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Globally rare oceanic-montane liverworts with disjunct distributions: evidence for long-distance dispersal

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Abstract

Disjunct distributions in bryophytes are well known, but when it comes to the mechanisms that have shaped these distributions, especially for apparently sterile species, the historical processes leading to inter-continental disjunctions remain enigmatic. In this study, we developed microsatellite markers to investigate the spatial distribution and extent of genotypic diversity of 147 Anastrophyllum alpinum samples collected from three populations each in Nepal and Scotland (UK). For a more general insight into genetic differences, sequence divergence in A. alpinum and eight other globally rare and disjunct oceanic-montane liverworts was also assessed. A nested allele distribution of Scottish populations of A. alpinum within the allele range of the Nepalese populations, and lower levels of genetic diversity within Scottish samples indicate that the Scottish populations likely have their origins in the Sino-Himalaya. The evidence for long-distance dispersal was supported by a lack of sequence divergence in chloroplast DNA between Scottish and Nepalese populations, with only a single substitution detected from 5160 bp of plastid sequence. Low levels of sequence divergence were also detected in species with similar distributions. While Scottish populations of A. alpinum do not appear to produce spores, they do still harbour a considerable genetic diversity. This indicates that sexual reproduction has been important at some point in their history. However, the current absence of evidence for sexual reproduction needs to be taken into account when designing conservation actions for these montane species, to ensure population maintenance and ability to track suitable climate and habitat space.

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References

  • Averis AM (1992) Where are all the hepatic mat liverworts in Scotland? Bot J Scotland 46:191–198

    Google Scholar 

  • Averis AM (1994) The ecology of an Atlantic liverwort community. PhD, University of Edinburgh

  • Barnett C, Hossell J, Perry M, Procter C, Hughes G (2006) Patterns of climate trends across Scotland: technical report. Sniffer project CC03. Scotland and Northern Ireland Forum for Environmental Research, Edinburgh, UK

  • Bell NE, Ignatov MS (2019) Placing the regionally threatened moss Orthodontium gracile in the big picture-Phylogeny, genome incongruence and anthropogenic dispersal in the order Orthodontiales. Mol. Phylogenet Evol 134:186–199

  • Birks HJB (1988) Long-term ecological change in the British Uplands. In: Usher MB, Thompson DBA (eds) Ecological change in the uplands. Blackwell Scientific Publications, Oxford

  • Chmielewski MW, Eppley SM (2019) Forest passerines as a novel dispersal vector of viable bryophyte propagules. Proc R Soc B 268:20182253

    Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cox CJ, Goffinet B, Newton AE, Shaw AJ, Hedderson TA (2000) Phylogenetic relationships among the diplolepidous-alternate mosses (Bryidae) inferred from nuclear and chloroplast DNA sequences. Bryologist 103:224–241

    CAS  Google Scholar 

  • Crum HA (1972) The geographic origins of the mosses of North America's eastern deciduous forest. J Hattori Bot Lab 35:269–298

    Google Scholar 

  • Demesure B, Sodzi N, Petit RJ (1995) A set of primers for the amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4:129–131

    CAS  PubMed  Google Scholar 

  • Dumolin-Lapegue S, Pemange MH, Petit RJ (1997) An enlarged set of consensus primers for the study of organelle DNA in plants. Mol Ecol 6:393–397

    CAS  PubMed  Google Scholar 

  • During HJ (1979) Life strategies of bryophytes: a preliminary review. Lindbergia 5:2–8

    Google Scholar 

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Mol Ecol 17:1170–1188

    CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feldberg K, Hentschel J, Wilson R, Rycroft DS, Glenny D, Heinrichs J (2007) Phylogenetic biogeography of the leafy liverwort Herbertus (Jungermanniales, Herbertaceae) based on nuclear and chloroplast DNA sequence data: correlation between genetic variation and geographical distribution. J Biogeogr 34:688–698

    Google Scholar 

  • Feldberg K, Váňa J, Long DG, Shaw AJ, Hentschel J, Heinrichs J (2010) A phylogeny of Adelanthaceae (Jungermanniales, Marchantiophyta) based on nuclear and chloroplast DNA markers, with comments on classification, cryptic speciation and biogeography. Mol Phylogenet Evol 55:293–304

