Eunuchs or Females? Causes and Consequences of Gynodioecy on Morphology, Ploidy, and Ecology of Stellaria graminea L. (Caryophyllaceae)

. 2021 ; 12 () : 589093. [epub] 20210412

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33912199

Plant speciation results from intricate processes such as polyploidization, reproductive strategy shifts and adaptation. These evolutionary processes often co-occur, blurring their respective contributions and interactions in the speciation continuum. Here, relying on a large-scale study, we tested whether gynodioecy triggers the divergent evolution of flower morphology and genome between sexes, and contributes to the establishment of polyploids and colonization of ecological niches in Stellaria graminea. We found that gynodioecy in S. graminea leads to flower morphology divergence between females and hermaphrodites, likely due to sexual selection. Contrary to our expectations, gynodioecy occurs evenly in diploids and tetraploids, suggesting that this reproductive strategy was not involved in the establishment of polyploids. Both diploid and tetraploid females have a larger genome size than hermaphrodites, suggesting the presence of sex chromosomes. Finally, ecology differs between cytotypes and to a lesser extent between sexes, suggesting that the link between environment and presence of females is indirect and likely explained by other aspects of the species' life history. Our study shows that gynodioecy leads to the consistent evolution of sexual traits across a wide range of populations, cytotypes and environments within a given species, and this likely contributes to the phenotypic and genetic distinctiveness of the species from its sister clades.

Zobrazit více v PubMed

Abdusalam A., Tan D., Chang S. M. (2017). Sexual expression and reproductive output in the ephemeral PubMed DOI

Alonso C., Herrera C. M. (2001). Neither vegetative nor reproductive advantages account for high frequency of male-steriles in southern Spanish gynodioecious PubMed DOI

Anderson M., Braak C. T. (2003). Permutation tests for multi-factorial analysis of variance. DOI

Ashman T. L., Kwok A., Husband B. C. (2013). Revisiting the dioecy-polyploidy association: alternate pathways and research opportunities. PubMed DOI

Bachtrog D., Mank J. E., Peichel C. L., Kirkpatrick M., Otto S. P. (2014). Sex determination: why so many ways of doing it? PubMed DOI PMC

Bačovský V., Čegan R., Šimoníková D., Hřibová E., Hobza R. (2020). The formation of sex chromosomes in PubMed DOI PMC

Bailey N. W., Marie-Orleach L., Moore A. J. (2017). Indirect genetic effects in behavioural ecology: does behaviour play a special role in evolution? DOI

Barrett S. C. H. (2002). Evolution of sex: the evolution of plant sexual diversity. PubMed DOI

Barrett S. C. H., Hough J. (2013). Sexual dimorphism in flowering plants. PubMed DOI

Bateman A. J. (1948). Intra-sexual selection in PubMed DOI

Bates D., Maechler M., Bolker B., Walker S. (2015). Fitting linear mixed-effects models using lme4. DOI

Bernasconi G., Antonovics J., Biere A., Charlesworth D., Delph L. F., Filatov D., et al. (2009). Silene as a model system in ecology and evolution. PubMed DOI

Bjornstad O. N. (2019).

Bjornstad O. N., Falck W. (2001). Nonparametric spatial covariance functions: estimation and testing. DOI

Blank C. M., Levin R. A., Miller J. S. (2014). Intraspecific variation in gender strategies in PubMed DOI

Bolker B. M., Brooks M. E., Clark C. J., Geange S. W., Poulsen J. R., Stevens M. H. H., et al. (2009). Generalized linear mixed models: a practical guide for ecology and evolution. PubMed DOI

Buide M. L., Del Valle J. C., Castilla A. R., Narbona E. (2018). Sex expression variation in response to shade in gynodioecious-gynomonoecious species: DOI

Caruso C. M., Case A. L. (2007). Sex ratio variation in gynodioecious PubMed DOI

Caruso C. M., Eisen K., Case A. L. (2016). An angiosperm-wide analysis of the correlates of gynodioecy. DOI

