Greater reproductive assurance of asexual plant compared with sexual relative in a low-density sympatric population: Experimental evidence for pollen limitation

. 2021 Sep ; 34 (9) : 1503-1509. [epub] 20210812

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34331325

High reproductive assurance is regarded as a key advantage of uniparentally reproducing organisms for establishing a new population. This demographic benefit should especially be relevant for plants with autonomous apomixis, that is those which produce seeds completely independently from mates and pollinators. Indeed, many autonomous apomicts occupy larger distributional ranges when compared to their sexual relatives, showing geographical parthenogenesis patterns. However, uniparental reproduction advantage has only rarely been quantified in natural populations and results provided a mixed support, partly because allopatric sexual and asexual populations were exposed to different environmental and pollination conditions causing considerable between-population variation in the level of reproductive assurance. Here, we compared the level and stability of reproductive assurance between sexual self-incompatible and asexual autonomously apomictic plants of Hieracium alpinum (Asteraceae) cultivated in a sympatric low-density population with two levels of spatial clumping of sexual plants. Overall, we found that the realized seed set (i.e. proportion of well-developed seeds per capitulum) of asexuals was ca. 3 times greater than that of sexuals (83% vs. 27%), whereas the variance of this trait expressed as coefficient of variation was ca. 4 times smaller in asexuals compared with sexuals (19% vs. 83%). Solitary sexual plants had more than 2 times lower realized seed set when compared to clumps composed of two spatially close (20-30 cm) sexual plants (13% vs. 34%). Our study provides experimental evidence for benefit of uniparental reproduction of asexuals in a sympatric situation when the availability of mates is limited. This, together with unpredictability of pollinator environment could provide autonomous apomicts with an ultimate demographic superiority during colonization reflected in geographical parthenogenesis observed in this species.

Zobrazit více v PubMed

Albert, M.J., Escudero, A., & Iriondo, J.M. (2001). Female reproductive success of narrow endemic Erodium paularense in contrasting microhabitats. Ecology, 82, 1734-1747.

Asker, S. E., & Jerling, L. (1992). Apomixis in plants. Boca Raton, USA: CRC Press.

Baker, H. G. (1955). Self-compatibility and establishment after ‘long distance’ dispersal. Evolution, 9, 347-349. https://www.jstor.org/stable/2405656

Baker, H. G. (1967). Support for Baker’s Law - as a rule. Evolution, 21, 853-856. https://doi.org/10.1111/j.1558-5646.1967.tb03440.x

Bierzychudek, P. (1985). Patterns in plant parthenogenesis. Experientia, 41, 1255-1264. https://doi.org/10.1007/BF01952068

Bräutigam, S. (1992). Hieracium L. In H. Meusel, & E. J. Jäger (eds) Vergleichende Chorologie der zentraleuropäischen Flora 3 (pp. 325-333, 550-560). Gustav Fischer, Jena etc.

Brennan, A. C., Tabah, D. A., Harris, S. A., & Hiscock, S. J. (2010). Sporophytic selfincompatibility in Senecio squalidus (Asteraceae): S allele dominance interactions and modifiers of cross-compatibility and selfing rates. Heredity, 106, 113-123. https://doi.org/10.1038/hdy.2010.29

Carman, J. G. (1997). Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biological Journal of the Linnean Society, 61, 51-94. https://doi.org/10.1111/j.1095-8312.1997.tb01778.x

Chrtek, J. Jr (1997). Taxonomy of the Hieracium alpinum group in the Sudeten Mts., the West and the Ukrainian East Carpathians. Folia Geobotanica et Phytotaxonomica, 32, 69-97.

Chrtek, J., Hartmann, M., Mrázová, V., Zdvořák, P., Štefánek, M., & Mráz, P. (2018). Seed traits, terminal velocity and germination in sexual diploid and apomictic triploid Hieracium alpinum (Asteraceae): Are apomicts better dispersers? Flora, 240, 76-81. https://doi.org/10.1016/j.flora.2018.01.003

Cosendai, A.-C., & Hörandl, E. (2010). Cytotype stability, facultative apomixis and geographical parthenogenesis in Ranunculus kuepferi (Ranunculaceae). Annals of Botany, 105, 457-470. https://doi.org/10.1093/aob/mcp304

Dickinson, T. A., Lo, E., & Talent, N. (2007). Polyploidy, reproductive biology, and Rosaceae: Understanding evolution and making classifications. Plant Systematic and Evolution, 266, 59-78. https://doi.org/10.1007/s00606-007-0541-2

Dobeš, C., Scheffknecht, S., Fenko, Y., Prohaska, D., Sykora, C., & Hülber, K. (2018). Asymmetric reproductive interference: The consequences of cross-pollination on reproductive success in sexual-apomictic populations of Potentilla puberula (Rosaceae). Ecology and Evolution, 8(1), 365-381.

Elam, D.R., Ridley, C.E., Goodell, K., & Ellstrand, N. (2007). Population size and relatedness affect fitness of a self-incompatible invasive plant. Proceedings of The National Academy of Sciences of the USA, 104, 549-552.

