Geographical range in liverworts: does sex really matter?
Corresponding Author
Benjamin Laenen
Department of Ecology, Environment, and Plant Sciences, Science for Life Laboratory, Stockholm University, 10691 Stockholm, Sweden
Department of Conservation Biology and Evolution, Institute of Botany, University of Liège, Liège, Belgium
Correspondence: Benjamin Laenen, Department of Ecology, Environment, and Plant Sciences, Science for Life Laboratory, Stockholm University, 10691 Stockholm, Sweden.
E-mail: [email protected]
Search for more papers by this authorAntonin Machac
Department of Ecology & Evolution, State University of New York, Stony Brook, NY, USA
Search for more papers by this authorS. Robbert Gradstein
Département de Systématique et Evolution, Museum National d'Histoire Naturelle, Paris, France
Search for more papers by this authorBlanka Shaw
Department of Biology, Duke University, Durham, NC, 27708 USA
Search for more papers by this authorJairo Patiño
Department of Conservation Biology and Evolution, Institute of Botany, University of Liège, Liège, Belgium
Search for more papers by this authorAurélie Désamoré
Department of Conservation Biology and Evolution, Institute of Botany, University of Liège, Liège, Belgium
Department of Zoology, Naturhistoriska riksmuseet, Stockholm, Sweden
Search for more papers by this authorBernard Goffinet
Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, 06269 USA
Search for more papers by this authorCymon J. Cox
Centro de Ciências do Mar (CCMAR), Universidade do Algarve, 8005-139 Faro, Portugal
Search for more papers by this authorJonathan Shaw
Department of Biology, Duke University, Durham, NC, 27708 USA
Contributed equally to this paper.Search for more papers by this authorAlain Vanderpoorten
Department of Conservation Biology and Evolution, Institute of Botany, University of Liège, Liège, Belgium
Contributed equally to this paper.Search for more papers by this authorCorresponding Author
Benjamin Laenen
Department of Ecology, Environment, and Plant Sciences, Science for Life Laboratory, Stockholm University, 10691 Stockholm, Sweden
Department of Conservation Biology and Evolution, Institute of Botany, University of Liège, Liège, Belgium
Correspondence: Benjamin Laenen, Department of Ecology, Environment, and Plant Sciences, Science for Life Laboratory, Stockholm University, 10691 Stockholm, Sweden.
E-mail: [email protected]
Search for more papers by this authorAntonin Machac
Department of Ecology & Evolution, State University of New York, Stony Brook, NY, USA
Search for more papers by this authorS. Robbert Gradstein
Département de Systématique et Evolution, Museum National d'Histoire Naturelle, Paris, France
Search for more papers by this authorBlanka Shaw
Department of Biology, Duke University, Durham, NC, 27708 USA
Search for more papers by this authorJairo Patiño
Department of Conservation Biology and Evolution, Institute of Botany, University of Liège, Liège, Belgium
Search for more papers by this authorAurélie Désamoré
Department of Conservation Biology and Evolution, Institute of Botany, University of Liège, Liège, Belgium
Department of Zoology, Naturhistoriska riksmuseet, Stockholm, Sweden
Search for more papers by this authorBernard Goffinet
Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, 06269 USA
Search for more papers by this authorCymon J. Cox
Centro de Ciências do Mar (CCMAR), Universidade do Algarve, 8005-139 Faro, Portugal
Search for more papers by this authorJonathan Shaw
Department of Biology, Duke University, Durham, NC, 27708 USA
Contributed equally to this paper.Search for more papers by this authorAlain Vanderpoorten
Department of Conservation Biology and Evolution, Institute of Botany, University of Liège, Liège, Belgium
Contributed equally to this paper.Search for more papers by this authorAbstract
Aim
Why some species exhibit larger geographical ranges than others remains a fundamental, but largely unanswered, question in ecology and biogeography. In plants, a relationship between range size and mating system was proposed over a century ago and subsequently formalized in Baker's Law. Here, we take advantage of the extensive variation in sexual systems of liverworts to test the hypothesis that dioecious species compensate for limited fertilization by producing vegetative propagules more commonly than monoecious species. As spores are assumed to contribute to random long-distance dispersal, whereas vegetative propagules contribute to colony maintenance and frequent short-distance dispersal, we further test the hypothesis that monoecious species exhibit larger geographical ranges than dioecious ones.
