Asymmetric hybridization in Central European populations of the Dryopteris carthusiana group

. 2019 Nov ; 106 (11) : 1477-1486. [epub] 20191021

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31634425

Grantová podpora
19-17379S Czech Science Foundation - International

PREMISE: Hybridization is a key process in plant speciation. Despite its importance, there is no detailed study of hybridization rates in fern populations. A proper estimate of hybridization rates is needed to understand factors regulating hybridization. METHODS: We studied hybridization in the European Dryopteris carthusiana group, represented by one diploid and two tetraploid species and their hybrids. We sampled ~100 individuals per population in 40 mixed populations of the D. carthusiana group across Europe. All plants were identified by measuring genome size (DAPI staining) using flow cytometry. To determine the maternal parentage of hybrids, we sequenced the chloroplast region trnL-trnF of all taxa involved. RESULTS: We found hybrids in 85% of populations. Triploid D. ×ambroseae occurred in every population that included both parent species and is most abundant when the parent species are equally abundant. By contrast, tetraploid D. ×deweveri was rare (15 individuals total) and triploid D. ×sarvelae was absent. The parentage of hybrid taxa is asymmetric. Despite expectations from previous studies, tetraploid D. dilatata is the predominant male parent of its triploid hybrid. CONCLUSIONS: This is a thorough investigation of hybridization rates in natural populations of ferns. Hybridization rates differ greatly even among closely related fern taxa. In contrast to angiosperms, our data suggest that hybridization rates are highest in balanced parent populations and support the notion that some ferns possess very weak barriers to hybridization. Our results from sequencing cpDNA challenge established notions about the correlation of ploidy level and mating tendencies.

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Arnold, M. L. 1992. Natural hybridization as an evolutionary process. Annual Review of Ecology, Evolution, and Systematics 1992: 237-261.

Arnold, M. L. 1997. Natural hybridization and evolution. Oxford University Press, Oxford, UK.

Arnold, M. L., and B. D. Bennett. 1993. Natural hybridization in Louisiana Irises: Genetic variation and ecological determinants. In R. G. Harrison [ed.], Hybrid Zones and the Evolutionary Process, 115-139. Oxford University Press, New York, USA.

Arnold, M. L., J. L. Hamrick, and B. D. Bennett. 1993. Interspecific pollen competition and reproductive isolation in Iris. Journal of Heredity 84: 13-16.

Baack, E., M. C. Melo, L. H. Rieseberg, and D. Ortiz-Barrientos. 2015. The origins of reproductive isolation in plants. New Phytologist 207: 968-984.

Bacilieri, R., A. Ducousso, R. J. Petit, and A. Kremer. 1996. Mating system and asymmetric hybridization in a mixed stand of European oaks. Evolution 50: 900-908.

Barker, J. 1988. The sexual expression and development in vitro of gametophytes of Dryopteris filix-mas (L.) Schott and Dryopteris dilatata (Hoffm.) A. Gray. M. Phil Thesis. Derbyshire College of Higher Education, Derby, UK.

Barrington, D. S., C. H. Haufler, and C. R. Werth. 1989. Hybridization, reticulation, and species concepts in the ferns. American Fern Journal 79: 55-64.

Beatty, G. E., M. Phillipp, and J. Provan. 2009. Unidirectional hybridization at a species’ range boundary: implications for habitat tracking. Diversity and Distribution 16: 1-9.

Bennert, H. W., W. Jäger, H. Bäppler, M. Lubienski, R. Theimann, R. Viane, and A. Sarazin. 2012. Dryopteris expansa (C. Presl) Frasek-Jenkins & Jermy und D. ×ambroseae Fraser-Jenk. & Jermy (Dryopteridaceae) in Nordrhein-Westfalen - Identifizierung, Verbreitung, Ökologie. Decheniana 165: 37-53.

Brownsey, P. J. 1977. Asplenium hybrids in the New Zealand flora. New Zealand Journal of Botany 15: 601-637.

Buggs, R. J. A., and J. R. Pannell. 2006. Rapid displacement of a monoecious plant lineage is due to pollen swamping by a dioecious relative. Current Biology 16: 996-1000.

Carney, S. E., M. B. Cruzan, and M. L. Arnold. 1994. Reproductive interactions between hybridizing irises: analyses of pollen-tube growth and fertilization success. American Journal of Botany 81: 1169-1175.

Corley, H. V., and M. Gibby. 1981. Dryopteris × sarvelae in Scotland: A new hybrid for the British Isles. Fern Gazette 12: 178.

