Polar Biology

, Volume 41, Issue 4, pp 599–610 | Cite as

Low genetic variation between South American and Antarctic populations of the bank-forming moss Chorisodontium aciphyllum (Dicranaceae)

  • E. M. BiersmaEmail author
  • J. A. Jackson
  • T. J. Bracegirdle
  • H. Griffiths
  • K. Linse
  • P. Convey
Original Paper


The Antarctic–South American bank-forming moss Chorisodontium aciphyllum is known for having the oldest sub-fossils of any extant plant in Antarctica as well as extreme survival abilities, making it a candidate species for possible long-term survival in Antarctica. Applying phylogeographic and population genetic methods using the plastid markers trnL-F and rps4 and the nuclear internal transcribed spacer, we investigated the genetic diversity within C. aciphyllum throughout its range. Low genetic variation was found in all loci, both between and within Antarctic and southern South American populations, suggesting a relatively recent (likely within the last million years) colonization of this moss to the Antarctic, as well as a likely severe bottleneck during Pleistocene glaciations in southern South America. We also performed a simple atmospheric transfer modeling approach to study potential colonization rates of small (microscopic/microbial) or spore-dispersed organisms (such as many mosses and lichens). These suggested that the northern Antarctic Peninsula shows potentially regular connectivity from southern South America, with air masses transferring, particularly southbound, between the two regions. We found elevated genetic variation of C. aciphyllum in Elephant Island, also the location of the oldest known moss banks (> 5500 years), suggesting this location to be a genetic hotspot for this species in the Antarctic.