Location
Worldwide.
Methods
We used comparative phylogenetic methods to assess the correlation between range size and life history traits related to dispersal, including mating systems, spore size and production of specialized vegetative propagules.
Results
No significant correlation was found between dioecy and production of vegetative propagules. However, production of vegetative propagules is correlated with the size of geographical ranges across the liverwort tree of life, whereas sexuality and spores size are not. Moreover, variation in sexual systems did not have an influence on the correlation between geographical range and production of asexual propagules.
Main conclusions
Our results challenge the long-held notion that spores, and not vegetative propagules, are involved in long-distance dispersal. Asexual reproduction seems to play a major role in shaping the global distribution patterns of liverworts, so that monoecious species do not tend to display, on average, broader distribution ranges than dioecious ones. Our results call for further investigation on the spatial genetic structure of bryophyte populations at different geographical scales depending on their mating systems to assess the dispersal capacities of spores and asexual propagules and determine their contribution in shaping species distribution ranges.
Supporting Information
| Filename | Description |
|---|---|
| jbi12661-sup-0001-AppendixS1.xlsxMS Excel, 8.9 MB | Appendix S1 Liverwort life history traits. |
| jbi12661-sup-0002-AppendixS2.docxWord document, 52.6 KB | Appendix S2 References of appendix S1. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Algar-Hedderson, N., Söderström, L. & Hedderson, T.A.J. (2013) Gemmae output in the liverwort Lophozia ventricosa (Dicks.) Dumort: spatial variation, density dependence, and relationships among production components. Journal of Bryology, 35, 173–179.
- Baker, H.G. (1955) Self-compatibility and establishment after ‘long distance’ dispersal. Evolution, 9, 347–348.
- Baker, H.G. (1967) Support for Baker's law as a rule. Evolution, 21, 853–856.
- Bisang, I. & Ehrlen, J. (2002) Reproductive effort and cost of reproduction in female Dicranum polysetum. Bryologist, 105, 384–397.
- Bisang, I., Ehrlén, J., Persson, C. & Hedenäs, L. (2014) Family affiliation, sex ratio and sporophyte frequency in unisexual mosses. Botanical Journal of the Linnean Society, 174, 163–172.
- Cheptou, P.O. (2012) Clarifying Baker's Law. Annals of Botany, 109, 633–641.
- Crawford, M., Jesson, L.K. & Garnock-Jones, P.J. (2009) Correlated evolution of sexual system and life history traits in mosses. Evolution, 63, 1129–1142.
- Cronberg, N., Natcheva, R. & Hedlund, K. (2006) Microarthropods mediate sperm transfer in mosses. Science, 313, 1255.
- De Waal, C., Rodger, J.G., Anderson, B. & Ellis, A.G. (2014) Selfing ability and dispersal are positively related, but not affected by range position: a multispecies study on southern African Asteraceae. Journal of Evolutionary Biology, 27, 950–959.
- Duckett, J. G. & Ligrone, R. (1992) A survey of liberation mechanisms and germination patterns in mosses. Journal of Bryology, 17, 335–354.
- During, H.J. (2007) Relations between clonal growth, reproduction and breeding system in the bryophytes of Belgium and The Netherlands. Nova Hedwigia Supplement, 131, 133–145.
- Eppley, S.M., Taylor, P.J. & Jesson, L.K. (2007) Self-fertilization in mosses: a comparison of heterozygote deficiency between species with combined versus separate sexes. Heredity, 98, 38–44.
- Freckleton, R.P., Harvey, P.H. & Pagel, M. (2002) Phylogenetic analysis and comparative data: a test and review of evidence. The American Naturalist, 160, 712–726.
- Gradstein, S.R. (2006) The lowland cloud forest of French Guiana: a liverwort hotspot. Cryptogamie Bryologie, 27, 141–152.
