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Type: Article
Published: 2021-06-30
Page range: 150–163
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Karyotypic diversity and cryptic speciation: Have we vastly underestimated moss species diversity?

Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Rd. Storrs, CT, 06269
Biodiversidad, Ecología y Evolución, Universidad Complutense de Madrid, C/ José Antonio Novais, 12, 28040 Madrid, Spain
Department of Biological Sciences, Texas Tech University 2901 Main Street, Lubbock TX 79404
Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Rd. Storrs, CT, 06269
Bryophyta polyploidy autopolyploidy diversity taxonomy

Abstract

Karyotypic diversity is critical to catalyzing change in the evolution of all plants. By resulting in meiotic incompatibility among sets of homologous chromosomes, polyploidy and aneuploidy may facilitate reproductive isolation and the potential for speciation. Across plants, karyotypic variants in the form of allopolyploids receive greater taxonomic attention relative to autopolyploids and aneuploids. In particular, the prevalence and significance of autopolyploidy and aneuploidy in bryophytes is little understood. Using Fritsch’s 1991 compendium of bryophyte karyotypes with augmentation from karyological studies published since, we have quantified the prevalence of karyotypic variants among ~1500 extant morphological species of mosses. We assessed the phylogenetic distribution of karyological data, the frequency of autopolyploidy and aneuploidy, and the methodological correlates with karyotypic diversity. At least two ploidy levels were recorded from 17% of species potentially increasing current taxonomic diversity of mosses to over 15,000 species. We find that for a given species, the number of unique karyotypes recorded is correlated with the number of populations sampled. The evidence suggests that cytological diversity likely underlies yet undescribed species diversity in mosses, and that intensive karyological sampling is a needed tool for its discovery.

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References

  1. Anderson, L.E. (1974) Bryology 1947–1972. Annals of the Missouri Botanical Garden 61: 56–85.   https://doi.org/10.2307/2395185
    Barker, M.S., Arrigo, N., Baniaga, A.E., Li, Z. & Levin, D.A. (2016) On the relative abundance of autopolyploids and allopolyploids. New Phytologist 210: 391–398.  https://doi.org/10.1111/nph.13698
    Beck, J.B., Windham, M.D., Yatskievych, G. & Pryer, K.M. (2010) A diploids-first approach to species delimitation and interpreting polyploid evolution in the fern genus Astrolepis (Pteridaceae). Systematic Botany 35: 223–234.  https://doi.org/10.1600/036364410791638388
    Beike, A.K., von Stackelberg, M., Schallenberg-Rüdinger, M., Hanke, S.T., Follo, M., Quandt, D., McDaniel, S., Reski, R., Tan, B. & Rensing, S.A. (2014) Molecular evidence for convergent evolution and allopolyploid speciation within the Physcomitrium-Physcomitrella species complex. BMC Evolutionary Biology 14: 158.  https://doi.org/10.1186/1471-2148-14-158
    Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22: 148–155.   https://doi.org/10.1016/j.tree.2006.11.004
    Brochmann, C., Brysting, A.K., Alsos, I.G., Borgen, L., Grundt, H.H., Scheen, A.C. & Elven, R. (2004) Polyploidy in arctic plants. Biological Journal of the Linnaean Society 82: 521–536. https://doi.org/10.1111/j.1095-8312.2004.00337.x
