, brown-blackish rhizome scales with a dark-sclerotic center and some marginal projections, a striate, hairy epidermis, echinolophate spore ornamentation with slim microechinate folds forming small lacunae, and Aspidium-type gametophytes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Molec Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Bercu R (2005) Contributions to the anatomy of Asplenium ruta-muraria. Stud Bot Hung 36:13–20

    Google Scholar 

  • Bercu R (2007) Variation in the anatomy of the vascular system of Asplenium trichomanes-ramosum L. Nat Montenegr 9:9–17

    Google Scholar 

  • Braggins JE, Large MF (1990) Spore morphology as a taxonomic data source in Cyathea J. E. Smith and Asplenium L. Rev Paleobot Palynol 64:149–158

    Article  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molec Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Chang Y, Li J, Lu S, Schneider H (2013) Species diversity and reticulate evolution in the Asplenium normale complex (Aspleniaceae) in China and adjacent areas. Taxon 62:673–687

    Article  Google Scholar 

  • Christenhusz MJM, Zhang X-C, Schneider H (2011) A linear sequence of extant families and genera of lycophytes and ferns. Phytotaxa 19:7–54

    Article  Google Scholar 

  • Copeland EB (1947) Genera filicum, the genera of ferns. Chronica Botanica Co., Waltham

    Google Scholar 

  • Dyer AF (1979) The culture of fern gametophytes for experimental investigation. In: Dyer AF (ed) The experimental biology of ferns. Academic, London, pp 253–305

    Google Scholar 

  • Dyer RJ, Savolainen V, Schneider H (2012) Apomixis and reticulate evolution in the Asplenium monanthes fern complex. Ann Bot (Oxford) 110:1515–1529

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards ME, Miller JH (1972) Growth regulation by ethylene in fern gametophytes. III: inhibition of spore germination. Amer J Bot 59:458–465

    Article  CAS  Google Scholar 

  • Gastony GJ, Johnson WP (2001) Phylogenetic placements of Loxoscaphe thecifera (Aspleniaceae) and Actiniopteris radiata (Pteridaceae) based on analysis of rbcL nucleotide sequences. Amer Fern J 91:197–213. doi:10.1640/0002-8444(2001)091[0197:ppolta]2.0.co;2

    Article  Google Scholar 

  • Gómez LD (1973) Contribuciones a la pteridología costarricense. IV. Cheiloplecton, Schaffneria y Paltonium en Costa Rica. Revista Biol Trop 21:91–101

    Google Scholar 

  • Herrero A, Prada C, Pajarón S (2002) Gametophyte morphology and gametangial ontogeny of Asplenium foreziense and related taxa (Aspleniaceae: Pteridophyta). Bot J Linn Soc 139:87–98

    Article  Google Scholar 

  • Hooker WJ (1857) On Asplenium (Schaffneria nigripes), a Mexican, and on Davallia nodosa, an Indian fern. Hooker’s J Bot Kew Gard Misc 9:268

    Google Scholar 

  • Hooker WJ (1862) Species filicum, vol 4. W. Pamplin, London

    Google Scholar 

  • Hooker WJ, Baker JG (1868) Synopsis filicum. Robert Hardwicke, London

    Google Scholar 

  • Johns RJ (2000) Spore ornamentation and the species of simple-fronded Asplenium (Aspleniaceae) in west Africa. In: Harley MM et al (eds) Pollen and spores: morphology and biology. Royal Botanic Gardens, Kew, pp 133–146

    Google Scholar 

  • Khare PK, Shankar R (1989) On the petiolar structure of some Asplenium species. Canad J Bot 67:95–103. doi:10.1139/b89-014

    Article  Google Scholar 

  • Kuntze O (1891) Revisio generum plantarum, vol 2. Arthus Felix, Leipzig

    Google Scholar 

  • Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molec Biol Evol 29:1695–1701

    Article  CAS  PubMed  Google Scholar 

  • Lin YX, Viane R (2013) Aspleniaceae. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China (Pteridophytes), vol 2–3. Missouri Botanical Garden Press, St. Louis, pp 267–316

    Google Scholar 

  • Lovis JD (1973) A biosystematic approach to phylogenetic problems and its application to the Aspleniaceae. Bot J Linn Soc 67:211–228

    Google Scholar 

  • Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. Available at: http://mesquiteproject.org

  • Mickel JT (1976) Sinephropteris, a new genus of scolopendrioid ferns. Brittonia 28:326–328

    Article  Google Scholar 

  • Mickel JT, Smith AR (2004) The Pteridophytes of Mexico. Mem New York Bot Gard 88:1–1054

  • Moran RC, Riba R (1995) Flora Mesoamericana vol I. Psilotaceae a Salviniaceae, vol I. Universidad Nacional Autónoma de México, México

    Google Scholar 

  • Moran RC, Smith AR (2001) Phytogeographic relationships between neotropical and African-Madagascan pteridophytes. Brittonia 53:304–351

  • Morton CV, Lellinger DB (1966) The Polypodiaceae subfamily Asplenioideae in Venezuela. Mem New York Bot Gard 5:1–49