- Henslow, G. (1879) On the self-fertilization of plants. Transactions of the Linnean Society London, 1, 317–398.
10.1111/j.1095-8339.1879.tb00139.x 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. Journal of Bryology, 36(3), 244–248.
- Hutsemekers, V., Hardy, O.J. & Vanderpoorten, A. (2013) Does water facilitate gene flow in spore-producing plants? Insights from the fine-scale genetic structure of the aquatic moss Rhynchostegium riparioides. Aquatic Botany, 108, 1–6.
- Johnson, M.G. & Shaw, A.J. (2015) Genetic diversity, sexual condition, and microhabitat preference determine mating patterns in Sphagnum (Sphagnaceae) peat-mosses. Biological Journal of the Linnean Society, 115, 96–113.
- Johnson, M.T.J., De Witt Smith, S. & Rausher, M.D. (2010) Effects of plant sex on range distributions and allocation to reproduction. New Phytologist, 186, 769–779.
- Karlin, E.F., Andrus, R.E., Boles, S.B. & Shaw, A.J. (2011) One haploid parent contributes 100% of the gene pool for a widespread species in northwest North America. Molecular Ecology, 20, 753–767.
- Kimmerer, R.W. (1991) Reproductive ecology of Tetraphis pellucida: differential fitness of sexual and asexual propagules. The Bryologist, 94, 284–288.
- Kimmerer, R.W. (1994) Ecological consequences of sexual vs. asexual reproduction in Dicranum flagellare. The Bryologist, 97, 20–25.
- Klips, R.A. (2015) DNA microsatellite analysis of sporophytes of the short-lived arable moss Physcomitrium pyriforme reveals a predominantly self-fertilizing mating pattern. The Bryologist, 118(2), 200–211.
- Laaka-Lindberg, S. (2005) Reproductive phenology of the leafy hepatic Lophozia silvicola Buch in southern Finland. Journal of Bryology, 27, 253–259.
- Laaka-Lindberg, S., Hedderson, T.A.J. & Longton, R.E. (2000) Rarity and reproductive characters in the British hepatic flora. Lindbergia, 25, 78–84.
- Laenen, B., Shaw, B., Schneider, H. et al. (2014) Extant diversity of bryophytes emerged from successive post-Mesozoic diversification bursts. Nature Communications, 5, e5134.
- Lambert, S.M. & Wiens, J.J. (2013) Evolution of viviparity: a phylogenetic test of the cold-climate hypothesis in Phrynosomatid lizards. Evolution, 67, 2614–2630.
- Laube, I., Graham, C.H. & Böhning-Gaese, K. (2013a) Intra-generic species richness and dispersal ability interact to determine geographic ranges of birds. Global Ecology and Biogeography, 22, 223–232.
- Laube, I., Korntheuer, H., Schwager, M., Trautmann, S., Rahbek, C. & Böhning-Gaese, K. (2013b) Towards a more mechanistic understanding of traits and range sizes. Global Ecology and Biogeography, 22, 233–241.
- Lester, S.E., Ruttenberg, B.I., Gaines, S.D. & Kinlan, B.P. (2007) The relationship between dispersal ability and geographic range size. Ecology Letters, 10, 745–758.
- Lewis, L.R., Behling, E., Gousse, H., Qian, E., Elphick, C.S., Lamarre, J., Bêty, J., Liebezeit, J., Rozzi, R. & Goffinet, B. (2014) First evidence of bryophyte diaspores in the plumage of transequatorial migrant birds. PeerJ, 2, e424.
- Löbel, S. & Rydin, H. (2010) Trade-offs and habitat constraints in the establishment of epiphytic bryophytes. Functional Ecology, 24, 887–897.
- Löbel, S., Snäll, T. & Rydin, H. (2009) Mating system, reproduction mode and diaspore size affect metacommunity diversity. Journal of Ecology, 97, 176–185.
- Longton, R.E. (1992) Reproduction and rarity in British mosses. Biological Conservation, 59, 89–98.
- Longton, R.E. (1997) Reproductive biology and life-history strategies. Advances in Bryology, 6, 65–101.