    Comai, L. (2005) The advantages and disadvantages of being polyploid. Nature Reviews Genetics 6: 836–846.   https://doi.org/10.1038/nrg1711
    Costich, D.E., Friebe, B., Sheehan, M.J., Casler, M.D. & Buckler, E.S. (2010) Genome‐size variation in switchgrass (Panicum virgatum): flow cytometry and cytology reveal rampant aneuploidy. The Plant Genome 3: 130–141.  https://doi.org/10.3835/plantgenome2010.04.0010
    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.   https://doi.org/10.1111/j.1558-5646.2009.00615.x
    Cui, L., Wall, P.K., Leebens‐Mack, J.H., Lindsay, B.G., Soltis, D.E., Doyle, J.J., Soltis, P.S., Carlson, J.E., Arumuganathan, K., Barakat, A., Albert, V.A., Ma, H. & dePamphilis, C.W. (2006) Widespread genome duplications throughout the history of flowering plants. Genome Research 16: 738–749. https://doi.org/10.1101/gr.4825606
    Derda, G.S. & Wyatt, R. (2000) Isozyme evidence regarding the origins of three allopolyploid species of Polytrichastrum (Polytrichaceae, Bryophyta). Plant Systematics and Evolution 22: 37–53.  https://doi.org/10.1007/BF00985369
    Doyle, G.G. (1986) Aneuploidy and inbreeding depression in random mating and self-fertilizing autotetraploid populations. Theoretical and Applied Genetics 72: 799–806.   https://doi.org/10.1007/BF00266548
    Doyle, J.J. & Coate, J.E. (2019) Polyploidy, the nucleotype, and novelty: the impact of genome doubling on the biology of the cell. International Journal of Plant Sciences 180: 1–52. https://doi.org/10.1086/700636
    Eriksson, J.S., Blanco-Pastor, J.L., Sousa, F., Bertrand, Y.J.K. & Pfeil, B.E. (2017) A cryptic species produced by autopolyploidy and subsequent introgression involving Medicago prostrata (Fabaceae). Molecular Phylogenetics and Evolution 107: 367–381.   https://doi.org/10.1016/j.ympev.2016.11.020
    Flatberg, K.I., Thingsgaard, K. & Såstad, S.M. (2006) Interploidal gene flow and introgression in bryophytes: Sphagnum girgensohnii× S. russowii, a case of spontaneous neotriploidy. Journal of bryology 28: 27–37. https://doi.org/10.1179/174328206X90459
    Fritsch, R. (1991) Index to bryophyte chromosome counts. Bryophytorum Bibliotheca 40: 1–352. 
    Gao, B., Chen, M.X., Li, X.S., Liang, Y.Q., Zhang, D.Y., Wood, A.J., Oliver, M.J. & Zhang, J.H. (2020) Integrated phylogenomic analyses reveal recurrent ancestral large-scale duplication events in mosses. Journal of Systematics and Evolution.  https://doi.org/10.1101/603191
    Goffinet, B. (2009) Morphology, anatomy, and classification of the Bryophyta. In: Goffinet, B. & Shaw, J. (Eds.) Bryophyte Biology. Cambridge University Press, London, pp.55–138.  
    Grusz, A.L. (2016) A current perspective on apomixis in ferns. Journal of Systematics and Evolution 54: 656–665. https://doi.org/10.1111/jse.12228
    Hanusch, M., Ortiz, E.M., Patiño, J. & Schaefer, H. (2020) Biogeography and integrative taxonomy of Epipterygium (Mniaceae, Bryophyta). Taxon 69: 1150–1171.   https://doi.org/10.1002/tax.12324
    Hedenäs, L. (2020) Cryptic speciation revealed in Scandinavian Racomitrium lanuginosum (Hedw.) Brid.(Grimmiaceae). Journal of Bryology 42: 117–127. https://doi.org/10.1080/03736687.2020.1722923
    Heinrichs, J., Hentschel, J., Feldberg, K., Bombosch, A. & Schneider, H. (2009) Phylogenetic biogeography and taxonomy of disjunctly distributed bryophytes. Journal of Systematics and Evolution 47: 497–508.   https://doi.org/10.1111/j.1759-6831.2009.00028.x