DeSoto, L., L. G. Quintanilla, and M. Méndez. 2008. Environmental sex determination in ferns: effects of nutrient availability and individual density in Woodwardia radicans. Journal of Ecology 96: 1319-1327.

Doležel, J., J. Greilhuber, S. Lucretti, A. Meister, M. A. Lysák, L. Nardi, and R. Obermayer. 1998. Plant genome size estimation by flow cytometry: Inter-laboratory comparison. Annals of Botany 82: 17-26.

Doležel, J., J. Greilhuber, and J. Suda. 2007. Estimation of nuclear DNA content in plants using flow cytometry. Nature Protocols 2: 2233-2244.

Ekrt, L., and P. Koutecký. 2016. Between sexual and apomictic: unexpectedly variable sporogenesis and production of viable polyhaploids in the pentaploid fern of the Dryopteris affinis agg. (Dryopteridaceae). Annals of Botany 117: 97-106.

Ekrt, L., R. Holubová, P. Trávníček, and J. Suda. 2010. Species boundaries and frequency of hybridization in the Dryopteris carthusiana (Dryopteridaceae) complex: A taxonomic puzzle resolved using genome size data. American Journal of Botany 97: 1208-1219.

Emms, S. K., S. A. Hodges, and M. L. Arnold. 1996. Pollen-tube competition, siring success, and consistent asymmetric hybridization in Louisiana irises. Evolution 50: 2201-2206.

Endress, P. K. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge, UK.

Flinn, K. M. 2006. Reproductive biology of three fern species may contribute to differential colonization success in post-agricultural forests. American Journal of Botany 93: 1289-1294.

de Groot, G. A., B. Verduyn, E. R. J. Wubs, R. H. J. Erkens, and H. J. During. 2012. Inter- and intraspecific variation in fern mating systems after long-distance colonization: the importance of selfing. BMC Plant Biology 12: 3.

Hamzeh, M., C. Sawchyn, P. Périnet, and S. Dayanandan. 2007. Asymmetrical natural hybridization between Populus deltoides and P. balsamifera (Salicaceae). Canadian Journal of Botany 85: 1227-1232.

Hanušová, K., M. Čertner, T. Urfus, P. Koutecký, J. Košnar, C. J. Rothfels, V. Jarolímová, et al. 2019. Widespread co-occurrence of multiple ploidy levels in fragile ferns (Cystopteris fragilis complex; Cystopteridaceae) likely stems from similar ecology of cytotypes, their efficient dispersal and inter-ploidy hybridization. Annals of Botany 123: 845-855.

Hori, K., Y. Okuyama, Y. Watano, and N. Murakami. 2018. Recurrent hybridization without homoeologous chromosome paring in the Dryopteris varia complex (Dryopteridaceae). Chromosome Botany 13: 9-24.

Hornych, O., and L. Ekrt. 2017. Spore abortion index (SAI) as a perspective tool of evaluation of spore fitness in ferns: An insight into sexual and apomictic species. Plant Systematics and Evolution 303: 497-507.

Hunt, H. V., S. W. Ansell, S. J. Russell, H. Schneider, and J. C. Vogel. 2011. Dynamics of polyploid formation and establishment in the allotetraploid rock fern Asplenium majoricum. Annals of Botany 108: 143-157.

Jessen, S., and H. Rasbach. 1987. Dryopteris × sarvelae, erster Nachweis für Mitteleuropa. Abstammung, verwandte Arten und Hybriden (Pteridophyta). Gleditschia 15: 57-72.

Jorgensen, R. B., and B. Andersen. 1994. Spontaneous hybridization between oilseed rape (Brassica napus) and weedy B. campestris (Brassicaceae): A risk of growing genetically modified oilseed rape. American Journal of Botany 81: 1620-1626.

Juslén, A., H. Väre, and N. Wikström. 2011. Relationships and evolutionary origins of polyploid Dryopteris (Dryopteridaceae) from Europe inferred using nuclear pgiC and plastid trnL-F sequence data. Taxon 60: 1284-1294.

Kaplan, Z., J. Danihelka, J. Štěpánková, L. Ekrt, J. Chrtek Jr, J. Zázvorka, V. Grulich, et al. 2016. Distributions of vascular plants in the Czech Republic. Part 2. Preslia 88: 229-322.

Kentner, E. K., and M. R. Mesler. 2000. Evidence for natural selection in a fern hybrid zone. American Journal of Botany 87: 1168-1174.

