Environmental stressors affect sex ratios in sexually dimorphic plant sexual systems.
dioecy
gynodioecy
sex ratio
sexual systems
subdioecy
trioecy
Journal
Plant biology (Stuttgart, Germany)
ISSN: 1438-8677
Titre abrégé: Plant Biol (Stuttg)
Pays: England
ID NLM: 101148926
Informations de publication
Date de publication:
Sep 2020
Sep 2020
Historique:
received:
06
01
2020
accepted:
29
03
2020
pubmed:
26
4
2020
medline:
14
1
2021
entrez:
26
4
2020
Statut:
ppublish
Résumé
Revealing the environmental pressures determining the frequency of females amongst populations of sexually dimorphic plants is a key research question. Analyses of sex ratio variation have been mainly done in dioecious plants, which misses key plant sexual systems that might represent intermediate stages in the evolution of dioecy from hermaphroditism. We investigated female frequency across populations of sexually dimorphic plant species in relation to environmental stressors (temperature, precipitation), totaling 342 species, 2011 populations, representing 40 orders and three different sexual systems (dioecy, gynodioecy and subdioecy). We also included the biome where the population was located to test how female frequency may vary more broadly with climate conditions. After correcting for phylogeny, our results for gynodioecious systems showed a positive relationship between female frequency and increased environmental stress, with the main effects being temperature-related. Subdioecious systems also showed strong positive relationships with temperature, and positive and negative relationships related to precipitation, while no significant effects on sex ratio in dioecious plants were detected. Combined, we show that female frequencies in an intermediate sexual system on the pathway from hermaphroditism to dioecy respond strongly to environmental stressors and have different selective agents driving female frequency.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
890-898Subventions
Organisme : H2020 Marie Sklodowska-Curie IF
ID : 660104
Informations de copyright
© 2020 The Authors. Plant Biology published by John Wiley & Sons Ltd on behalf of German Society for Plant Sciences, Royal Botanical Society of the Netherlands.
Références
Alonso C., Herrera C.M. (2001) Neither vegetative nor reproductive advantages account for high frequency of male-steriles in southern Spanish gynodioecious Daphne laureola (Thymelaeaceae). American Journal of Botany, 88, 1016-1024.
Ashman T.-L. (1994) Reproductive allocation in hermaphrodite and female plants of Sidalcea oregana ssp. spicata (Malvaceae) using four currencies. American Journal of Botany, 81, 433-438.
Ashman T.-L. (1999) Determinants of sex allocation in a gynodioecious wild strawberry: implications for the evolution of dioecy and sexual dimorphism. Journal of Evolutionary Biology, 12, 648-661.
Ashman T.-L. (2006) The evolution of separate sexes: a focus on the ecological context. In: Harder L.D., Barrett S.C.H. (Eds), Ecology and evolution of flowers. Oxford University Press, New York, USA, pp 204-222.
Asikainen E., Mutikainen P. (2003) Female frequency and relative fitness of females and hermaphrodites in gynodioecious Geranium sylvaticum (Geraniaceae). American Journal of Botany, 90, 226-234.
Barrett S.C.H., Yakimowski S.B., Field D.L., Pickup D.L. (2010) Ecological genetics of sex ratios in plant populations. Philosophical Transactions of the Royal Society of London, series B: Biological Sciences, 365, 2549-2557.
Bierzychudek P., Eckhart V. (1988) Spatial segregation of the sexes of dioecious plants. The American Naturalist, 132, 34-43.
Caruso C.M., Case A.L. (2007) Sex ratio variation in gynodioecious Lobelia siphilitica: effects of population size and geographic location. Journal of Evolutionary Biology, 20, 1396-1405.
Caruso C.M., Eisen K., Case A.L. (2016) An angiosperm-wide analysis of the correlates of gynodioecy. International Journal of Plant Sciences, 177, 115-121.