Čertner M., Kúr P., Kolář F., Suda J. (2019). Climatic conditions and human activities shape diploid–tetraploid coexistence at different spatial scales in the common weed DOI

Chalopin D., Volff J.-N., Galiana D., Anderson J. L., Schartl M. (2015). Transposable elements and early evolution of sex chromosomes in fish. PubMed DOI

Charlesworth B., Charlesworth D. (1978). A model for the evolution of dioecy and gynodioecy. DOI

Charlesworth D. (2002). Plant sex determination and sex chromosomes. PubMed DOI

Chater A. O., Heywood V. H. (1993). “Stellaria L,” in

Chinnappa C. C. (1985). Studies in the DOI

Chinnappa C. C., Donald G. M., Sasidharan R., Emery R. J. N. (2005). The biology of DOI

Dalton R., Koski M., Ashman T.-L. (2013). Maternal sex effects and inbreeding depression under varied environmental conditions in gynodioecious PubMed DOI PMC

Dang T. T. T., Chinnappa C. C. (2007). The reproductive biology of DOI

Darwin C. R. (1877).

Delph L. F. (1990). Sex-ratio variation in the gynodioecious shrub PubMed DOI

Delph L. F., Galloway L. F., Stanton M. L. (1996). Sexual dimorphism in flower size. DOI

Delph L. F., Touzet P., Bailey M. F. (2007). Merging theory and mechanism in studies of gynodioecy. PubMed DOI

Desfeux C., Maurice S., Henry J. P., Lejeune B., Gouyon P. H. (1996). Evolution of reproductive systems in the genus Silene. PubMed DOI

Doležel J., Doleželová M., Novák F. J. (1994). Flow cytometric estimation of nuclear DNA amount in diploid bananas ( DOI

Dufay M., Lahiani E., Brachi B. (2010) Gender variation and inbreeding depression in gynodioecious-gynomonoecious Silene nutans (Caryophyllaceae). DOI

Ehrendorfer F. (1980). “Polyploidy and distribution,” in DOI

Fox J., Weisberg S. (2018). Visualizing fit and lack of fit in complex regression models with predictor effect plots and partial residuals. DOI

Frank S. A. (1989). The evolutionary dynamics of cytoplasmic male sterility. DOI

Gadella T. W. J. (1977). Cytotaxonomic studies in

Geber M. A., Dawson T. E., Delph L. F. (1999).

Glick L., Sabath N., Ashman T. L., Goldberg E., Mayrose I. (2016). Polyploidy and sexual system in angiosperms: is there an association? PubMed DOI

Godin G. N. (2020). Distrbution of gynodioecy in flowering plants. [Распространение гинодиэции у цветковых растений]. DOI

Godin V. N., Demyanova E. I. (2013). On the distribution of gynodioecy in flowering plants.

Goldblatt P., Lowry P. P. (2011). The index to plant chromosome numbers (IPCN): three decades of publication by the missouri botanical garden come to an end. DOI

Harmaja H. (1992). A new chromosome number for finnish

Harrison X. A. (2014). Using observation-level random effects to model overdispersion in count data in ecology and evolution. PubMed DOI PMC

Hodálová I., Mered’a P., Jr., Vinikárová A., Grulich V., Rotreklová O. (2010). A new cytotype of DOI

Holmgren P. K., Holmgren N. H., Barnett L. C. (1990).

Horne A. S. (1914). Variability in DOI

Hurdu B., I, Escalante T., Pus̨cas̨ M., Novikoff A., Bartha L., Zimmermann N. E. (2016). Exploring the different facets of plant endemism in the South-Eastern Carpathians: a manifold approach for the determination of biotic elements, centres and areas of endemism. DOI

Käfer J., Marais G. A. B., Pannell J. R. (2017). On the rarity of dioecy in flowering plants. PubMed DOI

Kamath A., Levin R. A., Miller J. S. (2017). Floral size and shape evolution following the transition to gender dimorphism. PubMed DOI

Kliment J., Turis P., Janišová M. (2016). Taxa of vascular plants endemic to the Carpathian Mts.