Gathmann, A., & Tscharntke, T. (2002). Foraging ranges of solitary bees. Journal of Animal Ecology, 71, 757-764. https://doi.org/10.1046/j.1365-2656.2002.00641.x

Gustafsson, Å. (1946). Apomixis in higher plants. I. The mechanism of apomixis. Lunds Universitets Årsskrift, 42, 1-67.

Gustafsson, Å. (1947). Apomixis in higher plants. III. Biotype and species formation. Lunds Universitets Årsskrift, 43, 181-370.

Haag, C. R., & Ebert, D. (2004). A new hypothesis to explain geographic parthenogenesis. Annales Zoologici Fennici, 41, 539-544.

Hamston, T. J., Wilson, R. J., de Vere, N., Rich, T. C. G., Stevens, J. R., & Cresswell, J. E. (2017). Breeding system and spatial isolation from congeners strongly constrain seed set in an insect-pollinated apomictic tree: Sorbus subcuneata (Rosaceae). Scientific Reports, 7, 45122. https://doi.org/10.1038/srep45122

Hojsgaard, D., Klatt, S., Baier, R., Carman, J. G., & Hörandl, E. (2014). Taxonomy and biogeography of apomixis in Angiosperms and associated biodiversity characteristics. Critical Reviews in Plant Sciences, 33, 414-427. https://doi.org/10.1080/07352689.2014.898488

Hörandl, E. (2006). The complex causality of geographical parthenogenesis. New Phytologist, 171, 525-538. https://doi.org/10.1111/j.1469-8137.2006.01769.x

Hörandl, E. (2010). The evolution of self-fertility in apomictic plants. Sexual Plant Reproduction, 23, 73-86. https://doi.org/10.1007/s00497-009-0122-3

Hörandl, E., Cosendai, A.-C., & Temsch, E. M. (2008). Understanding the geographic distributions of apomictic plants: A case for a pluralistic approach. Plant Ecology and Diversity, 1, 309-320. https://doi.org/10.1080/17550870802351175

Kanarek, A. R., Webb, C. T., Barfield, M., & Holt, R. D. (2013). Allee effects, aggregation, and invasion success. Theoretical Ecology, 6, 153-164. https://doi.org/10.1007/s12080-012-0167-z

Karbstein, K., Rahmsdorf, E., Tomasello, S., Hodač, L., & Hörandl, E. (2020). Breeding system of diploid sexuals within the Ranunculus auricomus complex and its role in a geographical parthenogenesis scenario. Ecology and Evolution, 10, 14435-14450.

Karunarathne, P., Reutemann, A. V., Schedler, M., Glücksberg, A., Martínez, E. J., Honfi, A. I., & Hojsgaard, D. H. (2020). Sexual modulation in a polyploid grass: A reproductive contest between environmentally inducible sexual and genetically dominant apomictic pathways. Scientific Reports, 10, 8319. https://doi.org/10.1038/s41598-020-64982-6

Lepší, M., Koutecký, P., Nosková, J., Lepší, P., Urfus, T., & Rich, T. C. G. (2019). Versatility of reproductive modes and ploidy level interactions in Sorbus s.l. (Malinae, Rosaceae). Botanical Journal of the Linnean Society, 191, 502-522. https://doi.org/10.1093/botlinnean/boz054

Macková, L., Nosková, J., Ďurišová, Ľ., & Urfus, T. (2020). Insights into the cytotype and reproductive puzzle of Cotoneaster integerrimus in the Western Carpathians. Plant Systematics and Evolution, 306, 58. https://doi.org/10.1007/s00606-020-01684-6

Michaels, H. J., & Bazzaz, F. A. (1986). Resource allocation and demography of sexual and apomictic Antennaria parlinii. Ecology, 67, 27-36. https://doi.org/10.2307/1938500

Morales, C. L., & Traveset, A. (2008). Interspecific pollen transfer: Magnitude, prevalence and consequences for plant fitness. Critical Reviews in Plant Sciences, 27, 221-238. https://doi.org/10.1080/07352680802205631

Mráz, P. (2003). Mentor effects in the genus Hieracium s.str. (Compositae, Lactuceae). Folia Geobotanica, 38, 345-350. https://doi.org/10.1007/BF02803204

Mráz, P., Chrtek, J., & Šingliarová, B. (2009). Geographical parthenogenesis, genome size variation and pollen production in the arctic-alpine species Hieracium alpinum. Botanica Helvetica, 119, 41-51. https://doi.org/10.1007/s00035-009-0055-3

Mráz, P., & Ronikier, M. (2016). Biogeography of the Carpathians: Evolutionary and spatial facets of biodiversity. Biological Journal of the Linnean Society, 119, 528-559. https://doi.org/10.1111/bij.12918

Mráz, P., & Zdvořák, P. (2019). Reproductive pathways in Hieracium s.str. (Asteraceae): Strict sexuality in diploids and apomixis in polyploids. Annals of Botany, 123, 391-403. https://doi.org/10.1093/aob/mcy137

Mráz, P., Zdvořák, P., Hartmann, M., Štefánek, M., & Chrtek, J. (2019). Can obligate apomixis and more stable reproductive assurance explain the distributional successes of asexual triploids in Hieracium alpinum (Asteraceae)? Plant Biology, 21, 227-236.