Case A.L., Ashman T.-L. (2005) Sex-specific physiology and its implications for the cost of reproduction. In: Reekie E.G., Bazzaz F.A. (Eds), Reproductive allocation in plants. Elsevier/Academic Press, Cambridge, MA, USA, pp 129-157.
Case A.L., Barrett S.C.H. (2004) Environmental stress and the evolution of dioecy: Wurmbea dioica (Colchicaceae) in Western Australia. Evolutionary Ecology, 18, 145-164.
Charlesworth D. (1981) Allocation of resources to male and female functions in hermaphrodites. Biological Journal of the Linnean Society, 15, 57-74.
Charlesworth D. (2002) Plant sex determination and sex chromosomes. Heredity, 88, 94-101.
Chase D.L. (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends in Genetics, 23, 81-90.
Clarke B.C., Shelton P.R., Mani G.S. (1988) Frequency-dependent selection, metrical characters and molecular evolution. Philosophical Transactions of the Royal Society of London, series B Biological Sciences, 319, 631-40.
Core Team R. (2018) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria Available from: https://www.R-project.org.
Darwin C.R. (1877) The different forms of flowers on plants of the same species. John Murray, London, UK.
Delph L.F. (1990) Sex-differential resource allocation patterns in the subdioecious shrub Hebe subalpina. Ecology, 71, 1342-1351.
Delph L.F., Johannsson M.H., Stephenson A.G. (1997) How environmental factors affect pollen performance: ecological and evolutionary perspectives. Ecology, 78, 1632-1639.
Dorken M.E., Pannell J.R. (2008) Density-dependent regulation of the sex ratio in an annual plant. The American Naturalist, 171, 824-830.
Dudley L.S. (2006) Ecological correlates of secondary sexual dimorphism in Salix glauca (Salicaceae). American Journal of Botany, 93, 1775-1783.
Ehlers B.K., Bataillon T. (2007) “Inconstant males” and the maintenance of labile sex expression in subdioecious plants. New Phytologist, 174, 194-211.
Field D.L., Pickup M., Barrett S.C.H. (2012) Comparative analyses of sex-ratio variation in dioecious flowering plants. Evolution, 67, 661-672.
Field D.L., Pickup M., Barrett S.C.H. (2013) Ecological context and metapopulation dynamics affect sex-ratio variation among dioecious plant populations. Annals of Botany, 111, 917-923.
Fisher R.A. (1930) The genetical theory of natural selection. Clarendon Press, Oxford, UK.
Frank S.A. (1989) The evolutionary dynamics of cytoplasmic male sterility. The American Naturalist, 133, 345-376.
Freckleton R.P. (2011) Dealing with collinearity in behavioural and ecological data: model averaging and the problems of measurement error. Behavioral Ecology and Sociobiology, 65, 91-101.
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.
Geber M.A., Dawson T.E., Delph L.F. (1999) Gender and sexual dimorphism in flowering plants. Springer, Berlin, Germany.
Gibson J., Diggle P. (1997) Structural analysis of female and hermaphroditic flowers of a gynodioecious tree, Ocotea tenera (Lauraceae). American Journal of Botany, 84, 298-298.
Goldberg E.E., Otto S.P., Vamosi J.C., Mayrose I., Sabath N., Ming R., Ashman T.-L. (2017) Macroevolutionary synthesis of flowering plant sexual systems. Evolution, 71, 898-912.
Gomez N.N., Shaw R.G. (2006) Inbreeding effect on male and female fertility and inheritance of male sterility in Nemophila menziesii (Hydrophyllaceae). American Journal of Botany, 93, 739-746.
Gouyon P.H., Vichot F., Van Damme J.M.M. (1991) Nuclear-cytoplasmic male sterility: single point equilibria versus limit cycles. The American Naturalist, 137, 498-514.
Hadfield J.D. (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R Package. Journal of Statistical Software, 33, 1-22.
Hedhly A., Hormaza J.I., Herrero M. (2009) Global warming and sexual plant reproduction. Trends in Plant Science, 14, 30-36.