Knobloch, I. W., M. Gibby, and C. Fraser-Jenkins. 1984. Recent advances in our understanding of pteridophyte hybrids. Taxon 33: 256-270.

Köhler, C., O. Mittelsten Scheid, and A. Erilova. 2010. The impact of the triploid block on the origin and evolution of polyploid plants. Trends in Genetics 26: 142-148.

Korpelainen, H. 1994. Growth, sex determination and reproduction of Dryopteris filix-mas (L.) Schott gametophytes under varying nutritional conditions. Botanical Journal of the Linnean Society 114: 357-366.

Koutecký, P., T. Baďurová, M. Štech, J. Košnar, and J. Karásek. 2011. Hybridization between diploid Centaurea pseudophrygia and tetraploid C. jacea (Asteraceae): the role of mixed pollination, unreduced gametes, and mentor effects. Biological Journal of the Linnean Society 104: 93-106.

Landis, J. B., D. E. Soltis, Z. Li, H. E. Marx, M. S. Barker, D. C. Tank, and P. S. Soltis. 2018. Impact of whole-genome duplication events on diversification rates in angiosperms. American Journal of Botany 105: 348-363.

Lepais, O., R. J. Petit, E. Guichoux, E. Lavabre, F. Alberto, A. Kremer, and S. Gerber. 2009. Species relative abundance and direction of introgression in oaks. Molecular Ecology 18: 2228-2242.

Lewis, D., and L. K. Crowe. 1958. Unilateral interspecific incompatibility in flowering plants. Heredity 12: 233-256.

Li, F. W., B. C. Tan, V. Buchbender, R. C. Moran, G. Rouhan, C. N. Wang, and D. Quandt. 2009. Identifying a mysterious aquatic fern gametophyte. Plant Systematics and Evolution 281: 77-86.

Ma, Y., W. Xie, X. Tian, W. Sun, Z. Wu, and R. Milne. 2014. Unidirectional hybridization and reproductive barriers between two heterostylous primrose species in north-west Yunnan, China. Annals of Botany 113: 763-775.

Maheshwari, S., and D. A. Barbash. 2011. The genetics of hybrid incompatibilities. Annual Review of Genetics 45: 331-355.

Masuyama, S. 1979. Reproductive biology of the fern Phegopteris decursive-pinnata. I. The dissimilar mating systems of diploids and tetraploids. Botanical Magazine (Tokyo) 92: 275-289.

Natcheva, R., and N. Cronberg. 2004. What do we know about hybridization among bryophytes in nature? Canadian Journal of Botany 82: 1687-1704.

Nieto-Lugilde, M., O. Werner, S. F. McDaniel, P. Koutecký, J. Kučera, S. M. Rizk, and R. M. Ros. 2018. Peripatric speciation associated with genome expansion and female-biased sex ratios in the moss genus Ceratodon. American Journal of Botany 105: 1-12.

Njuguna, W., A. Liston, R. Cronn, T.-L. Ashman, and N. Bassil. 2013. Insights into phylogeny, sex function and age of Fragaria based on whole chloroplast genome sequencing. Molecular Phylogenetics and Evolution 66: 17-29.

Otto, S. P., and J. Whitton. 2000. Polyploid incidence and evolution. Annual Review of Genetics 34: 401-437.

Ouayjan, A., and A. Hampe. 2018. Extensive sib-mating in a refugial population of beech (Fagus sylvatica) growing along a lowland river. Forest Ecology and Management 407: 66-74.

Pangua, E., L. G. Quintanilla, A. Sancho, and S. Pajarón. 2003. A comparative study of the gametophytic generation in the Polystichum aculeatum group (Pteridophyta). International Journal of Plant Sciences 164: 295-303.

Peng, C.-I., and T.-Y. Chiang. 2000. Molecular confirmation of unidirectional hybridization in Begonia x taipeiensis Peng (Begoniaceae) from Taiwan. Annals of the Missouri Botanical Garden 87: 273-285.

Peredo, E. L., M. Méndez-Couz, M. A. Revilla, and H. Fernández. 2013. Mating system in Blechnum spicant and Dryopteris affinis ssp. affinis correlates with genetic variability. American Fern Journal 103: 27-39.

Perley, D. S., and L. K. Jesson. 2015. Hybridization is associated with changes in sexual system in the bryophyte genus Atrichum. American Journal of Botany 102: 555-565.

