Advertisement

Symbiosis

pp 1–7 | Cite as

Evolution of substrate specificity and fungal symbiosis in filmy ferns (Hymenophyllaceae): a Bayesian approach for ambiguous character state reconstruction

  • Marcus LehnertEmail author
  • Michael Krug
Article
  • 27 Downloads

Abstract

Ferns, as landplants in general, originally form a symbiosis involving Arbuscular Mycorrhizal Fungi (AMF), which are prevalent in habitats directly connected to the soil, including low epiphytic sites, but are largely absent in the high epiphytic habitat. High probabilities of AMF should be expected in chiefly terrestrial lineages whereas truly, fully adapted epiphytic lineages should be lacking fungal endophytes or may have switched to other types of fungi; e.g. Dark Septate Endophytes (DSE), a morphological class of mostly unspecified fungi that is often found in epiphytic ferns and may include potentially symbiotic ascomycetes. We used a Bayesian approach for a comparison of the ambiguous character of preferred substrate with the incompletely known mycorrhization status for an ancient lineage of ferns, the Hymenophyllaceae or filmy ferns. The majority of the analysed 167 species prefers either the saxicolous, terrestrial or epiphytic habitat (differentiated into low and high epiphytic), but there are also many generalists without clear preference. For the whole family Hymenophyllaceae and one of the two main clades of the subfamily Trichomanoidae, the terrestrial habitat and AMF received the highest probability for representing the ancestral state. For the subfamily Hymenophylloidae, the low epiphytic habitat and DSE received the highest probability as ancestral state, whereas that for AMF was very low. The other main clade of the subfamily Trichomanoidae as well as the whole subfamily was found most likely to be originally terrestrial; but in both cases the probability values did not differ much from the values for low epiphytism, with all values around 50 ± 5%. The high epiphytic habitat, which in its present condition is thought to be possible only in angiosperm-dominated vegetation, did not receive high probability to be the ancestral state in any clade. This decouples the evolution of epiphytism in filmy ferns in time from the advent of the angiosperms, which is hypothesized to have triggered the radiation of all other major epiphytic fern lineages.

Keywords

Fern mycorrhiza Filmy ferns Gymnosperm forest Habitat Low epiphyte Niche evolution Substrate 

Notes

Acknowledgments

We thank Jürgen Kluge, Rayko Jonas, and Ramona Güdel for their participation in fieldwork and lab analyses.

Author contributions

ML conceived the study, coded the characters, wrote the manuscript and made the illustrations. MK performed the phylogenetic analyses.

Supplementary material

13199_2018_594_MOESM1_ESM.docx (36 kb)
ESM 1 (DOCX 35 kb)
13199_2018_594_Fig2_ESM.png (502 kb)
Supplement Fig. 1.

Resolved unrooted phylogenetic reconstruction of the filmy ferns (Hymenophyllaceae) based on coding cp data (rbcL, rps4) of 167 ingroup taxa and 26 outgroup taxa; left tree with Hymenopyhllum-clade collapsed, right one the same with Trichomanes-clade collapsed. (PNG 501 kb)

13199_2018_594_MOESM2_ESM.tif (883 kb)
High Resolution Image (TIF 882 kb)