- Longton, R.E. & Schuster, R.M. (1983) Reproductive biology. New manual of bryology, Vol. 1 (ed. by R.M. Schuster), pp 386–462. Hattori Botanical Laboratory, Nichinan.
- Lowry, E. & Lester, S.E. (2006) The biogeography of plant reproduction: potential determinants of species' range sizes. Journal of Biogeography, 33, 1975–1982.
- Maddison, W.P. & Fitzjohn, R.G. (2015) The unsolved challenge to phylogenetic correlation tests for categorical characters. Systematic Biology, 64(1), 127–136.
- McDaniel, S.F., Atwood, J. & Burleigh, J.G. (2013) Recurrent evolution of dioecy in bryophytes. Evolution, 67, 567–572.
- Mishler, B.D. & Newton, A.E. (1988) Influences of mature plants and desiccation on germination of spores and gametophytic fragments of Tortula. Journal of Bryology, 15, 327–342.
- Mota de Oliveira, S.M. & ter Steege, H. (2015) Bryophyte communities in the Amazon forest are regulated by height on the host tree and site elevation. Journal of Ecology, 103, 441–450.
- Muñoz, J., Felicisimo, A.M., Cabezas, F., Burgaz, A.R. & Martinez, I. (2004) Wind as a long-distance dispersal vehicle in the southern hemisphere.SH. Science, 304, 1144–1147.
- Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N. & Pearse, W. (2013) caper: Comparative Analyses of Phylogenetics and Evolution in R. R package version 0.5.2. http://CRAN.R-project.org/package=caper .
- Pagel, M. (1994) Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society B: Biological Sciences, 255, 37–45.
- Pannell, J.R. (2015) Evolution of the mating system in colonizing plants. Molecular Ecology, 24, 2018–2037.
- Patiño, J., Bisang, I., Hedenäs, L., Dirkse, G., Bjarnason, A.H., Ah-Peng, C. & Vanderpoorten, A. (2013) Baker's law and the island syndromes in bryophytes. Journal of Ecology, 101, 1245–1255.
- Pohjamo, M. & Laaka-Lindberg, S. (2003) Reproductive modes in a leafy hepatic Anastrophyllum hellerianum. Perspectives in Plant Ecology, Evolution and Systematics, 6, 159–168.
- Pohjamo, M., Laaka-Lindberg, S., Ovaskainen, O. & Korpelainen, H. (2006) Dispersal potential of spores and asexual propagules in the epixylic hepatic Anastrophyllum hellerianum. Evolutionary Ecology, 20, 415–430.
- Randle, A.M., Slyder, J.B. & Kalisz, S. (2009) Can differences in autonomous selfing ability explain differences in range size among sister-taxa pairs of Collinsia (Plantaginaceae)? An extension of Baker's law. New Phytologist, 183, 618–629.
- R Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
- Rosengren, F. & Cronberg, N. (2014) The adaptive background of nannandry: dwarf male distribution and fertilization in the moss Homalothecium lutescens. Biological Journal of the Linnean Society, 113, 74–84.
- Rydgren, K. & Okland, R. (2003) Short-term costs of sexual reproduction in the clonal moss Hylocomium splendens. Bryologist, 106, 212–220.
- Sanmartín, I. & Ronquist, F. (2004) Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns. Systematic Biology, 53, 216–243.
- Sanmartín, I., Wanntorp, L. & Winkworth, R.C. (2007) West Wind Drift revisited: testing for directional dispersal in the Southern Hemisphere using eventbased-tree fitting. Journal of Biogeography, 34, 398–416.
- Schuster, R.M. & Longton, R.E. (1983) Reproductive biology. New manual of bryology, 1, 386–462.
- Shortlidge, E.E., Rosenstiel, T.N. & Eppley, S.M. (2012) Tolerance to environmental desiccation in moss sperm. New Phytologist, 194, 741–750.
- Slatyer, R.A., Hirst, M. & Sexton, J.P. (2013) Niche breadth predicts geographical range size: a general ecological pattern. Ecology Letters, 16, 1104–1114.