    Henry, I.M., Dilkes, B.P., Miller, E.S., Burkart-Waco, D. & Comai, L. (2010) Phenotypic consequences of aneuploidy in Arabidopsis thaliana. Genetics 186: 1231–1245. https://doi.org/10.1534/genetics.110.121079

  2. Husband, B.C. (2004) The role of triploid hybrids in the evolutionary dynamics of mixed-ploidy populations. Biological Journal of the Linnean Society 82: 537–546.  https://doi.org/10.1111/j.1095-8312.2004.00339.x
    Husband, B.C., Baldwin, S.J. & Suda, J. (2013) The incidence of polyploidy in natural plant populations: major patterns and evolutionary processes. In: Leitch, I., Greilhuber, J., Dolezel, J. & Wendel, J. (Eds.) Plant Genome Diversity. volume 2. Springer, Vienna, pp. 255–276.  https://doi.org/10.1007/978-3-7091-1160-4_16
    Husband, B.C. & Sabara, H.A. (2004) Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium (Onagraceae). New Phytologist 161: 703–713.   https://doi.org/10.1046/j.1469-8137.2004.00998.x
    Jauhar, P.P. (2003) Formation of 2n gametes in durum wheat haploids: sexual polyploidization. Euphytica 133: 81–94.   https://doi.org/10.1023/A:1025692422665
    Jesson, L.K., Cavanagh, A.P. & Perley, D.S. (2011) Polyploidy influences sexual system and mating patterns in the moss Atrichum undulatum sensu lato. Annals of Botany 107: 135–143.   https://doi.org/10.1093/aob/mcq216
    Jiao, Y., Wickett, N.J., Ayyampalayam, S., Chanderbali, A.S., Landherr, L., Ralph, P.E., Tomsho, L.P., Hu, Y., Liang, H., Soltis, P.S., Soltis, D.E., Clifton, S.W., Schlarbaum, S.E., Schuster, S.C., Ma, H., Leebens-Mack, J. & de Pamphilis, C.W. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97–100.  https://doi.org/10.1038/nature09916
    Karlin, E.F., Boles, S.B., Ricca, M., Temsch, E.M., Greilhuber, J. & Shaw, A.J. (2009) Three‐genome mosses: complex double allopolyploid origins for triploid gametophytes in Sphagnum. Molecular Ecology 18: 1439–1454.  https://doi.org/10.1111/j.1365-294X.2009.04113.x
    Karlin, E.F. & Robinson, S.C. (2017) Update on the Holantarctic Sphagnum× falcatulum sl (Sphagnaceae) complex: S. irritans is associated with the allo-diploid plants. Journal of Bryology 39: 8–15.  https://doi.org/10.1080/03736687.2016.1218674
    Köhler, C., Scheid, O.M. & Erilova, A. (2010) The impact of the triploid block on the origin and evolution of polyploid plants. Trends in Genetics 26: 142–148.   https://doi.org/10.1016/j.tig.2009.12.006
    Košnar, J., Herbstová, M., Kolář, F., Koutecký, P. & Kučera, J. (2012) A case study of intragenomic ITS variation in bryophytes: assessment of gene flow and role of polyploidy in the origin of European taxa of the Tortula muralis (Musci: Pottiaceae) complex. Taxon 61: 709–720.  https://doi.org/10.1002/tax.614001
    Kumar, P.K. & Chopra, R.N. (1980) Occurrence of apogamy and apospory from the capsules of Funaria hygrometrica Hedw. Cryptogamie, Bryologie, et Lichénologie 2: 197–200. 
    Kuta, E. & Przywara, L. (1997) Polyploidy in mosses. Acta Biologica Cracoviensia. Series Botanica 39: 17–26.
    Lazarenko, A.S. (1967) Polyploidy in the evolution of Musci. Tsitologiya i Genetika 1: 15–26. 
    Levin, D.A. (1975) Minority cytotype exclusion in local plant populations. Taxon 24: 35–43.   https://doi.org/10.2307/1218997
    Levin, D.A. (2002) The role of chromosomal change in plant evolution. Oxford University Press, London.