Bryophyte LGM Last glacial maximum Peat moss Sub-Antarctic Wind 



We thank Helen Peat at the AAS herbarium (British Antarctic Survey; BAS) for access to herbarium specimens; Dr. Jessica Royles for providing fresh samples, Instituto Antartico Chileno (INACH) for logistic support; and Laura Gerrish (BAS) for preparing Fig. 2. Thanks to James Fenton for the photographs shown in Fig. 1. This research was funded by a Natural Environment Research Council (NERC) Ph.D. studentship (ref. NE/K50094X/1) to E.M.B. and supported by NERC core funding to the BAS Biodiversity, Evolution and Adaptation Team. This study also contributes to the Scientific Committee on Antarctic Research ‘State of the Antarctic Ecosystem’ programme.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Allegrucci G, Carchini G, Todisco V, Convey P, Sbordoni V (2006) A molecular phylogeny of Antarctic Chironomidae and its implications for biogeographical history. Polar Biol 29:320–326CrossRefGoogle Scholar
  2. Allegrucci G, Carchini G, Convey P, Sbordoni V (2012) Evolutionary geographic relationships among orthocladine chironomid midges from maritime Antarctic and sub-Antarctic islands. Biol J Linn Soc 106:258–274CrossRefGoogle Scholar
  3. Bartlett JK, Frahm J-P (1983) Notes on Campylopus and Chorisodontium from New Zealand. J Bryol 12:365–382CrossRefGoogle Scholar
  4. Biersma EM, Jackson JA, Hyvönen J, Koskinen S, Linse K, Griffiths H, Convey P (2017) Global biogeographic patterns in bipolar moss species. R Soc Open Sci 4:170147CrossRefPubMedPubMedCentralGoogle Scholar
  5. Björck S, Malmer N, Hjort C, Sandgren P, Ingólfsson Ó, Wallén B, Smith RIL, Jónsson BL (1991) Stratigraphic and paleoclimatic studies of a 5500-year-old moss bank on Elephant Island, Antarctica. Arct Alp Res 23:361–374CrossRefGoogle Scholar
  6. Blattner FR (1999) Direct amplification of the entire ITS region from poorly preserved plant material using recombinant PCR. Biotechniques 27:1180–1186PubMedGoogle Scholar
  7. Chong CW, Pearce DA, Convey P (2015) Emerging spatial patterns in Antarctic prokaryotes. Front Microbiol 6:1058. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Collins NJ (1976a) The development of moss-peat banks in relation to changing climate and ice cover on Signy Island in the maritime Antarctic. Br Antarct Surv B 43:85–102Google Scholar
  9. Collins NJ (1976b) Growth and population dynamics of the moss Polytrichum alpestre in the Maritime Antarctic. Oikos 27:389–401CrossRefGoogle Scholar
  10. Convey P, Stevens MI (2007) Antarctic biodiversity. Science 317:1877–1878CrossRefPubMedGoogle Scholar
  11. Convey P, Gibson JA, Hillenbrand CD, Hodgson DA, Pugh PJ, Smellie JL, Stevens MI (2008) Antarctic terrestrial life - challenging the history of the frozen continent? Biol Rev 83:103–117CrossRefPubMedGoogle Scholar
  12. Convey P, Bindschadler R, Di Prisco G, Fahrbach E, Gu J, Hodgson DA, Mayewski PA, Summerhayes CP, Turner J, ACCE Consortium (2009a) Antarctic climate change and the environment. Antarct Sci 21:541–563CrossRefGoogle Scholar
  13. Convey P, Stevens MI, Hodgson DA, Smellie JL, Hillenbrand C-D, Barnes DKA, Clarke A, Pugh PJA, Linse K, Cary SC (2009b) Exploring biological constraints on the glacial history of Antarctica. Quat Sci Rev 28:3035–3048CrossRefGoogle Scholar
  14. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. CrossRefPubMedPubMedCentralGoogle Scholar
  15. De Wever A, Leliaert F, Verleyen E, Vanormelingen P, Van der Gucht K, Hodgson DA, Sabbe K, Vyverman W (2009) Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proc R Soc Lond B Biol Sci 276:3591–3599CrossRefGoogle Scholar
  16. Department of Conservation, New Zealand (2013) New listing of the threatened status of New Zealand bryophytes, consultation closed Aug 2013. Accessed 10 Sept 2017
  17. Fenton JHC (1980) The rate of peat accumulation in Antarctic moss banks. J Ecol 68:211–228CrossRefGoogle Scholar
  18. Fenton JHC (1982a) The formation of vertical edges on Antarctic moss peat banks. Arct Alp Res 14:21–26CrossRefGoogle Scholar
  19. Fenton JHC (1982b) Vegetation re-exposed after burial by ice and its relationship to changing climate in the South Orkney Islands. Brit Antarct Surv B 51:247–255Google Scholar
  20. Fenton JHC, Smith RIL (1982) Distribution, composition and general characteristics of the moss banks of the maritime Antarctic. Br Antarct Surv B 51:215–236Google Scholar
  21. Frahm JP (1989) The genus Chorisodontium (Dicranaceae, Musci) in the Neotropics. Bryophyt Divers Evol 1:11–24CrossRefGoogle Scholar
  22. Fraser CI, Nikula R, Ruzzante DE, Waters JM (2012) Poleward bound: biological impacts of Southern Hemisphere glaciation. Trends Ecol Evol 27:462–471CrossRefPubMedGoogle Scholar
  23. Fraser CI, Terauds A, Smellie J, Convey P, Chown SL (2014) Geothermal activity helps life survive glacial cycles. Proc Natl Acad Sci USA 111:5634–5639. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Guglielmin M, Convey P, Malfasi F, Cannone N (2015) Glacial fluctuations since the ‘Medieval Warm Period’ at Rothera Point (western Antarctic Peninsula). Holocene 26:154–158CrossRefGoogle Scholar
  25. Hills SF, Stevens MI, Gemmill CEC (2010) Molecular support for Pleistocene persistence of the continental Antarctic moss Bryum argenteum. Antarct Sci 22:721–726CrossRefGoogle Scholar
  26. Hodgson DA, Convey P (2005) A 7000-year record of oribatid mite communities on a maritime-Antarctic island: responses to climate change. Arct Alp Res 37:239–245CrossRefGoogle Scholar
  27. Hulton NRJ, Purves RS, McCulloch RD, Sugden DE, Bentley MJ (2002) The last glacial maximum and deglaciation in southern South America. Quat Sci Rev 21:233–241CrossRefGoogle Scholar
  28. Hyvönen J (1991) Chorisodontium (Dicranaceae, Musci) in southern South America. Ann Bot Fenn 28:247–258Google Scholar
