Skip to main content
SpringerLink
Log in

Fine-scale spatial genetic structure of a liverwort (Barbilophozia attenuata) within a network of ant trails

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Fine-scale spatial genetic structure (SGS) of the liverwort, Barbilophozia attenuata, occupying an area characterized by a network of ant trails, was investigated using microsatellite markers. This is the first study investigating SGS in a liverwort. Significant genetic differentiation was detected among colonies along and outside ant trails, and the SGS pattern varied depending on the spatial scale. At short distances, kinship coefficients were significantly positive up to about eight meters, after which they approached zero and turned negative, while at distances greater than 25 m the values were about zero. Thus, nearby individuals are more closely related than expected, at mid-distances less related, and at great distances genotypes show a random distribution. We suggest that the reproductive mode strongly affects SGS in B. attenuata. Asexual propagation by relatively large gemmae allows more effective establishment than sexual reproduction by small-sized spores, and causes an aggregation of similar genotypes, although the inbreeding effect cannot be ruled out. In environments with small-scale disturbances, e.g., ant trails, gemmae are favoured over spores at establishment. Also, the diaspore bank of the forest floor can be activated by disturbances, which may affect SGS. At mid-distances, the isolation by distance effect, presumably related to comparatively ineffective gemma dispersal, is visible, while at greater distances, the role of spores as effective means of dispersal is evident. The Sp statistic values, which quantify the strength of SGS, indicate that outsider colonies possess less SGS than do plant colonies along ant trails, which relates to the more frequent spore production of outsider colonies. Moreover, dispersal from fallen logs or stumps may be more effective than dispersal from ground-level colonies along ant trails. Apparently, ants do not have much role as dispersal vectors, nor do the physical structures of ant trails as dispersal corridors, although they provide open areas for colonization.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andersson K (2002) Dispersal of spermatozoids from splash-cups of the moss Plagiomnium affine. Lindbergia 27:90–96

    Google Scholar 

  • Bengtsson BO, Cronberg N (2009) The effective size of bryophyte populations. J Theor Biol 258:121–126

    Article  PubMed  Google Scholar 

  • Born C, Hardy OJ, Chevallier M-H, Ossari S, Attéké C, Wickings J, Hossaert-McKey M (2008) Small-scale spatial genetic structure in the Central African rainforest tree species Aucoumea klaineana: a stepwise approach to infer the impact of limited gene dispersal, population history and habitat fragmentation. Mol Ecol 17:2041–2050

    Article  PubMed  Google Scholar 

  • Cronberg N, Rydgren K, Økland RH (2006) Clonal structure and genet-level sex ratios suggest diffreent roles of vegetative and sexual reproduction in the clonal moss Hylocomium splendens. Ecography 29:95–103

    Article  Google Scholar 

  • Damsholt K (2002) Illustrated flora of nordic liverworts and hornworts. Nordic Bryological Society, Lund

    Google Scholar 

  • Ennos RA (2001) Inferences about spatial processes in plant populations from the analysis of molecular markers. In: Silvertown J, Antonovics J (eds) Integrating ecology and evolution in a spatial context. Blackwell, Cambridge, pp 45–71

    Google Scholar 

  • Epperson BK (2003) Geographical genetics. Princeton University Press, New Jersey

    Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin Ver. 3.0: an integrated software package for population genetics data analysis. Computational and Molecular Population Genetics Lab, University of Berne, Switzerland

    Google Scholar 

  • Gunnarsson U, Shaw AJ, Lonn M (2007) Local-scale genetic structure in the peatmoss Sphagnum fuscum. Mol Ecol 16:305–312

    Article  CAS  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hardy OJ, Maggia L, Bandou E, Breyne P, Caron H, Chevallier M-H, Doligez A, Dutech C, Kremer A, Latouche-Hallé C, Troispoux V, Veron V, Degen B (2006) Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Mol Ecol 15:559–571

    Article  CAS  PubMed  Google Scholar 

  • Hedenås H, Bolyukh VO, Jonsson BG (2003) Spatial distribution of epiphytes on Populus tremula in relation to dispersal mode. J Veget Sci 14:233–242

    Article  Google Scholar 

  • Heinken T, Rohner MS, Hoppert M (2007) Red wood ants (Formica rufa group) disperse bryophyte and lichen fragments on a local scale. Nova Hedw 131:147–163