Petit, R. J., E. Pineau, B. Demesure, R. Bacilieri, A. Ducousso, and A. Kremer. 1997. Chloroplast DNA footprints of postglacial recolonization by oaks. Proceedings of the National Academy of Sciences, USA 94: 9996-10001.

Prentis, P. J., E. M. White, I. J. Radford, A. J. Lowe, and A. R. Clarke. 2007. Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis? New Phytologist 176: 902-912.

R Core Team. 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Website http://www.R-project.org/ [accessed 19 March 2019].

Raghavan, V. 1989. Developmental biology of fern gametophytes. Cambridge University Press, New York, USA.

Reichstein, T. 1981. Hybrids in European Aspleniaceae (Pteridophyta). Botanica Helvetica 91: 89-139.

Rieseberg, L. H., and S. E. Carney. 1998. Plant hybridization. New Phytologist 140: 599-624.

Rieseberg, L. H., A. Desrochers, and S. J. Youn. 1995. Interspecific pollen competition as a reproductive barrier between sympatric species of Helianthus (Asteraceae). American Journal of Botany 82: 515-519.

Rieseberg, L. H., S. J. E. Baird, and A. M. Desrochers. 1998. Patterns of mating in wild sunflower hybrid zones. Evolution 52: 713-726.

Rothfels, C. J., A. K. Johnson, P. H. Hovenkamp, D. L. Swofford, H. C. Roskam, C. R. Fraser-Jenkins, M. D. Windham, and K. M. Pryer. 2015. Natural hybridization between parental lineages that diverged approximately 60 million years ago. American Naturalist 185: 433-442.

Rünk, K., M. Zobel, and K. Zobel. 2010. Different factors govern the performance of three closely related and ecologically similar Dryopteris species with contrastingly different abundance in transplant experiment. Botany 88: 961-969.

Rünk, K., Z. Zobel, and K. Zobel. 2012. Biological flora of the British Isles: Dryopteris carthusiana, D. dilatata and D. expansa. Journal of Ecology 100: 1039-1063.

Schneider, H., H. M. Liu, Y. F. Chang, D. Ohlsen, L. R. Perrie, L. Shepherd, M. Kessler, et al. 2017. Neo- and paleopolyploidy contribute to the species diversity of Asplenium - the most species-rich genus of ferns. Journal of Systematics and Evolution 55: 353-364.

Schneller, J. J. 2008. Antheridiogens. In T. A. Ranker and C. H. Haufler [eds.], Biology and evolution of ferns and lycophytes. Cambridge University Press, Cambridge, UK.

Schneller, J. J., C. H. Haufler, and T. A. Ranker. 1990. Antheridiogens and natural gametophyte populations. American Fern Journal 80: 143-152.

Schnittler, M., K. Horn, R. Kaufmann, R. Rimgailė-Voicik, A. Klahr, M. Bog, J. Fuchs, and H. W. Bennert. 2018. Genetic diversity and hybrid formation in Central European club-mosses (Diphasiastrum, Lycopodiaceae) - new insights from cp microsatellites, two nuclear markers and AFLP. Molecular Phylogenetics and Evolution 131: 181-192.

Sessa, E. B., E. A. Zimmer, and T. J. Givnish. 2012a. Reticulate evolution on a global scale: A nuclear phylogeny for New World Dryopteris (Dryopteridaceae). - Molecular Phylogenetics and Evolution 64: 563-581.

Sessa, E. B., E. A. Zimmer, and T. J. Givnish. 2012b. Unraveling reticulate evolution in North American Dryopteris (Dryopteridaceae). BMC Evolutionary Biology 12: 104.

Sessa, E. B., W. L. Testo, and J. E. Watkins Jr. 2016. On the widespread capacity for, and functional significance of, extreme inbreeding in ferns. New Phytologist 211: 1108-1119.

Sharpe, J. M., K. Mehltreter, and L. R. Walker. 2010. Ecological importance of ferns. In K. Mehltreter, L. R. Walker and J. M. Sharpe [eds.], Fern ecology, 1-21. Cambridge University Press, Cambridge, UK.

Shaw, J. 1994. Systematics of Mielichhoferia (Bryaceae: Musci). III. Hybridization between M. elongate and M. mielichhoferiana. American Journal of Botany 81: 782-790.

Sigel, E. M. 2016. Genetic and genomic aspects of hybridization in ferns. Journal of Systematics and Evolution 54: 638-655.