  29. Iakovenko NS, Smykla J, Convey P, Kašparová E, Kozeretska IA, Trokhymets V, Dykyy I, Plewka M, Devetter M, Duriš Z, Janko K (2015) Antarctic bdelloid rotifers: diversity, endemism and evolution. Hydrobiologia 761:5–43CrossRefGoogle Scholar
  30. Kato K, Arikawa T, Imura S, Kanda H (2013) Molecular identification and phylogeny of an aquatic moss species in Antarctic lakes. Polar Biol 36:1557–1568CrossRefGoogle Scholar
  31. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. CrossRefPubMedGoogle Scholar
  32. Leigh JW, Bryant D (2015) PopART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116CrossRefGoogle Scholar
  33. Les DH, Crawford DJ, Kimball RT, Moody ML, Landolt E (2003) Biogeography of discontinuously distributed hydrophytes: a molecular appraisal of intercontinental disjunctions. Int J Plant Sci 164:917–932CrossRefGoogle Scholar
  34. Lewis LR, Behling E, Gousse H, Qian E, Elphick CS, Lamarre JF, Bêty J, Liebezeit J, Rozzi R, Goffinet B (2014) First evidence of bryophyte diaspores in the plumage of transequatorial migrant birds. PeerJ 2:e424CrossRefPubMedPubMedCentralGoogle Scholar
  35. Marshall GJ (2003) Trends in the southern annular mode from observations and reanalyses. J Clim 16:4134–4143CrossRefGoogle Scholar
  36. McGaughran A, Stevens MI, Holland B (2010) Biogeography of circum-Antarctic springtails. Mol Phylogenet Evol 57:48–58CrossRefPubMedGoogle Scholar
  37. Nadot S, Bajon R, Lejeune B (1994) The chloroplast generps 4 as a tool for the study of Poaceae phylogeny. Plant Syst Evol 191:27–38CrossRefGoogle Scholar
  38. Ochyra R, Smith RIL, Bednarek-Ochyra H (2008) The illustrated moss flora of Antarctica. Cambridge University Press, CambridgeGoogle Scholar
  39. Peat HJ, Clarke A, Convey P (2007) Diversity and biogeography of the Antarctic flora. J Biogeogr 34:132–146CrossRefGoogle Scholar
  40. Pisa S, Biersma EM, Convey P, Patiño J, Vanderpoorten A, Werner O, Ros RM (2014) The cosmopolitan moss Bryum argenteum in Antarctica: recent colonisation or in situ survival? Polar Biol 37:1469–1477CrossRefGoogle Scholar
  41. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6.
  42. Roads E, Longton RE, Convey P (2014) Millennial timescale regeneration in a moss from Antarctica. Curr Biol 24:R222–R223. CrossRefPubMedGoogle Scholar
  43. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  44. Royles J, Amesbury MJ, Roland TP, Jones GD, Convey P, Griffiths H, Hodgson DA, Charman DJ (2016) Moss stable isotopes (carbon-13, oxygen-18) and testate amoebae reflect environmental inputs and microclimate along a latitudinal gradient on the Antarctic Peninsula. Oecologia 181:931–945CrossRefPubMedPubMedCentralGoogle Scholar
  45. Sersic AN, Cosacov A, Cocucci AA, Johnson LA, Pozner R, Avila LJ, Sites JW Jr, Morando M (2011) Emerging phylogeographical patterns of plants and terrestrial vertebrates from Patagonia. Biol J Linn Soc 103:475–494CrossRefGoogle Scholar
  46. Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381CrossRefPubMedGoogle Scholar
  47. Smith RIL (1972) Vegetation of the South Orkney Islands with particular reference to Signy Island. British Antarctic Survey Scientific Reports No. 68. British Antarctic Survey, LondonGoogle Scholar
  48. Smith RIL (1979) Peat forming vegetation in the Antarctic. In: Kivunen E, Heikurainen EL, Pakarinen P (eds) Classification of peat and peatlands. International Peat Society, Helsinki, pp 38–67Google Scholar
  49. Smith RIL (1990) Signy Island as a paradigm of biological and environmental change in Antarctic terrestrial ecosystems. In: Kerry KR, Hempel G (eds) Antarctic ecosystems: ecological change and conservation. Springer, Berlin, pp 32–50CrossRefGoogle Scholar
  50. Smith RIL (1996) Terrestrial and freshwater biotic components of the western Antarctic Peninsula. In: Ross R, Hofmann E, Quetin L (eds) Foundations for ecological research west of the Antarctic Peninsula. American Geophysical Union, Washington, D.C., pp 15–59CrossRefGoogle Scholar
  51. Souza-Chies TT, Bittar G, Nadot S, Carter L, Besin E, Lejeune B (1997) Phylogenetic analysis of Iridaceae with parsimony and distance methods using the plastid gene rps4. Plant Syst Evol 204:109–123. CrossRefGoogle Scholar
  52. Stech M (1999) Molekulare Systematik haplolepider Laubmoose (Dicrananae, Bryopsida). Freie Universität Berlin, BerlinGoogle Scholar
  53. Stech M, Quandt D (2010) 20,000 species and five key markers: the status of molecular bryophyte phylogenetics. Phytotaxa 9:196–228CrossRefGoogle Scholar
  54. Stevens MI, Greenslade P, Hogg ID, Sunnucks P (2006) Southern Hemisphere springtails: could any have survived glaciation of Antarctica? Mol Biol Evol 23:874–882CrossRefPubMedGoogle Scholar
  55. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109CrossRefPubMedGoogle Scholar
  56. Uppala SM et al (2005) The ERA-40 re-analysis. ‎Q J R Meteorol Soc 131:2961–3012. CrossRefGoogle Scholar
  57. Viana DS, Santamaría L, Figuerola J (2016) Migratory birds as global dispersal vectors. Trends Ecol Evol 31:763–775CrossRefPubMedGoogle Scholar
  58. Vyverman W, Verleyen E, Wilmotte A, Hodgson DA, Willems A, Peeters K, Van de Vijver B, De Wever A, Leliaert F, Sabbe K (2010) Evidence for widespread endemism among Antarctic micro-organisms. Polar Sci 4:103–113CrossRefGoogle Scholar
  59. White TJ, Bruns T, Lee SJWT, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • E. M. Biersma
    • 1
    • 2
    Email author
  • J. A. Jackson
    • 1
  • T. J. Bracegirdle
    • 1
  • H. Griffiths
    • 2
  • K. Linse
    • 1
  • P. Convey
    • 1
    • 3
  1. 1.British Antarctic Survey, Natural Environment Research CouncilCambridgeUK
  2. 2.Department of Plant SciencesUniversity of CambridgeCambridgeUK
  3. 3.National Antarctic Research Center, Institute of Graduate Studies, University of MalayaKuala LumpurMalaysia

Personalised recommendations