    Lewis, W.H. (1980) Polyploidy in species populations. Basic Life Sciences. Springer, Boston, pp. 103–144.  https://doi.org/10.1007/978-1-4613-3069-1_6
    Lobachevska, O., Kyjak, N., Khorkavtsiv, O., Dovgalyuk, A., Kit, N., Klyuchivska, O., Stoikab, R., Ripetskya, R. & Cove, D. (2005) Influence of metabolic stress on the inheritance of cell determination in the moss, Pottia intermedia. Cell Biology International 29: 181–186.  https://doi.org/10.1016/j.cellbi.2005.02.001
    Luceño, M. & Castroviejo, S. (1991) Agmatoploidy in Carex laevigata (Cyperaceae). Fusion and fission of chromosomes as the mechanism of cytogenetic evolution in Iberian populations. Plant Systematics and Evolution 177: 149–159.  https://doi.org/10.1007/BF00937952
    Magill, R.E. (2010) Moss diversity: new look at old numbers. Phytotaxa 9: 167–174.  https://doi.org/10.11646/phytotaxa.9.1.9
    Mandáková, T. & Lysak, M.A. (2018) Post-polyploid diploidization and diversification through dysploid changes. Current Opinion in Plant Biology 42: 55–65. https://doi.org/10.1016/j.pbi.2018.03.001

  3. Marks, G.E. (1966) The origin and significance of intraspecific polyploidy: experimental evidence from Solanum chacoense. Evolution 20: 552–557.   https://doi.org/10.1111/j.1558-5646.1966.tb03385.x
    McDaniel, S.F., Von Stackelberg, M., Richardt, S., Quatrano, R.S., Reski, R. & Rensing, S.A. (2010) The speciation history of the Physcomitrium—Physcomitrella species complex. Evolution 64: 217–231.  https://doi.org/10.1111/j.1558-5646.2009.00797.x
    Medina, R., Johnson, M.G., Liu, Y., Wickett, N.J., Shaw, A.J. & Goffinet, B. (2019) Phylogenomic delineation of Physcomitrium (Bryophyta: Funariaceae) based on targeted sequencing of nuclear exons and their flanking regions rejects the retention of Physcomitrella, Physcomitrium and Aphanorrhegma. Journal of Systematics and Evolution 57: 404–417.  https://doi.org/10.1111/jse.12516
    Mishra, M.K. (1997) Stomatal characteristics at different ploidy levels in Coffea L. Annals of Botany 80: 689–692.  https://doi.org/10.1006/anbo.1997.0491
    Natcheva, R. & Cronberg, N. (2004) What do we know about hybridization among bryophytes in nature? Canadian Journal of Botany 82: 1687–1704. https://doi.org/10.1139/b04-139
    Newton, M.E. (1973) Chromosome studies in some New Zealand and Jamaican bryophytes. Journal of Bryology 7: 399–403.  https://doi.org/10.1179/jbr.1973.7.3.399
    Newton, M.E. (1975) Chromosome studies in some British bryophytes. Journal of Bryology 8: 365–382.  https://doi.org/10.1179/jbr.1975.8.3.365
    Newton, M.E. (1984) Cytogenetics of bryophytes. In: Dyer, A. & Duckett, J. (Eds.) Experimental Biology of Bryophytes. Academic Press, London, pp. 65–96. 