    Google Scholar 

  • Hock Z, Szövenyi P, Schneller JJ, Toth Z, Urmi E (2008) Bryophyte diaspore bank: a genetic memory? Genetic structure and genetic diversity of surface populations and diaspore bank in the liverwort Mannia fragrans (Aytoniaceae). Am J Bot 95:542–548

    Article  CAS  Google Scholar 

  • Hutsemekers V, Dopagne C, Vanderpoorten A (2008a) How far and how fast do bryophytes travel at the landscape scale? Divers Distrib 14:483–492

    Article  Google Scholar 

  • Hutsemekers V, Risterucci AM, Ricca M, Boles S, Hardy OJ, Shaw AJ, Vanderpoorten A (2008b) Identification and characterization of nuclear microsatellite loci in the aquatic moss Platyhypnidium riparioides (Brachytheciaceae). Mol Ecol Res 8:1130–1132

    Article  CAS  Google Scholar 

  • Jonsson BG (1993) The bryophyte diaspore bank and its role after small-scale disturbance in a boreal forest. J Veg Sci 4:819–826

    Article  Google Scholar 

  • Kimmerer RW (1991) Reproductive ecology of Tetraphis pellucida II. How far and how fast do bryophytes travel at the landscape scale? Bryologist 94:284–288

    Article  Google Scholar 

  • Kimmerer RW (1994) Ecological consequences of sexual versus asexual reproduction in Dicranum flagellare and Tetraphis pellucida. Bryologist 97:20–25

    Article  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, Kostamo K, Virtanen V (2007) Microsatellite marker identification using genome screening and restriction-ligation. BioTechniques 42:479–486

    Article  CAS  PubMed  Google Scholar 

  • Korpelainen H, Kostamo K, Karttunen H, Virtanen V, Pohjamo M (2008a) Isolation and characterization of microsatellite loci for twenty common bryophyte species. In: Mohamed H, Baki BB, Nasrulhaq-Boyce A, Lee PKY (eds) Bryology in the new millennium. University of Malaya, Kuala Lumpur, pp 241–257

    Google Scholar 

  • Korpelainen H, Virtanen V, Kostamo K, Karttunen H (2008b) Molecular evidence shows that the moss Rhytidiadelphus subpinnatus (Hylocomiaceae) is clearly distinct from R. squarrosus. Mol Phylogenet Evol 48:372–376

    Article  CAS  PubMed  Google Scholar 

  • Laaka-Lindberg S, Korpelainen H, Pohjamo M (2003) Dispersal of asexual propagules in bryophytes. J Hattori Bot Lab 93:319–330

    Google Scholar 

  • Laaka-Lindberg S, Korpelainen H, Pohjamo M (2006) Spatial distribution of epixylic hepatics in relation to substrate in a boreal old-growth forest. J Hattori Bot Lab 100:311–323

    Google Scholar 

  • Leonardia AAP, Kumar PP, Tan B (2006) Development of microsatellite markers for the tropical moss, Acanthorrhynchium papillatum. Mol Ecol Notes 6:396–398

    Article  CAS  Google Scholar 

  • Löbel S, Snäll T, Rydin H (2006) Metapopulation processes in epiphytes inferred from patterns of regional distribution and local abundance in fragmented forest landscapes. J Ecol 94:856–868

    Article  Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Amer J Bot 82:1420–1425

    Article  Google Scholar 

  • Longton RE, Schuster RM (1983) Reproductive biology. In: Schuster RM (ed) New manual of bryology, vol 1. Hattori Botanical Laborarory, Nichinan, pp 386–462

    Google Scholar 

  • Miles CJ, Longton RE (1992) Deposition of moss spores in relation to distance from parent gametophytes. J Bryol 17:355–368

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Pohjamo M, Laaka-Lindberg S, Ovaskainen O, Korpelainen H (2006) Dispersal potential of spores and asexual gemmae in an epixylic hepatic Anastrophyllum hellerianum. Evol Ecol 20:415–430

    Article  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

    Article  Google Scholar 

  • Provan J, Wilson PJ (2007) Development of microsatellites for the peat moss Sphagnum capillifolium using ISSR cloning. Mol Ecol Notes 7:254–256

    Article  CAS  Google Scholar 

  • Roads E, Longton RE (2003) Reproductive biology and population studies in two annual shuttle mosses. J Hattori Bot Lab 93:305–318