References

  1. Antonelli A, Nylander JAA, Persson C, Sanmartín I (2009) Tracing the impact of the Andean uplift on Neotropical plant evolution. Proc Natl Acad Sci 106:9749–9754CrossRefGoogle Scholar
  2. Benzing DH 2004) Vascular epiphytes. Forest canopies. p. 175–211Google Scholar
  3. Bomfleur B, Grimm GW, McLoughlin S (2017) The fossil Osmundales (Royal Ferns)—a phylogenetic network analysis, revised taxonomy, and evolutionary classification of anatomically preserved trunks and rhizomes. PeerJ 5:e3433CrossRefGoogle Scholar
  4. Boullard B (1958) La mycotrophie chez les ptéridophytes. Sa fréquence, ses caractères, sa signification. Botaniste 41:5–185Google Scholar
  5. Bravo A, York T, Pumplin N, Mueller LA, Harrison MJ (2016) Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nat Plants 2:15208CrossRefGoogle Scholar
  6. Bronstein JL, Alarcón R, Geber M (2006) The evolution of plant–insect mutualisms. New Phytol 172:412–428CrossRefGoogle Scholar
  7. Brownlie G (1969) Pteridophytes. In: Aubréville A (ed) Flore de la Nouvelle Calédonie et Dépendances, Number 3. Museum National d'Histoire Naturelle, ParisGoogle Scholar
  8. Brownlie G (1977) The pteridophyte flora of Fiji. Nova Hedwig Beih 55:1–397Google Scholar
  9. Brownsey PJ, Smith-Dodsworth JC (1989) New Zealand ferns and allied plants. David Bateman Ltd.Google Scholar
  10. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304CrossRefGoogle Scholar
  11. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77CrossRefGoogle Scholar
  12. Cardelús CL, Mack MC (2010) The nutrient status of epiphytes and their host trees along an elevational gradient in Costa Rica. Plant Ecol 207:25–37CrossRefGoogle Scholar
  13. Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715CrossRefGoogle Scholar
  14. Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago PressGoogle Scholar
  15. Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071CrossRefGoogle Scholar
  16. Dassler CL, Farrar DR (2001) Significance of gametophyte form in long-distance colonization by tropical, epiphytic ferns. Brittonia 53:352–369CrossRefGoogle Scholar
  17. Davis CC, Schaefer H (2011) Plant evolution: pulses of extinction and speciation in gymnosperm diversity. Curr Biol 21:R995–R998CrossRefGoogle Scholar
  18. Dubuisson J-Y, Hennequin S, Rakotondrainibe F, Schneider (2003) Ecological diversity and adaptive tendencies in the tropical fern Trichomanes L. (Hymenophyllaceae) with special reference to climbing and epiphytic habits. Bot J Linn Soc 142:41–63CrossRefGoogle Scholar
  19. Dubuisson JY, Schneider H, Hennequin S (2009) Epiphytism in ferns: diversity and history. C R Biol 332:120–128Google Scholar
  20. Ebihara A, Dubuisson JY, Iwatsuki K, Hennequin S, Ito M (2006) A taxonomic revision of Hymenophyllaceae. Blumea 51:221–280CrossRefGoogle Scholar
  21. Egan C, Li D-W, Klironomos J (2014) Detection of arbuscular mycorrhizal fungal spores in the air across different biomes and ecoregions. Fungal Ecol 12:26–31CrossRefGoogle Scholar
  22. Eiserhardt WL, Borchsenius F, Plum CM, Ordonez A, Svenning J (2015) Climate-driven extinctions shape the phylogenetic structure of temperate tree floras. Ecol Lett 18:263–272CrossRefGoogle Scholar
  23. Enright NJ (2001) Nutrient accessions in a mixed conifer–angiosperm forest in northern New Zealand. Austral Ecol 26:618–629CrossRefGoogle Scholar
  24. Farrar DR, Dassler C, Watkins JE Jr, Skelton C (2008) Gametophyte ecology. Chapter 9. In: Ranker TA, Haufler CH (eds) Biology and evolution of ferns and lycophytes. Cambridge University Press, Cambridge, pp 222–256CrossRefGoogle Scholar
  25. Futuyma DJ, Agrawal A (2009) Macroevolution and the biological diversity of plants and herbivores. Proc Natl Acad Sci U S A 106:18054–18061CrossRefGoogle Scholar