    CAS  PubMed  Google Scholar 

  • Flagmeier M, Long DG, Genney DR, Hollingsworth PM, Woodin SJ (2013) Regeneration capacity of oceanic-montane liverworts: implications for community distribution and conservation. J Bryol 35:12–19

    Google Scholar 

  • Flagmeier M, Long DG, Genney DR, Hollingsworth PM, Ross LC, Woodin SJ (2014) Fifty years of vegetation change in oceanic-montane liverwort-rich heath in Scotland. Plant Ecol Divers 7:457–470

    Google Scholar 

  • Flagmeier M, Hollingsworth PM, Genney DR, Long DG, Muñoz J, Moreno-Jiménez E, Woodin SJ (2016) Transplanting the leafy liverwort Herbertus hutchinsiae: a suitable conservation tool to maintain oceanic-montane liverwort-rich heath? Plant Ecol Divers 9:175–185

    Google Scholar 

  • Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (ver. 2.9.3.2). https://www2.unil.ch/izea/software/fstat.html

  • Hassel K, Blom HH, Flatberg KI, Halvorsen R, Johansen JI (2010) Moser: anthocerophyta, marchantiophyta, bryophyta. In: Kålås J, Viken Å, Henriksen S, Skjelseth S (eds) The 2010 Norwegian red list for species. Norwegian Biodiversity Information Centre, Norway, pp 139–153

    Google Scholar 

  • He X, Sun Y (2017) Contrasting patterns of postglacial range shifts between the northern and southern hemisphere in Herbertus (Herbertaceae, Marchantiophyta). Syst Biodivers 15:541–551

    Google Scholar 

  • Heinrichs J, Broth H, Lindner M, Renker C, Pócs T, Pröschold T (2004) Intercontinental distribution of Plagiochila corrugata (Plagiochilaceae, Hepaticae) inferred from nrDNA ITS sequences and morphology. Bot J Linn Soc 146:469–481

    Google Scholar 

  • Heinrichs J, Lindner M, Groth H, Renker C (2005) Distribution and synonymy of Plagiochila punctata (Taylor) Taylor, with hypotheses on the evolutionary history of Plagiochila sect. Arrectae (Plagiochilaceae, Hepaticae). Plant Syst Evol 250:105–117

    Google Scholar 

  • Hill MO, Preston CD, Smith AJ (1991) Atlas of the bryophytes of Britain and Ireland. Liverworts, vol 1. Harley Books, Colchester

    Google Scholar 

  • Hodd RL, Bourke D, Sheehy Skeffington M (2014) Projected range contractions of european protected oceanic montane plant communities: focus on climate change impacts is essential for their future conservation. PLoS ONE 9:e95147

    PubMed  PubMed Central  Google Scholar 

  • Hodgetts NG (2011) A revised Red List of bryophytes in Britain. Field Bryol 103:41–49

    Google Scholar 

  • Hodgetts NG (2015) Checklist and country status of European bryophytes—towards a new Red List for Europe. National Parks and Wildlife Service, Department of Arts, Heritage and the Gaeltacht, Ireland. Irish Wildlife Manuals 84

  • Hodgetts N, Cálix M, Englefield E et al (2019) A miniature world in decline: European Red List of Mosses, Liverworts and Hornworts. IUCN, Brussels

    Google Scholar 

  • Hola E, Košnar J, Kučera J (2015) Comparison of Genetic Structure of Epixylic Liverwort Crossocalyx hellerianus between Central European and Fennoscandian Populations. PLoS ONE 10:e0133134

    PubMed  PubMed Central  Google Scholar 

  • Holyoak DT (2006) Progress towards a species inventory for conservation of bryophytes in Ireland. Proc R Ir Acad 106B:225–236

    Google Scholar 

  • Hugonnot V, Blay B, Celle J (2014) The male gender as a key for understanding the reproductive biology of Anomobryum concinnatum (Spruce) Lindb. J Bryol 36:244–248

    Google Scholar 

  • Klamá H, Górski P (2018) Red list of liverworts and hornworts of Poland. Cryptogam Bryol 39:415–441

    Google Scholar 

  • Korpelainen H, Pohjamo M, Laaka-Lindberg S (2005) How efficiently does bryophyte dispersal lead to gene flow? J Hattori Bot Lab 97:195–205