Henry I.M., Akagi T., Tao R., Comai I. (2018) One hundred ways to invent the sexes: theoretical and observed paths to dioecy in plants. Annual Review in Plant Biology, 69, 553-575.
Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G., Jarvis A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978.
Hultine K.R., Grady K.C., Wood T.E., Shuster S.M., Stella J.C. (2016) Climate change perils for dioecious plant species. Nature Plants, article number, 16109, https://doi.org/10.1038/NPLANTS.2016.109.
Iossa G. (2019) Sex-specific differences in thermal fertility limits. Trends in Ecology & Evolution, 34, 490-492.
Jin Y., Qian H. (2019) S.PhyloMaker: an R package that can generate very large phylogenies for vascular plants. Ecography, 42, 1353-1359.
de Jong T.J., van de Meijden E. (2004) Sex ratio of some long-lived dioecious plants in a sand dune area. Plant Biology, 6, 616-620.
Käfer J., Marais G.A.B., Pannell J.R. (2017) On the rarity of dioecy in flowering plants. Molecular Ecology, 26, 1225-1241.
Korpelainen H. (1998) Labile sex expression in plants. Biological Reviews, 73, 157-180.
Lloyd D.G., Bawa K.S. (1984) Modification of the gender of seed plants in varying conditions. Evolutionary Biology, 17, 255-338.
Loveless M.D., Hamrick J.L. (1984) Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics, 15, 65-95.
Maurice S., Fleming T. (1995) The effect of pollen limitation on plant reproductive systems and the maintenance of sexual polymorphisms. Oikos, 74, 55-60.
McCauley D.E., Bailey M.F. (2009) Recent advance in the study of gynodioecy: the interface of theory and empiricism. Annals of Botany, 104, 611-620.
McCauley D.E., Brock M.T. (1998) Frequency-dependent fitness in Silene vulgaris, a gynodioecious plant. Evolution, 52, 30-36.
Moeller D.A., Briscoe Runquist R.D., Moe A.M., Geber M.A., Goodwillie C., Cheptou P.-O., Eckert C.G., Elle E., Johnston M.O., Kalisz S., Ree R.H., Sargent R.D., Vallejo-Marin M., Winn A.A. (2017) Global biogeography of mating system variation in seed plants. Ecology Letters, 20, 375-384.
Munné-Bosch S. (2015) Sex ratios in dioecious plants in the framework of global change. Environmental and Experimental Botany, 109, 99-102.
Obeso J.-R. (2002) The costs of reproduction in plants. New Phytologist, 155, 321-348.
O'Donnel M.S., Ignizio D.A. (2012) Bioclimatic predictors for supporting ecological applications in the conterminous United States. U.S. Geological Survey Data Series 691.
Olson D.M., Dinerstein E., Wikramanayake E.D. (2001) Terrestrial ecoregions of the world: A new map of life on Earth. BioScience, 51, 933-938.
Purrington C.B., Schmitt J. (1998) Consequences of sexually dimorphic timing of emergence and flowering in Silene latifolia. Journal of Ecology, 86, 397-404.
Reekie E.G., Bazzaz F.A. (2005) Reproductive allocation in plants. Elsevier/Academic Press, New York, USA.
Renner S.S. (2014) The relative and absolute frequencies of angiosperm sexual systems: Dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany, 101, 1588-1596.
Retuerto R., Sánchez-Vilas J., Varga S. (2018) Sexual dimorphism in response to stress. Environmental and Experimental Botany, 146, 1-4.
Ruffatto D.M., Zaya D.N., Molano-Flores B. (2015) Reproductive success of the gynodioecious Lobelia spicata Lam. (Campanulaceae): Female frequency, population demographics, and latitudinal patterns. International Journal of Plant Sciences, 176, 120-130.
Shykoff J.A., Kolokotronis S.-O., Collin C.L., López-Villavicencio M. (2003) Effects of male sterility in reproductive traits in gynodioecious plants: a meta-analysis. Oecologia, 135, 1-9.