    Google Scholar 

  • Murakami N (1995) Systematics and evolutionary biology of the fern genus Hymenasplenium (Aspleniaceae). J Pl Res 108:257–268

    Article  Google Scholar 

  • Murakami N, Schaal B (1994) Chloroplast DNA variation and the phylogeny of Asplenium sect. Hymenasplenium (Aspleniaceae) in the New World tropics. J Pl Res 107:245–251

    Article  CAS  Google Scholar 

  • Murakami N, Nogami S, Watanabe M, Iwatsuki K (1999a) Phylogeny of Aspleniaceae inferred from rbcL nucleotide sequences. Amer Fern J 89:232–243

    Article  Google Scholar 

  • Murakami N, Watanabe M, Yokoyama J, Yatabe Y, Iwasaki H, Serizawa S (1999b) Molecular taxonomic study and revision of the three Japanese species of Asplenium sect. Thamnopteris. J Pl Res 112:15–25. doi:10.1007/pl00013856

    Article  CAS  Google Scholar 

  • Nayar BK, Devi S (1964) Spore morphology of Indian ferns. II Aspleniaceae and Blechnaceae. Grana Palynol 5:222–242

    Article  Google Scholar 

  • Nayar B, Kaur S (1969) Types of prothallial development in homosporous ferns. Phytomorphol 19:179–188

    Google Scholar 

  • Nayar B, Kaur S (1971) Gametophytes of homosporous ferns. Bot Rev 37:295–396

    Article  Google Scholar 

  • Ohlsen DJ, Perrie LR, Shepherd LD, Brownsey PJ, Bayly MJ (2015) Phylogeny of the fern family Aspleniaceae in Australasia and the south-western Pacific. Austral Syst Bot 27:355–371. doi:10.1071/SB14043

    Article  Google Scholar 

  • Pangua E, Prada C (1988) Tipos esporales en Aspleniáceas ibéricas. Lagascalia 15:157–167

    Google Scholar 

  • Peña E, Saralegui H (1982) Técnicas de anatomía vegetal. Universidad de La Habana, La Habana

    Google Scholar 

  • Perrie LR, Brownsey PJ (2005) Insights into the biogeography and polyploid evolution of New Zealand Asplenium from chloroplast DNA sequence data. Amer Fern J 95:1–21. doi:10.1640/0002-8444(2005)095[0001:iitbap]2.0.co;2

    Article  Google Scholar 

  • Pichi-Sermolli REG (1977) Tentamen pteridophytorum genera in taxonomicum ordinem redigendi. Webbia 31:313–512

    Article  Google Scholar 

  • Pinter I, Bakker F, Barrett J, Cox C, Gibby M, Henderson S, Morgan-Richards M, Rumsey F, Russell S, Trewick S, Schneider H, Vogel J (2002) Phylogenetic and biosystematic relationships in four highly disjunct polyploid complexes in the subgenera Ceterach and Phyllitis in Asplenium (Aspleniaceae). Org Diversity Evol 2:299–311

    Article  Google Scholar 

  • Prada C, Pangua E, Blanco P, Cubas P, Pardo C (1989) Las aspleniáceas de los herbarios Mutis e Isern. Anales Jard Bot Madrid 46:539–552

    Google Scholar 

  • Prada C, Pangua E, Pajarón S, Herrero A, Escudero A, Rubio A (1995) A comparative study of gametophyte morphology, gametangial ontogeny and sex expression in the Asplenium adiantum-nigrum complex (Aspleniaceae, Pteridophyta). Ann Bot Fenn 32:107–115

    Google Scholar 

  • Prada C, Pangua E, Herrero A, Pajarón S (1996) A comparative study of the gametophytes of Asplenium majoricum Litard (Aspleniaceae) and related taxa. Anales Jard Bot Madrid 54:126–136

    Google Scholar 

  • Puttock CF, Quinn CJ (1980) Perispore morphology and the taxonomy of the Australian Aspleniaceae. Austral J Bot 28:305–322

    Article  Google Scholar 

  • Regalado L, Sánchez C (2002) Spore morphology as a taxonomic tool in the delimitation of three Asplenium L. species complexes (Aspleniaceae: Pteridophyta) in Cuba. Grana 41:107–113

    Article  Google Scholar 

  • Riba R, Pérez-García B, Pérez-García M (1992) Schaffneria nigripes (Aspleniaceae): morfogénesis del gametófito y anatomía y morfología del esporófito. Bol Soc Bot Mexico 52:105–113

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rothfels CJ, Sundue MA, Kuo L-Y, Larsson A, Kato M, Schuettpelz E, Pryer KM (2012) A revised family-level classification for eupolypod II ferns (Polipodiidae: Polypodiales). Taxon 61:515–533

    Google Scholar 

  • Sánchez C, Regalado L (2003) Aspleniaceae. Flora de la República de Cuba, vol 8. Koeltz Scientific Books, Königstein, pp 1–65