Noyes, R. D. (2007). Apomixis in the asteraceae: Diamonds in the rough. Functional Plant Science & Biotechnology, 1, 207-222.

Noyes, R. D., & Givens, A. D. (2013). Quantitative assessment of megasporogenesis for the facultative apomicts Erigeron annuus and Erigeron strigosus (Asteraceae). International Journal of Plant Sciences, 174, 1239-1250.

O’Connell, L. M., & Eckert, C. G. (1999). Differentiation in sexuality among populations of Antennaria parlinii (Asteraceae). International Journal of Plant Sciences, 160, 567-575.

Pannell, J. R., Auld, J. R., Brandvain, Y., Burd, M., Busch, J. W., Cheptou, P. O., Conner, J. K., Goldberg, E. E., Grant, A. G., Grossenbacher, D. L., Hovick, S. M., Igic, B., Kalisz, S., Petanidou, T., Randle, A. M., De Casas, R. R., Pauw, A., Vamosi, J. C., & Winn, A. A. (2015). The scope of Baker’s law. New Phytologist, 208, 656-667. https://doi.org/10.1111/nph.13539

Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & Core Team R. (2017). nlme: linear and nonlinear mixed effects models. R package version 3.1-131. R Foundation for Statistical Computing, Vienna, Austria.

Pinc, J., Chrtek, J., Latzel, V., & Mráz, P. (2020). Negative effect of inbreeding on fitness of an arctic-alpine Hieracium alpinum (Asteraceae), a species with a geographical parthenogenesis distribution pattern. Plant Systematics and Evolution, 306, 62. https://doi.org/10.1007/s00606-020-01692-6

Quarin, C. L. (1999). Effect of pollen source and pollen ploidy on endosperm formation and seed set in pseudogamous apomictic Paspalum notatum. Sexual Plant Reproduction, 11, 331-335. https://doi.org/10.1007/s004970050160

R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Rasmussen, K. K., & Kollmann, J. (2004). Poor sexual reproduction on the distribution limit of the rare tree Sorbus torminalis. Acta Oecologica, 25, 211-218. https://doi.org/10.1016/j.actao.2004.02.001

Richards, A. J. (1997). Plant breeding systems (2nd ed.). Chapman and Hall.

Sailer, C., Stöcklin, J., & Grossniklaus, U. (2020). Dynamics of apomictic and sexual reproduction during primary succession on a glacier forefield in the Swiss Alps. Scientific Reports, 10, e8269. https://doi.org/10.1038/s41598-020-64367-9

Sanz, R., & Pulido, F. (2015). Pollen limitation and fruit abortion in a declining rare tree, the Eurasian yew (Taxus baccata L.): A reproductive cost of ecological marginality. Plant Biosystems, 149, 818-826. http://dx.doi.org/10.1080/11263504.2014.976290.

Schinkel, C. C. F., Kirchheimer, B., Dellinger, A. S., Klatt, S., Winkler, M., Dullinger, S., & Hörandl, E. (2016). Correlations of polyploidy and apomixis with elevation and associated environmental gradients in an alpine plant. AoB Plants, 8, plw064. https://doi.org/10.1093/aobpla/plw064

Skawińska, R. (1963). Apomixis in Hieracium alpinum L. Acta Biologica Cracoviensia, 5(1962), 7-14.

Slade, K., & Rich, T. C. G. (2007). Pollen studies in British Hieracium sect. Alpina (Asteraceae). Watsonia, 26, 443-450.

Stebbins, G. L. (1957). Self-fertilization and population variability in the higher plants. The American Naturalist, 91, 337-354. https://doi.org/10.1086/281999

Stephenson, A. G. (1981). Flower and fruit abortion: Proximate causes and ultimate functions. Annual Review of Ecology and Systematics, 12, 253-279. https://doi.org/10.1146/annurev.es.12.110181.001345

van Dijk, P. J. (2007). Potential and realized costs of sex in dandelions, Taraxacum officinale s.l. In E. Hörandl, U. Grossniklaus, P. J. van Dijk, & T. Sharbel (Eds.), Apomixis: evolution, mechanisms and perspectives (pp. 215-233). Regnum Vegetabile 147. Gantner, Ruggell.

Vandel, A. P. M. (1928). La parthénogénèse géographique. Contribution à l’étude biologique et cytologique de la parthénogénèse naturelle. Bulletin Biologique de la France et de la Belgique, 62, 164-182.

Waser, N. M. (1978). Interspecific pollen transfer and competition between co-occurring plant species. Oecologia, 36(2), 223-236. https://www.jstor.org/stable/4215704.

Zobrazit více v PubMed

Dryad
10.5061/dryad.vhhmgqntq

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...