    Google Scholar 

  • Rousset F (2001) Inferences from spatial population genetics. In: Balding DJ, Bishop M, Cannings C (eds) Handbook of statistical genetics. Wiley, Chichester, pp 239–269

    Google Scholar 

  • Rudolphi J (2009) Ant-mediated dispersal of asexual moss propagules. Bryologist 112:73–79

    Article  Google Scholar 

  • Snäll T, Ribeiro PJ Jr, Rydin H (2003) Spatial occurrence and colonizations in patch-tracking metapopulations of epiphytic bryophytes: local conditions versus dispersal. Oikos 103:566–578

    Article  Google Scholar 

  • Snäll T, Fogelqvist P, Ribeiro PJ Jr, Lascoux M (2004a) Spatial genetic structure in two congeneric epiphytes with different dispersal strategies analysed by three different methods. Mol Ecol 13:2109–2119

    Article  PubMed  Google Scholar 

  • Snäll T, Hagstrom A, Rudolphi J, Rydin H (2004b) Distribution pattern of the epiphyte Neckera pennata on three spatial scales–importance of past landscape structure, connectivity and local conditions. Ecography 27:757–766

    Article  Google Scholar 

  • Snäll T, Ehrlen J, Rydin H (2005) Colonization-extinction dynamics of an epiphyte metapopulation in a dynamic landscape. Ecology 86:106–115

    Article  Google Scholar 

  • Stackelberg M, von Rensing S, Reski R (2006) Identification of genic moss SSR markers and a comparative analysis of twenty-four algal and plant gene indices reveal species-specific rather than group-specific characteristics of microsatellites. BMC Plant Biol 6:9

    Article  Google Scholar 

  • Sundberg S (2005) Larger capsules enhance short-range dispersal in Sphagnum, but what happens further on? Oikos 108:115–124

    Article  Google Scholar 

  • Szövenyi P, Terracciano S, Ricca M, Giordano S, Shaw AJ (2008) Recent divergence, intercontinental dispersal and shared polymorphism are shaping the genetic structure of amphi- Atlantic peatmoss populations. Mol Ecol 17:5364–5377

    Article  PubMed  Google Scholar 

  • van der Velde M, van der Strate HJ, van de Zande L, Bijlsma R (2000) Isolation and characterization of microsatellites in the moss species Polytrichum formosum. Mol Ecol 9:1678–1680

    Article  PubMed  Google Scholar 

  • van der Velde M, During HJ, van de Zande L, Bijlsma R (2001) The reproductive biology of Polytrichum formosum: clonal structure and paternity revealed by microsatellites. Mol Ecol 10:2423–2434

    Article  PubMed  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935

    Article  CAS  PubMed  Google Scholar 

  • Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST doesn’t equal 1/(4Nm + 1). Heredity 82:117–125

    Article  PubMed  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    CAS  PubMed  Google Scholar 

  • Wyatt R (1985) Species concept in bryophytes: input from population biology. Bryologist 88:182–189

    Article  Google Scholar 

  • Yamagishi H, Tomimatsu H, Ohara M (2007) Fine-scale spatial genetic structure within continuous and fragmented populations of Trillium camschatcense. J Hered 98:367–372

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Hanna Forsman for help in the laboratory, and we acknowledge financial support from the Academy of Finland (project number 50525) and University of Helsinki Research Funds.

Author information

Authors and Affiliations

  1. Department of Agricultural Sciences, University of Helsinki, P.O. Box 27, 00014, Helsinki, Finland

    Helena Korpelainen & Maria von Cräutlein

  2. Lammi Biological Station, 16900, Lammi, Finland

    Sanna Laaka-Lindberg

  3. Department of Biology, University of Turku, 20014, Turku, Finland

    Sanna Huttunen

Authors
  1. Helena Korpelainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria von Cräutlein
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sanna Laaka-Lindberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sanna Huttunen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Helena Korpelainen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Korpelainen, H., von Cräutlein, M., Laaka-Lindberg, S. et al. Fine-scale spatial genetic structure of a liverwort (Barbilophozia attenuata) within a network of ant trails. Evol Ecol 25, 45–57 (2011). https://doi.org/10.1007/s10682-010-9378-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-010-9378-1

Keywords

Search

Navigation