    Google Scholar 

  • Korpelainen H, Von Cräutlein M, Laaka-Lindberg S, Huttunen S (2011) Fine-scale spatial genetic structure of a liverwort (Barbilophozia attenuata) within a network of ant trails. Evol Ecol 25:45–57

    Google Scholar 

  • Korpelainen H, Forsman H, Virtanen V, Pietiläinen M, Kostamo K (2012) Genetic composition of bryophyte populations occupying habitats differing in the level of human disturbance. Int J Plant Sci 173:1015–1022

    Google Scholar 

  • Laaka-Lindberg S, Hedderson TA, Longton RE (2000) Rarity and reproductive characters in the British hepatic flora. Lindbergia 25:78–84

    Google Scholar 

  • 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 plumaje of transequatorial migrant birds. PeerJ 2:e424

    PubMed  PubMed Central  Google Scholar 

  • Long DG (2010) The tragedy of the Twelve Bens of Connemara: is there a future for Adelanthus lindenbergianus? Field Bryol 100:2–8

    Google Scholar 

  • Long DG, Paton JA, Squirrell J, Woodhead M, Hollingsworth PM (2006) Morphological, ecological and genetic evidence for distinguishing Anastrophyllum joergensenii Schiffn. and A. alpinum Steph. (Jungermanniopsida: Lophoziaceae). J Bryol 28:108–117

    Google Scholar 

  • Longton RE, Schuster RM (1983) Reproductive biology. New Manual Bryol 1:386–462

    Google Scholar 

  • Mehta P, Sekar KC, Bhatt D et al (2020) Conservation and prioritization of threatened plants in Indian Himalayan Region. Biodivers Conserv. https://doi.org/10.1007/s10531-020-01959-x

    Article  Google Scholar 

  • Moore O, Crawley MJ (2015) The impact of red deer on liverwort-rich oceanic heath vegetation. Plant Ecol Divers 8:437–447

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    CAS  PubMed  Google Scholar 

  • Nadot S, Bajon R, Lejeune B (1994) The chloroplast gene rps4 as a toll for the study of the Poaceae phylogeny. Plant Syst Evol 191:27–38

    Google Scholar 

  • Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. PhD, University of Dublin

  • Patiño J, Vanderpoorten A (2018) Bryophyte biogeography. CRC Crit Rev Plant Sci 37:175–209

    Google Scholar 

  • Paton JA (1999) The liverwort flora of the British Isles. Harley Books, Colchester

    Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28:2537–2539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. Heredity 90:502–503

    Google Scholar 

  • Pócs T (1976) Correlations between the tropical African and Asian bryofloras. J Hattori Bot Lab 41:95–106

    Google Scholar 

  • Pohjamo M, Korpelainen H, Kalinauskaité N (2008) Restricted gene flow in the clonal hepatic Trichocolea tomentella in fragmented landscapes. Biol Conserv 141:1204–1217

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ratcliffe DA (1968) An ecological account of Atlantic bryophytes in the British Isles. New Phytol 67:365–439

    Google Scholar 

  • Ratcliffe DA, Thompson DBA (1988) The British Uplands: their ecological character and international significance. In: Usher MB, Thompson DBA (eds) Ecological change in the uplands. Blackwells, London, pp 9–36

    Google Scholar 

  • Russo NJ, Robertson M, MacKenzie R, Goffinet B, Jiménez JE (2020) Evidence of targeted consumption of mosses by birds in Sub-Antarctic South America. Austral Ecol 45:399–403

    Google Scholar 

  • Schill D, Long DG (2003) A revision of Anastrophyllum (Spruce) Steph. (Jungermanniales, Lophoziaceae) in the Himalayan region and western China. Hattori Bot Lab 94:115–157

    Google Scholar 

  • Schofield WB, Crum HA (1972) Disjunctions in bryophytes. Ann Mo Bot Gard 59:174–202

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin: A software for population genetics data analysis. ver 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva

  • Schumacker R, Váňa J (2005) Identification keys to the liverworts and hornworts of Europe and Macaronesia (distribution and status), 2nd edn. Sorus Publishing, Poznań