Kolář F., Četner M., Suda J., Schönswetter P., Husband B. C. (2017). Mixed-ploidy species: progress and opportunities in polyploid research. PubMed DOI

Kolář F., Lučanová M., Záveská E., Fuxová G., Mandáková T., Španiel S., et al. (2016). Ecological segregation does not drive the intricate parapatric distribution of diploid and tetraploid cytotypes of the DOI

Kurepin L. V., Pharis R. P., Emery R. J. N., Reid D. M., Chinnappa C. C. (2015). Phenotypic plasticity of sun and shade ecotypes of PubMed DOI

Kurtto A. (2001). “Caryophyllaceae,” in

Legendre P., Anderson M. J. (1999). Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. DOI

Macdonald S. E., Chinnappa C. C., Reid D. M. (1988). Evolution of phenotypic plasticity in the PubMed DOI

Mártonfi P., Michálek J., Hadinec J., Mártonfiová L., Repčák M. (1999). Hypericum dubium - A new species of the

McCauley D. E., Bailey M. F. (2009). Recent advances in the study of gynodioecy: the interface of theory and empiricism. PubMed DOI PMC

McCullagh P., Nelder J. A. (1989).

Miller J. S., Kamath A., Husband B. C., Levin R. A. (2016). Correlated polymorphism in cytotype and sexual system within a monophyletic species Lycium californicum. PubMed DOI PMC

Miller J. S., Venable D. L. (2000). Polyploidy and the evolution of gender dimorphism in plants. PubMed DOI

Ming R., Wang J., Moore P. H., Paterson A. H. (2007). Sex chromosomes in flowering plants. PubMed DOI

Morton J. K. (2005). “Stellaria,” in

Mráz P., Barabas D., Lengyelová L., Turis P., Schmotzer A., Janišová M., et al. (2016). Vascular plant endemism in the Western Carpathians: Spatial patterns, environmental correlates and taxon traits. DOI

Mulcahy D. L. (1979). The rise of the angiosperms: a genecological factor. PubMed DOI

Murín A. (1960). Substitution of cellophane for glass covers to facilitate preparation of permanent squashes and smears. PubMed

Nakagawa S., Johnson P. C., Schielzeth H. (2017). The coefficient of determination R2 and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. PubMed DOI PMC

Otto S. P. (2007). The evolutionary consequences of polyploidy. PubMed DOI

Ozenda P. (1985).

Pannell J. R., Obbard D. J., Buggs R. J. A. (2004). Polyploidy and the sexual system: what can we learn from DOI

Paterno G. P., Silveira C. L., Kollman J., Westoby M., Fonseca C. R. (2020). The maleness of larger angiosperm flowers. PubMed DOI PMC

Pawłowski B. (1970). Remarques sur l’endéemisme dans la flore des Alpes et des Carpates. DOI

Peterson R., Slovin J. P., Chen C. (2010). A simplified method for differential staining of aborted and non-aborted pollen grains. DOI

Philipp M. (1980). Reproductive biology of Stellaria longipes Goldie as revealed by a cultivation experiment. DOI

Pinheiro J. C., Bates D. M. (2000).

Quinn G. P., Keough M. J. (2002).

R Core Team (2019).

Ramsey J., Schemske D. W. (1998). Pathways, mechanisms, and rates of polyploid formation in flowering plants. DOI

Rao C. R. (1964). The use and interpretation of principal component analysis in applied research.

Renner S. S. (2014). The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. PubMed DOI

Rice A., Glick L., Abadi S., Einhorn M., Kopelman N. M., Salman-Minkov A., et al. (2015). The chromosome counts database (CCDB) – a community resource of plant chromosome numbers. PubMed DOI

Richards A. J. (1997).