Sinclair J.P., Emlen J., Freeman D.C. (2012) Biased sex ratios in plants: theory and trends. Botanical Review, 78, 63-86.
Sloan D.B. (2015) Using plants to elucidate the mechanisms of cytonuclear co-evolution. New Phytologist, 205, 1040-1046.
Spigler R.B., Ashman T.-L. (2011) Sex ratio and subdioecy in Fragaria virginiana: the roles of plasticity and gene flow examined. New Phytologist, 190, 158-168.
Spigler R.B., Ashman T.-L. (2012) Gynodioecy to dioecy: are we there yet? Annals of Botany, 109, 531-543.
Stehlik I., Friedman J., Barrett S.C.H. (2008) Environmental influence on primary sex ratio in a dioecious plant. Proceedings of the National Academy of Sciences, USA, 105, 10847-10852.
Thomson J.D., Barrett S.C.H. (1981) Selection for outcrossing, sexual selection, and the evolution of dioecy in plants. The American Naturalist, 118, 443-449.
Vamosi J.C., Otto S.P., Barrett S.C.H. (2003) Phylogenetic analysis of the ecological correlates of dioecy in angiosperms. Journal of Evolutionary Biology, 16, 1006-1018.
Van Etten M.L., Prevost L.B., Deen A.C., Ortiz B.V., Donovan L.A., Chang S.M. (2008) Gender differences in reproductive and physiological traits in a gynodioecious species, Geranium maculatum (Geraniaceae). International Journal of Plant Sciences, 169, 271-279.
Varga S., Kytöviita M.-M. (2016) Light availability affects sex lability in a gynodioecious plant. American Journal of Botany, 103, 1928-1936.
Vaughton G., Ramsey M. (2004) Dry environments promote the establishmnt of females in monomorphic populations of Wurmbea biglandulosa (Colchicaceae). Evolutionary Ecology, 18, 323-341.
Vega-Frutis R., Macias-Ordonez R.Guevara R.Fromhage L. (2014) Sex change in plants and animals: a unified perspective. Journal of Evolutionary Biology, 27, 667-675.
Webb C.J. (1979) Breeding systems and the evolution of dioecy in New Zealand apioid Umbelliferae. Evolution, 33, 662-672.
Werren J.H., Beukeboom L.W. (1998) Sex determination, sex ratios, and genetic conflict. Annual Review of Ecology and Systematics, 29, 233-261.
Wolf D.E., Takebayashi N. (2004) Pollen limitation and the evolution of androdioecy from dioecy. The American Naturalist, 163, 122-137.
Wolfe L.M., Shmida A. (1997) The ecology of sex expression in a gynodioecious Israeli desert shrub (Ochradenus baccatus). Ecology, 78, 101-110.
Yamauchi A., Yamagishi T., Booton R., Telschow A., Kudo G. (2019) Theory of coevolution of cytoplasmic male-sterility, nuclear restorer and selfing. Journal of Theoretical Biology, 477, 96-107.
Yang J., Hu L., Wang Z., Zhu W., Meng L. (2014) Responses to drought stress among sex morphs of Oxyria sinensis (Polygonaceae), a subdioecious perennial herb native to the East Himalayas. Ecology and Evolution, 4, 4033-4040.
Zanne A.E., Tank D.C., Cornwell W.K., Eastman L.M., Smith S.A., FitzJohn R.G., … Beaulieu J.M. (2014) Three keys to the radiation of angiosperms into freezing environments. Nature, 506, 89-92.
Zeppel M.J.B., Wilks J.V., Lewis J.D. (2014) Impacts of extreme precipitation and seasonal changes in precipitation on plants. Biogeosciences, 11, 3083-3093.
Zinn K.E., Tunc-Ozdemir M., Harper J.F. (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. Journal of Experimental Botany, 61, 1959-1968.