    Google Scholar 

  • Schuster RM (1983) Phytogeography of the Bryophyta. In: Schuster RM (ed) New manual of bryology. Hattori Botanical Laboratory, Nichinan, pp 463–626

    Google Scholar 

  • Shaw AJ (2001) Biogeographic patterns and cryptic speciation in bryophytes. J Biogeogr 28:253–261

    Google Scholar 

  • Shaw AJ, Werner O, Ros RM (2003) Intercontinental Mediterranean disjunct mosses: morphological and molecular patterns. Am J Bot 90:540–550

    PubMed  Google Scholar 

  • Stamati K, Hollingsworth PM, Russell J (2007) Patterns of clonal diversity in three species of sub-arctic willow (Salix lanata, Salix lapponum and Salix herbacea). Plant Syst Evol 269:75–88

    Google Scholar 

  • Squirrell J, Woodhead M, Hollingsworth PM, Russell J, Gibby M, Powell W (2004) Isolation of polymorphic microsatellite markers for the Alpine Lady Fern, Athyrium distentifolium Tausch ex Opiz, from an enriched genomic library. Conserv Genet 5:283–286

    CAS  Google Scholar 

  • Squirrell J, Hollingsworth PM, Bateman RM, Tebbitt MC, Hollingsworth ML (2002) Taxonomic complexity and breeding system transitions: conservation genetics of the Epipactis leptochila complex (Orchidaceae). Mol Ecol 11:1957–1964

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Travis JMJ (2003) Climate change and habitat destruction: a deadly anthropogenic cocktail. Proc R Soc Lond B 270:467–473

    CAS  Google Scholar 

  • Van Zanten BO, Gradstein SR (1988) Experimental dispersal geography of neotropical liverworts. Nova Hedwig 90:41–94

    Google Scholar 

  • Vigalondo B, Lara F, Draper I, Valcarcel V, Garilleti R, Mazimpaka V (2016) Is it really you, Orthotrichum acuminatum? Ascertaining a new case of intercontinental disjunction in mosses. Bot J Linn Soc 180:30–49

    Google Scholar 

  • Wang J (2017) The computer program STRUCTURE for assigning individuals to populations: easy to use but easier to misuse. Mol Ecol Resour 17:981–990

    CAS  PubMed  Google Scholar 

  • Wangen K, Speed JDM, Hassel K (2016) Hyper-oceanic liverwort species of conservation concern: evidence for dispersal limitation and identification of suitable uncolonised regions. Biodivers Conserv 25:1053–1071

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:6531–6535

    Google Scholar 

  • Woodhead M, Russell J, Squirrell J, Hollingsworth PM, Cardle L, Ramsay L, Gibby M, Powell W (2003) Development of EST-SSRs from the Alpine Lady-fern, Athyrium distentifolium. Mol Ecol Resour 3:287–290

    CAS  Google Scholar 

  • Zachariah Peery M, Kirby R, Reid BN, Stoelting R, Doucet-Beer E, Robinson S, Vásquez-Carillo C, Pauli JN, Palsbøll EJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

    PubMed  Google Scholar 

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Acknowledgements

The Royal Botanic Garden Edinburgh (RBGE) is supported by the Scottish Government’s Rural and Environment Science and Analytical Services Division, and the former Scottish Executive Environmental and Rural Affairs Department helped fund the project “Microsatellites as Population Genetic markers”. During 2020 we are also grateful for the support of players of People’s Postcode Lottery towards our scientific research. DGL thanks the Royal Horticultural Society, University of Edinburgh Davis Expedition Fund, Gordon Fraser Charitable Trust, Merlin Trust, William Steel Trust, Percy Sladen Trust and the Oleg Polunin Fund for supporting the Edinburgh Nepal Expedition. MF is grateful for funding from the Sibbald Trust, project 2018#27 (Population structure & dispersal in montane liverworts). We thank Markus Ruhsam and two anonymous reviewers for helpful comments on the manuscript.

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Flagmeier, M., Squirrell, J., Woodhead, M. et al. Globally rare oceanic-montane liverworts with disjunct distributions: evidence for long-distance dispersal. Biodivers Conserv 29, 3245–3264 (2020). https://doi.org/10.1007/s10531-020-02022-5

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