  26. Heijden MGA, Martin FM, Selosse M, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423CrossRefGoogle Scholar
  27. Hennequin S, Schuettpelz E, Pryer KM, Ebihara A, Dubuisson JY (2008) Divergence times and the evolution of Epiphytism in filmy ferns (Hymenophyllaceae) revisited. Int J Plant Sci 169:1278–1287CrossRefGoogle Scholar
  28. Hoysted GA, Kowal J, Jacob A, Rimington WR, Duckett JG, Pressel S, Orchard S, Ryan MH, Field KJ, Bidartondo MI (2018) A mycorrhizal revolution. Curr Opin Plant Biol 44:1–6CrossRefGoogle Scholar
  29. Hu S, Dilcher DL, Jarzen DM, Taylor DW (2008) Early steps of angiosperm–pollinator coevolution. Proc Natl Acad Sci 105:240–245CrossRefGoogle Scholar
  30. Janos DP (1993) Vesicular-arbuscular mycorrhizae of epiphytes. Mycorrhiza 4:1–4CrossRefGoogle Scholar
  31. Jarman SJ, Kantvilas G (1995) Epiphytes on an old Huon pine tree (Lagarostrobos franklinii) in Tasmanian rainforest. N Z J Bot 33:65–78CrossRefGoogle Scholar
  32. Jones DL, Clemesha SC (1976) Australian ferns and fern allies, with notes on their cultivation. AH & AW ReedGoogle Scholar
  33. Kissling WD, Eiserhardt WL, Baker WJ, Borchsenius F, Couvreur TLP, Balslev H, Svenning J-C (2012) Cenozoic imprints on the phylogenetic structure of palm species assemblages worldwide. Proc Natl Acad Sci 109:7379–7384CrossRefGoogle Scholar
  34. Kottke I, Nebel M (2005) The evolution of mycorrhiza-like associations in liverworts: an update. New Phytol 167:330–334CrossRefGoogle Scholar
  35. Krömer T, Kessler M (2006) Filmy ferns (Hymenophyllaceae) as high-canopy epiphytes. Ecotropica 12:57–63Google Scholar
  36. Lehnert M, Kottke I, Setaro S, Pazmiño LF, Suárez JP, Kessler M (2009) Mycorrhizal associations in ferns from southern Ecuador. Amer Fern J 99:292–306CrossRefGoogle Scholar
  37. Lehnert M, Krug M, Kessler M (2017) A review of symbiotic fungal endophytes in lycophytes and ferns – a global phylogenetic and ecological perspective. Symbiosis 71:77–89CrossRefGoogle Scholar
  38. Lekberg Y, Rosendahl S, Olsson PA (2015) The fungal perspective of arbuscular mycorrhizal colonization in “nonmycorrhizal”plants. New Phytol 205:1399–1403CrossRefGoogle Scholar
  39. Marino P, Raguso R, Goffinet B (2009) The ecology and evolution of fly dispersed dung mosses (family Splachnaceae): manipulating insect behaviour through odour and visual cues. Symbiosis 47:61–76CrossRefGoogle Scholar
  40. Müller, J, Müller, K, Neinhuis, C, Quandt, D (2005) PhyDE-phylogenetic data editor. Program distributed by the authors. http://www.phyde.de. Accessed 27 Jan 2017
  41. Parker GG (1983) Throughfall and stemflow in the forest nutrient cycle. Adv Ecol Res 13:57–133CrossRefGoogle Scholar
  42. PPG I (2016) A community derived classification for extant ferns. J Syst Evol 54:561–705CrossRefGoogle Scholar
  43. Pressel S, Bidartondo MI, Field KJ, Rimington WR, Duckett JG (2016) Pteridophyte fungal associations: current knowledge and future perspectives. J Syst Evol 54:666–678CrossRefGoogle Scholar
  44. Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R (2004) Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am J Bot 91(10):1582–1598Google Scholar
  45. Rambaut A, Suchard MA, Xie D & Drummond AJ (2014) Tracer v1.6, Available from http://tree.bio.ed.ac.uk/software/tracer/. Accessed 9 May 2017
  46. Rimington WR, Pressel S, Duckett JG, Bidartondo MI (2015) Fungal associations of basal vascular plants: reopening a closed book? New Phytol 205:1394–1398CrossRefGoogle Scholar
  47. Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542CrossRefGoogle Scholar
  48. Scheckler SE (2001) In: DEG B, Crowther PR (eds) Afforestation: The first forests. Palaeobiology II. Blackwell Science, Oxford, pp 67–71Google Scholar