    Nieto‐Lugilde, M., Werner, O., McDaniel, S.F., Koutecký, P., Kučera, J., Rizk, S.M. & Ros, R.M. (2018) Peripatric speciation associated with genome expansion and female‐biased sex ratios in the moss genus Ceratodon. American Journal of Botany 105: 1009–1020.  https://doi.org/10.1002/ajb2.1107
    Oswald, B.P. & Nuismer, S.L. (2011) A unified model of autopolyploid establishment and evolution. The American Naturalist 178: 687–700.  https://doi.org/10.1086/662673
    Otto, S.P. & Whitton, J. (2000) Polyploid incidence and evolution. Annual Review of Genetics 34: 401–437.  https://doi.org/10.1146/annurev.genet.34.1.401
    Parisod, C., Holderegger, R. & Brochmann, C. (2010) Evolutionary consequences of autopolyploidy. New Phytologist 186: 5–17.  https://doi.org/10.1111/j.1469-8137.2009.03142.x
    Patel, N., Li, C.X., Zhang, L.B. & Barrington, D.S. (2018) Biodiversity and apomixis: Insights from the East-Asian holly ferns in Polystichum section Xiphopolystichum. Molecular Phylogenetics and Evolution 127: 345–355. https://doi.org/10.1016/j.ympev.2018.05.003
    Pavlíková, Z., Paštová, L. & Münzbergová, Z. (2017) Synthetic polyploids in Vicia cracca: methodology, effects on plant performance and aneuploidy. Plant Systematics and Evolution 303: 827–839.  https://doi.org/10.1007/s00606-017-1414-y
    Ramsay, H.P. (1983) Cytology of mosses. In: Schuster, R. (Ed.) New manual of bryology vol 1. Hattori Botanical Society, pp. 149–221. 
    Ramsey, J. & Schemske, D.W. (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics 29: 467–501.  https://doi.org/10.1146/annurev.ecolsys.29.1.467
    Ramsey, J. & Schemske, D.W. (2002) Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33: 589–639.
    Randolph, L.F. (1935) Cytogenetics of tetraploid maize. Journal of Agricultural Research 50: 591–605. 
    Rensing, S.A., Beike, A.K. & Lang, D. (2013) Evolutionary importance of generative polyploidy for genome evolution of haploid-dominant land plants. In: Leitch, I., Greilhuber, J., Dolezel, J. & Wendel, J. (Eds.) Plant Genome Diversity Volume 2. Springer, Vienna, pp. 295–305.  https://doi.org/10.1007/978-3-7091-1160-4_18
    Ricca, M. & Shaw, A.J. (2010) Allopolyploidy and homoploid hybridization in the Sphagnum subsecundum complex (Sphagnaceae: Bryophyta). Biological Journal of the Linnean Society 99: 135–151.  https://doi.org/10.1111/j.1095-8312.2009.01340.x
    Rice, A., Šmarda, P., Novosolov, M., Drori, M., Glick, L., Sabath, N., Sahi, M., Belmaker, J. & Mayrose, I. (2019) The global biogeography of polyploid plants. Nature Ecology & Evolution 3: 265–273. https://doi.org/10.1038/s41559-018-0787-9

  4. Robinson, D.O., Coate, J.E., Singh, A., Hong, L., Bush, M., Doyle, J.J. & Roeder, A.H. (2018) Ploidy and size at multiple scales in the Arabidopsis sepal. The Plant Cell 30: 2308–2329.  https://doi.org/10.1105/tpc.18.00344
    Schemske, D.W. (2000) Understanding the origin of species. Evolution 54: 1069–1073. https://doi.org/10.1111/j.0014-3820.2000.tb00111.x
    Schinkel, C.C., Kirchheimer, B., Dullinger, S., Geelen, D., De Storme, N. & Hörandl, E. (2017) Pathways to polyploidy: indications of a female triploid bridge in the alpine species Ranunculus kuepferi (Ranunculaceae). Plant Systematics and Evolution 303: 1093–1108.  https://doi.org/10.1007/s00606-017-1435-6
    Shaw, A.J. (2009) Bryophyte species and speciation. In: Goffinet, B., Shaw, J. (eds.) Bryophyte biology, Cambridge University Press, London, pp.55–138.  
    Smith, A.J.E. (1978) Cytogenetics, biosystematics and evolution in the Bryophyta. In: Advances in botanical research. Academic Press, Cambridge, pp. 195–276.  https://doi.org/10.1016/S0065-2296(08)60331-6
    Soltis, D.E., Soltis, P.S., Schemske, D.W., Hancock, J.F., Thompson, J.N., Husband, B.C. & Judd, W.S. (2007) Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56: 13–30. 