    Google Scholar 

  • Schneider H, Russell SJ, Cox CJ, Bakker F, Henderson S, Rumsey F, Barrett J, Gibby M, Vogel JC (2004) Chloroplast phylogeny of asplenioid ferns based on rbcL and trnL-F spacer sequences (Polypodiidae, Aspleniaceae) and its implications for biogeography. Syst Bot 29:260–274

    Article  Google Scholar 

  • Schneider H, Ranker TA, Russell SJ, Cranfill R, Geiger JMO, Aguraiuja R, Wood KR, Grundmann M, Kloberdanz K, Vogel JC (2005) Origin of the endemic fern genus Diellia coincides with the renewal of Hawaiian terrestrial life in the Miocene. Proc Roy Soc B 272:455–460

    Article  Google Scholar 

  • Schneider H, Navarro-Gomez A, Russell SJ, Ansell S, Grundmann M, Vogel JC (2013) Exploring the utility of three nuclear regions to reconstruct reticulate evolution in the fern genus Asplenium. J Syst Evol 5:142–153

    Article  Google Scholar 

  • Schuettpelz E, Pryer KM (2007) Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes. Taxon 56:1037–1050

    Article  Google Scholar 

  • Smith J (1875) Historia Filicum. Macmillan, London

    Google Scholar 

  • Smith AR, Cranfill RB (2002) Intrafamilial relationships of the thelypteroid ferns (Thelypteridaceae). Amer Fern J 92:131–149

    Article  Google Scholar 

  • Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf PG (2006) A classification for extant ferns. Taxon 55:705–731

    Article  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Sundue MA, Rothfels CJ (2014) Stasis and convergence characterize morphological evolution in eupolypod II ferns. Ann Bot (Oxford) 113:35–54. doi:10.1093/aob/mct247

    Article  Google Scholar 

  • Sylvestre LS, Windisch PG (2002) New combinations in Antigramma C. Presl (Aspleniaceae) and a synopsis of the species. Bradea 8:331–337

    Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109

    Article  CAS  Google Scholar 

  • Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molec Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tardieu-Blot ML (1957) Sur un Antigramma de Madagascar et sur la repartition geographique des genres Antigramma et Schaffneria. Naturaliste Malgache 9:29–32

    Google Scholar 

  • Trewick SA, Morgan-Richards M, Russell SJ, Henderson S, Rumsey FJ, Pintér I, Barrett JA, Gibby M, Vogel JC (2002) Polyploidy, phylogeography and Pleistocene refugia of the rockfern Asplenium ceterach: evidence from chloroplast DNA. Molec Ecol 11:2003–2012

    Article  CAS  Google Scholar 

  • Tryon AF, Lugardon B (1991) Spores of Pteridophyta. Springer, Berlin

    Book  Google Scholar 

  • Tryon RM, Stolze RG (1993) Pteridophyta of Peru, part 5:18. Aspleniaceae—21. Polypodiaceae. Fieldiana Bot 32:1–49

    Google Scholar 

  • Tryon R, Tryon AF (1982) Ferns and allied plants with special reference to tropical America. Springer, New York

    Book  Google Scholar 

  • Viane R, Van Cotthem W (1977) Spore morphology and stomatal characters of some Kenyan Asplenium species. Ber Deutch Bot Ges 90:219–239

    Google Scholar 

  • Wagner WH (1953a) An Asplenium prototype of the genus Diellia. Bull Torrey Bot Club 80:76–94. doi:10.2307/2482236

    Article  Google Scholar 

  • Wagner WH (1953b) The genus Diellia and the value of characters in determining fern affinities. Amer J Bot 40:34–40

    Article  Google Scholar 

  • Wagner WH (1979) Reticulate veins in the systematics of modern ferns. Taxon 28:87–95

    Article  Google Scholar 

  • Wei LL, Dong SY (2012) Taxonomic studies in Asplenium sect. Thamnopteris (Aspleniaceae) II; spore morphology. Nordic J Bot 30:90–103

    Article  Google Scholar 

Download references

Acknowledgments

A German Academic Exchange Service scholarship (DAAD, 2013/16, 57076385) to J. L. is gratefully acknowledged. Financial support from the International Association of Plant Taxonomists to J. L. and from the Mohamed bin Zayed Species Conservation Fund to L. R. enabled field work in Cuba. We are grateful to Ariel Rodríguez and Julio León for their support during fieldwork and the curators and directors of the herbaria BM, HAC, HAJB, M and MABC for access to specimens. We thank Miguel Vences for kindly providing access to the laboratory and computer facilities of the Zoological Institute of the Technical University of Braunschweig and the late Siwert Nilsson for providing access to the SEM facilities of the Palynological Laboratory of the Swedish Museum of Natural History.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Josmaily Lóriga.

Ethics declarations

Conflict of interest

The authors declare they have no conflict of interest.

Additional information

Handling editor: Frank Blattner.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lóriga, J., Regalado, L., Prada, C. et al. Phylogenetic relationships of two Cuban spleenworts with unusual morphology: Asplenium (Schaffneria) nigripes and Asplenium pumilum (Aspleniaceae, leptosporangiate ferns). Plant Syst Evol 303, 165–176 (2017). https://doi.org/10.1007/s00606-016-1359-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-016-1359-6

Keywords

Navigation