  49. Schiestl FP, Johnson SD (2013) Pollinator-mediated evolution of floral signals. Trends Ecol Evol 28:307–315CrossRefGoogle Scholar
  50. Schmid E, Oberwinkler F, Gomez LD (1995) Light and electron microscopy of a host–fungus interaction in the roots of some epiphytic ferns from Costa Rica. Can J Bot 73:991–996CrossRefGoogle Scholar
  51. Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallón S, Lupia R (2004) Ferns diversified in the shadow of angio sperms. Nature 428:553–557CrossRefGoogle Scholar
  52. Schuettpelz E, Pryer KM (2009) Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proc Natl Acad Sci U S A 106:11200–11205CrossRefGoogle Scholar
  53. Shaw AJ, Szövényi P, Shaw B (2011) Bryophyte diversity and evolution: windows into the early evolution of land plants. Am J Bot 98:352–369CrossRefGoogle Scholar
  54. Stöver B, Müller K (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinf 11:7CrossRefGoogle Scholar
  55. Testo W, Sundue M (2016) A 4000-species dataset provides new insight into the evolution of ferns. Mol Phylogenet Evol 105:200–211CrossRefGoogle Scholar
  56. Tewari LM, Tewari G, Nailwal T, Pangtey YPS (2009) Bark factors affecting the distribution of epiphytic fern communities. Nat Sci 7:76–81Google Scholar
  57. Tidwell WD, Ash SR (1994) A review of selected triassic to early cretaceous ferns. J Plant Res 107:417–442CrossRefGoogle Scholar
  58. Van Bocxlaer I, Roelants K, Biju SD, Nagaraju J, Bossuyt F (2006) Late cretaceous vicariance in Gondwanan amphibians. PLoS One 1:e74CrossRefGoogle Scholar
  59. van der Niet T, Peakall R, Johnson SD (2014) Pollinator-driven ecological speciation in plants: new evidence and future perspectives. Ann Bot 113:199–212CrossRefGoogle Scholar
  60. Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363CrossRefGoogle Scholar
  61. Wang B, Yeun LH, Xue J, Liu Y, Ané J, Qiu Y (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 186:514–525CrossRefGoogle Scholar
  62. Watkins JE, Cardelús CL (2012) Ferns in an angiosperm world: cretaceous radiation into the epiphytic niche and diversification on the Forest floor. Int J Plant Sci 173:695–710CrossRefGoogle Scholar
  63. Wheat CW, Vogel H, Wittstock U, Braby MF, Underwood D, Mitchell-Olds T (2007) The genetic basis of a plant–insect coevolutionary key innovation. Proc Natl Acad Sci 104:20427–20431CrossRefGoogle Scholar
  64. Willis A, Rodrigues BF, Harris PJC (2013) The ecology of arbuscular mycorrhizal fungi. CRC Crit Rev Plant Sci 32:1–20CrossRefGoogle Scholar
  65. Willson MF, Sabag C, Figueroa J, Armesto JJ (1996) Frugivory and seed dispersal of Podocarpus nubigena in Chiloe, Chile. Rev Chil Hist Nat 69:343–349Google Scholar
  66. Wolf PG, Sipes SD, White MR, Martines ML, Pryer KM, Smith AR, Ueda K (1999) Phylogenetic relationships of the enigmatic fern families Hymenophyllopsidaceae and Lophosoriaceae: evidence fromrbcL nucleotide sequences. Plant Syst Evol 219:263–270CrossRefGoogle Scholar
  67. Xu HH, Berry CM, Stein WE, Wang Y, Tang P, Fu Q (2017) Unique growth strategy in the Earth’s first trees revealed in silicified fossil trunks from China. PNAS:201708241Google Scholar
  68. Yoder JB, Clancey E, Des Roches S, Eastman JM, Gentry L, Godsoe W, Hagey TJ, Jochimsen D, Oswald BP, Robertson J (2010) Ecological opportunity and the origin of adaptive radiations. J Evol Biol 23:1581–1596CrossRefGoogle Scholar
  69. Zotz G (2013) The systematic distribution of vascular epiphytes–a critical update. Bot J Linn Soc 171:453–481CrossRefGoogle Scholar
  70. Zotz G (2016) Epiphyte taxonomy and evolutionary trends. Plants on plants–the biology of vascular epiphytes. Springer, p. 13–49Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Nees-Institut für Biodiversität der PflanzenRheinische Friedrich Wilhelms-Universität BonnBonnGermany

Personalised recommendations