Soltis, D. E., and P. S. Soltis. 1987. Breeding system of the fern Dryopteris expansa: Evidence for mixed mating. American Journal of Botany 74: 504-509.

Soltis, P. S., and D. E. Soltis. 2000. The role of genetic and genomic attributes in the success of polyploids. Proceedings of the National Academy of Sciences, USA 97: 7051-7057.

Soltis, D. E., C. J. Visger, D. B. Marchant, and P. S. Soltis. 2000. Polyploidy: Pitfalls and paths to a paradigm. American Journal of Botany 103: 1146-1166.

Sorsa, V., and C. J. Widén. 1968. The Dryopteris spinulosa complex in Finland, a cytological and chromatographic study of some hybrids. Hereditas 60: 273-293.

Stein, D. B., C. Hutton, D. S. Conant, C. H. Haufler, and C. R. Werth. 2010. Reconstructing Dryopteris “semicristata” (Dryopteridaceae): Molecular profiles of tetraploids verify their undiscovered diploid ancestor. American Journal of Botany 97: 998-1004.

Taberlet, P., L. Gielly, G. Pautou, and J. Bouvet. 1991. Universal primers for amplification of three noncoding regions of chloroplast DNA. Plant Molecular Biology 17: 1105-1109.

Testo, W. L., J. E. Watkins, and D. S. Barrington. 2015. Dynamics of asymmetrical hybridization in North American wood ferns: reconciling patterns of inheritance with gametophyte reproductive biology. New Phytologist 206: 785-795.

Thiers, B. 2019 onward (continuously updated). Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden's Virtual Herbarium. Available at http://sweetgum.nybg.org/science/ih/ [accessed 28 March 2019].

Trucco, F., T. Tatum, A. L. Rayburn, and P. J. Tranel. 2009. Out of the swamp: unidirectional hybridization with weedy species may explain the prevalence of Amaranthus tuberculatus as a weed. New Phytologist 184: 819-827.

Turelli, M., and L. C. Moyle. 2007. Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics 176: 1059-1088.

Twyford, A. D., and R. A. Ennos. 2012. Next-generation hybridization and introgression. Heredity 108: 179-189.

van der Velde, M., and R. Bijlsma. 2004. Hybridization and asymmetric reproductive isolation between the closely related bryophyte taxa Polytrichum commune and P. uliginosum. Molecular Ecology 13: 1447-1454.

van der Velde, M., H. J. During, L. van de Zande, and R. Bijlsma. 2001. The reproductive biology of Polytrichum formosum: clonal structure and paternity revealed by microsatellites. Molecular Ecology 10: 2423-2434.

Vogel, J. C., S. J. Russell, F. J. Rumsey, J. A. Barrett, and M. Gibby. 1998. On hybrid formation in the rock fern Asplenium ×alternifolium (Aspleniaceae, Pteridophyta). Botanica Acta 111: 241-246.

Wagner, W. H. Jr, and L. C. Chen. 1965. Abortion of spores and sporangia as a tool in the detection of Dryopteris hybrids. American Fern Journal 55: 9-29.

Widén, C. J., J. Sarvela, and T. Ahti. 1967. The Dryopteris spinulosa complex in Finland. Acta Botanica Fennica 77: 1-25.

Wood, T. E., N. Takebayashi, M. S. Barker, I. Mayrose, P. B. Greenspoon, and L. H. Rieseberg. 2009. The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences, USA 106: 13875-13879.

Wubs, E. R. J., G. A. de Groot, H. J. During, J. C. Vogel, M. Grundmann, P. Bremer, and H. Schneider. 2010. Mixed mating system in the fern Asplenium scolopendrium: implications for colonization potential. Annals of Botany 106: 583-590.

Xiang, L., C. R. Werth, S. N. Emery, and D. E. McCauley. 2000. Population-specific gender-biased hybridization between Dryopteris intermedia and D. carthusiana: evidence from chloroplast DNA. American Journal of Botany 87: 1175-1180.

Zhang, R., T. Liu, W. Wu, Y. Li, L. Chao, L. Huang, Y. Huang, et al. 2013. Molecular evidence for natural hybridization in the mangrove fern genus Acrostichum. BMC Plant Biology 13: 74.

Zhou, R., X. Gong, D. Boufford, C.-I. Wu, and S. Shi. 2008. Testing a hypothesis of unidirectional hybridization in plants: Observations on Sonneratia, Bruguiera and Ligularia. BMC Evolutionary Biology 8: 149.

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