    Soltis, D.E., Visger, C.J. & Soltis, P.S. (2014) The polyploidy revolution then and now: Stebbins revisited. American Journal of Botany 101: 1057–1078.  https://doi.org/10.3732/ajb.1400178
    Spoelhof, J.P., Soltis, P.S. & Soltis, D.E. (2017) Pure polyploidy: closing the gaps in autopolyploid research. Journal of Systematics and Evolution 55: 340–352.  https://doi.org/10.1111/jse.12253
    Stebbins Jr., G.L. (1947) Types of polyploids: their classification and significance. In: Demerec, M. (Ed.) Advances in genetics. Academic Press, Cambridge, pp. 403–429.  https://doi.org/10.1016/S0065-2660(08)60490-3
    Stebbins, G.L. (1950) Variation and Evolution in Plants. Columbia University Press, New York, 623 pp. https://doi.org/10.7312/steb94536
    Svačina, R., Sourdille, P., Kopecký, D., & Bartoš, J. (2020) Chromosome pairing in polyploid grasses. Frontiers in Plant Science 11: 1056.    https://doi.org/10.3389/fpls.2020.01056
    Tate, J.A., Soltis, D.E. & Soltis, P.S. (2005) Polyploidy in plants. In: Gregory, T. (Ed.) The Evolution of the Genome. Academic Press, Cambridge, pp. 371–426.  https://doi.org/10.1016/B978-012301463-4/50009-7
    Vaarama, A. (1976) The cytotaxonomic approach to the study of bryophytes. Journal of Hattori Botanical Laboratory 41: 7–12. 
    Vickery, R.K. (1995) Speciation by aneuploidy and polyploidy in Mimulus (Scrophulariaceae). The Great Basin Naturalist 55: 174–176. 
    Vitt, D.H. (1971) The infrageneric evolution, phylogeny, and taxonomy of the genus Orthotrichum (Musci) in North America. Nova Hedwigia 21: 683–711. 
    Wettstein, F.V. (1924) Morphologie und Physiologie des Formwechsels der Moose auf genetischer Grundlage. I. Zeitschrift für induktive Abstammungs-und Vererbungslehre 33: 1–236. https://doi.org/10.1007/BF01762372
    Wood, T.E., Takebayashi, N., Barker, M.S., Mayrose, I., Greenspoon, P.B. & Rieseberg, L.H. (2009) The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences 106 (33): 13875–13879.  https://doi.org/10.1073/pnas.0811575106
    Wyatt, R., Odrzykoski, I.J. & Stoneburner, A. (2013) Isozyme evidence regarding the nature of  polyploidy in the moss genus Cinclidiu (Mniaceae). The Bryologist 116: 229–237.  https://doi.org/10.1639/0007-2745-116.3.229
    Wyatt, R., Odrzykoski, I.J., Stoneburner, A., Bass, H.W. & Galau, G.A. (1988) Allopolyploidy in bryophytes: multiple origins of Plagiomnium medium. Proceedings of the National Academy of Sciences 85: 5601–5604.  https://doi.org/10.1073/pnas.85.15.5601
    Xiong, Z., Gaeta, R.T. & Pires, J.C. (2011) Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proceedings of the National Academy of Sciences 108: 7908–7913.  https://doi.org/10.1073/pnas.1014138108

  5. Zhang, H., Bian, Y., Gou, X., Zhu, B., Xu, C., Qi, B., Li, N., Rustgi, S., Zhou, H. Han, F., Jiang, J., von Wettstein, D. & Jiang, J. (2013) Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat. Proceedings of the National Academy of Sciences 110: 3447–3452.  https://doi.org/10.1073/pnas.1300153110
    Zhang, J., Wang, M., Guo, Z., Guan, Y., Guo, Y. & Yan, X. (2020) Variation in ploidy level and genome size of Cynodon dactylon (L.) Pers. along a latitudinal gradient. Folia Geobotanica 54: 267–278. https://doi.org/10.1007/s12224-019-09359-y