Rivkin L. R., Case A. L., Caruso C. M. (2016). Why is gynodioecy a rare but widely distributed sexual system? Lessons from the Lamiaceae. PubMed DOI

Rodríguez-Riaño T., Dafni A. (2007). Pollen-stigma interference in two gynodioecious species of Lamiaceae with intermediate individuals. PubMed DOI PMC

Ruffatto D., Zaya D. N., Molano-Flores B. (2015). Reproductive success of the gynodioecious DOI

Schnable P. S., Wise R. P. (1998). The molecular basis of cytoplasmic male sterility and fertility restoration. DOI

Schönswetter P., Suda J., Popp M., Weiss-Schneeweiss H., Brochmann C. (2007). Circumpolar phylogeography of Juncus biglumis (Juncaceae) inferred from AFLP fingerprints, cpDNA sequences, nuclear DNA content and chromosome numbers. PubMed DOI

Shykoff J. A., Kolokotronis S. O., Collin C. L., López-Villavincencio M. (2003). Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. PubMed DOI

Singmann H., Bolker B., Westfall J., Aust F. (2019).

Slancarova V., Zdanska J., Janousek B., Talianova M., Zschach C., Zluvova J., et al. (2013). Evolution of sex determination systems with heterogametic males and females in Silene. PubMed DOI

Slovák M., Kučera J., Goliašová K. (2012). “Stellaria L,” in

Soltis P. S., Soltis D. E. (2009). The role of hybridization in plant speciation. PubMed DOI

Sonnleitner M., Flatscher R., Escobar Garcıa P., Rauchová J., Suda J., Schneeweiss G. M., et al. (2010). Distribution and habitat segregation on different spatial scales among diploid, tetraploid and hexaploid cytotypes of PubMed DOI PMC

Spigler R. B., Ashman T.-L. (2011). Sex ratio and subdioecy in PubMed DOI

Stephenson A. G., Travers S. E., Mena-Ali J. I., Winsor J. A. (2003). Pollen performance before and during the autotrophic-heterotrophic transition of pollen tube growth. PubMed DOI PMC

Van de Paer C., Saumitou-Laprade P., Vernet P., Billiard S. (2015). The joint evolution and maintenance of self-incompatibility with gynodioecy or androdioecy. PubMed DOI

Van de Peer Y., Maere S., Meyer A. (2009). The evolutionary significance of ancient genome duplications. PubMed DOI

Vaughton G., Ramsey M. (2005). Dry environments promote the establishment of females in monomorphic populations of DOI

Vaughton G., Ramsey M. (2012). Gender plasticity and sexual system stability in Wurmbea. PubMed DOI PMC

Vyskot B., Hobza R. (2015). The genomics of plant sex chromosomes. PubMed DOI

Wang L. L., Zhang Z. Q., Yang Y. P., Duan Y. W. (2019). The coexistence of hermaphroditic and dioecious plants is associated with polyploidy and gender dimorphism in PubMed DOI PMC

Wei N., Cronn R., Liston A., Ashman T. L. (2019). Functional trait divergence and trait plasticity confer polyploid advantage in heterogeneous environments. PubMed DOI PMC

Weiss-Schneeweiss H., Emadzade K., Jang T. S., Schneeweiss G. M. (2013). Evolutionary consequences, constraints and potential of polyploidy in plants. PubMed DOI PMC

Wise R. P., Pring D. R. (2002). Nuclear-mediated mitochondrial gene regulation and male fertility in higher plants: light at the end of the tunnel? PubMed DOI PMC

Yu Q., Navajas-Pérez R., Tong E., Robertson J., Moore P. H. (2008). Recent origin of dioecious and gynodioecious Y chromosomes in papaya. DOI

Zhang D. (2017). A coefficient of determination for generalized linear models. DOI

Zhang D. (2020).

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Reversibility of sex changes in the plant kingdom: more important than we thought?

. 2025 Dec ; 100 (6) : 2199-2216. [epub] 20250601

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...