- Snäll, T., Fogelqvist, J., Ribeiro, P.J. & Lascoux, M. (2004) Spatial genetic structure in two congeneric epiphytes with different dispersal strategies analysed by three different methods. Molecular Ecology, 13, 2109–2119.
- Söderström, L. & During, H.J. (2005) Bryophyte rarity viewed from the perspectives of life history strategy and metapopulation dynamics. Journal of Bryology, 27, 261–268.
- Stark, L.R. & McLetchie, D.N. (2006) Gender-specific heat-shock tolerance of hydrated leaves in the desert moss Syntrichia caninervis. Physiologia Plantarum, 126, 187–195.
- Stark, L.R., Brinda, J.C. & McLetchie, D.N. (2009) An experimental demonstration of the cost of sex and a potential resource limitation on reproduction in the moss Pterygoneurum (Pottiaceae). American Journal of Botany, 96, 1712–1721.
- Stebbins, G.L. (1950) Variation and evolution in plants. Columbia University Press, New York.
10.7312/steb94536 Google Scholar
- Stieha, C.R., Middleton, A.R., Stieha, J.K., Trott, S.H. & Mcletchie, D.N. (2014) The dispersal process of asexual propagules and the contribution to population persistence in Marchantia (Marchantiaceae). American Journal of Botany, 101, 348–356.
- Symonds, M.R.E. & Blomberg, S.P. (2014) A primer on phylogenetic generalised least squares. Modern phylogenetic comparative methods and their application in evolutionary biology (ed. by L.Z. Garamszegi), pp. 105–130. Springer-Verlag, Berlin Heidelberg.
10.1007/978-3-662-43550-2_5 Google Scholar
- Tan, B. C. & Pocs, T. (2000). Bryogeography and conservation of bryophytes. Bryophyte biology (ed. by A. J. Shaw and B. Goffinet), pp. 403–448. Cambridge University Press, Cambridge.
10.1017/CBO9781139171304.014 Google Scholar
- Taylor, P.J., Eppley, S.M. & Jesson, L.K. (2007) Sporophytic inbreeding depression in mosses occurs in a species with separate sexes but not in a species with combined sexes. American Journal of Botany, 94, 1853–1859.
- Vamosi, M. & Vamosi, J.C. (2012) Causes and consequences of range size variation: the influence of traits, speciation, and extinction. Frontiers in Biogeography, 4, 168–177.
10.21425/F54413024 Google Scholar
- Van der Wijk, R., Margadant, W.D. & Florschütz, P.A. (1959) Index Muscorum. International Association of Plant Taxonomists, Utrecht.
- Van Zanten, B.O. & Gradstein, S.R. (1988) Experimental dispersal geography of neotropical liverworts. Nova Hedwigia Beihefte, 90, 41–94.
- Vanderpoorten, A., Gradstein, S.R., Carine, M.A. & Devos, N. (2010) The ghosts of Gondwana and Laurasia in modern liverwort distributions. Biological Reviews, 85, 471–487.
- Villarreal, J.C. & Renner, S.S. (2013) Correlates of monoicy and dioicy in hornworts, the apparent sister group to vascular plants. BMC Evolutionary Biology, 13, e329.
- Wiens, J.J. (1998) The accuracy of methods for coding and sampling higher-level taxa for phylogenetic analysis: a simulation study. Systematic Biology, 47, 397–413.
- Wilkinson, D.M., Koumoutsaris, S., Mitchell, E.A.D. & Bey, I. (2012) Modelling the effect of size on the aerial dispersal of microorganisms. Journal of Biogeography, 39, 89–97.
- Wright, S. (1934) An analysis of variability in the number of digits in an inbred strain of guinea pigs. Genetics, 19, 506–536.
- van Zanten, B.O. (1976) Preliminary report on germination experiments designed to estimate the survival chances of moss spores during aerial trans-oceanic long-range dispersal in the southern hemisphere, with particular reference to New Zealand. Journal of the Hattori Botanical Laboratory, 41, 133–140.
- van Zanten, B.O. (1978) Experimental studies on trans-oceanic long-range dispersal of moss spores in the southern hemisphere. Journal of the Hattori Botanical Laboratory, 44, 455–482.
