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Genetic potential for changes in breeding systems: Predicted and observed trait changes during artificial selection for male and female allocation in a gynodioecious species

PREMISE: Evolution of separate sexes from hermaphroditism often proceeds through gynodioecy, but genetic constraints on this process are poorly understood. Genetic (co‐)variances and between‐sex genetic correlations were used to predict evolutionary responses of multiple reproductive traits in a sex...

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Autores principales: Campbell, Diane R., Sakai, Ann K., Weller, Stephen G., Culley, Theresa M., Dunbar‐Wallis, Amy K., Andres, Allen M., Wong, Tiffany G., Dang, Tam, Au, Bryan, Ku, Mickey, Marcantonio, Andrea R., Ngo, Paul J., Nguyen, Andrew A., Tran, My Hanh, Tran, Quoc‐Phong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9828115/
https://www.ncbi.nlm.nih.gov/pubmed/36380502
http://dx.doi.org/10.1002/ajb2.16096
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author Campbell, Diane R.
Sakai, Ann K.
Weller, Stephen G.
Culley, Theresa M.
Dunbar‐Wallis, Amy K.
Andres, Allen M.
Wong, Tiffany G.
Dang, Tam
Au, Bryan
Ku, Mickey
Marcantonio, Andrea R.
Ngo, Paul J.
Nguyen, Andrew A.
Tran, My Hanh
Tran, Quoc‐Phong
author_facet Campbell, Diane R.
Sakai, Ann K.
Weller, Stephen G.
Culley, Theresa M.
Dunbar‐Wallis, Amy K.
Andres, Allen M.
Wong, Tiffany G.
Dang, Tam
Au, Bryan
Ku, Mickey
Marcantonio, Andrea R.
Ngo, Paul J.
Nguyen, Andrew A.
Tran, My Hanh
Tran, Quoc‐Phong
author_sort Campbell, Diane R.
collection PubMed
description PREMISE: Evolution of separate sexes from hermaphroditism often proceeds through gynodioecy, but genetic constraints on this process are poorly understood. Genetic (co‐)variances and between‐sex genetic correlations were used to predict evolutionary responses of multiple reproductive traits in a sexually dimorphic gynodioecious species, and predictions were compared with observed responses to artificial selection. METHODS: Schiedea (Caryophyllaceae) is an endemic Hawaiian lineage with hermaphroditic, gynodioecious, subdioecious, and dioecious species. We measured genetic parameters of Schiedea salicaria and used them to predict evolutionary responses of 18 traits in hermaphrodites and females in response to artificial selection for increased male (stamen) biomass in hermaphrodites or increased female (carpel, capsule) biomass in females. Observed responses over two generations were compared with predictions in replicate lines of treatments and controls. RESULTS: In only two generations, both stamen biomass in hermaphrodites and female biomass in females responded markedly to direct selection, supporting a key assumption of models for evolution of dioecy. Other biomass traits, pollen and ovule numbers, and inflorescence characters important in wind pollination evolved indirectly in response to selection on sex allocation. Responses generally followed predictions from multivariate selection models, with some responses unexpectedly large due to increased genetic correlations as selection proceeded. CONCLUSIONS: Results illustrate the power of artificial selection and utility of multivariate selection models incorporating sex differences. They further indicate that pollen and ovule numbers and inflorescence architecture could evolve in response to selection on biomass allocation to male versus female function, producing complex changes in plant phenotype as separate sexes evolve.
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spelling pubmed-98281152023-01-10 Genetic potential for changes in breeding systems: Predicted and observed trait changes during artificial selection for male and female allocation in a gynodioecious species Campbell, Diane R. Sakai, Ann K. Weller, Stephen G. Culley, Theresa M. Dunbar‐Wallis, Amy K. Andres, Allen M. Wong, Tiffany G. Dang, Tam Au, Bryan Ku, Mickey Marcantonio, Andrea R. Ngo, Paul J. Nguyen, Andrew A. Tran, My Hanh Tran, Quoc‐Phong Am J Bot Special Issue Articles PREMISE: Evolution of separate sexes from hermaphroditism often proceeds through gynodioecy, but genetic constraints on this process are poorly understood. Genetic (co‐)variances and between‐sex genetic correlations were used to predict evolutionary responses of multiple reproductive traits in a sexually dimorphic gynodioecious species, and predictions were compared with observed responses to artificial selection. METHODS: Schiedea (Caryophyllaceae) is an endemic Hawaiian lineage with hermaphroditic, gynodioecious, subdioecious, and dioecious species. We measured genetic parameters of Schiedea salicaria and used them to predict evolutionary responses of 18 traits in hermaphrodites and females in response to artificial selection for increased male (stamen) biomass in hermaphrodites or increased female (carpel, capsule) biomass in females. Observed responses over two generations were compared with predictions in replicate lines of treatments and controls. RESULTS: In only two generations, both stamen biomass in hermaphrodites and female biomass in females responded markedly to direct selection, supporting a key assumption of models for evolution of dioecy. Other biomass traits, pollen and ovule numbers, and inflorescence characters important in wind pollination evolved indirectly in response to selection on sex allocation. Responses generally followed predictions from multivariate selection models, with some responses unexpectedly large due to increased genetic correlations as selection proceeded. CONCLUSIONS: Results illustrate the power of artificial selection and utility of multivariate selection models incorporating sex differences. They further indicate that pollen and ovule numbers and inflorescence architecture could evolve in response to selection on biomass allocation to male versus female function, producing complex changes in plant phenotype as separate sexes evolve. John Wiley and Sons Inc. 2022-11-15 2022-11 /pmc/articles/PMC9828115/ /pubmed/36380502 http://dx.doi.org/10.1002/ajb2.16096 Text en © 2022 The Authors. American Journal of Botany published by Wiley Periodicals LLC on behalf of Botanical Society of America. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Special Issue Articles
Campbell, Diane R.
Sakai, Ann K.
Weller, Stephen G.
Culley, Theresa M.
Dunbar‐Wallis, Amy K.
Andres, Allen M.
Wong, Tiffany G.
Dang, Tam
Au, Bryan
Ku, Mickey
Marcantonio, Andrea R.
Ngo, Paul J.
Nguyen, Andrew A.
Tran, My Hanh
Tran, Quoc‐Phong
Genetic potential for changes in breeding systems: Predicted and observed trait changes during artificial selection for male and female allocation in a gynodioecious species
title Genetic potential for changes in breeding systems: Predicted and observed trait changes during artificial selection for male and female allocation in a gynodioecious species
title_full Genetic potential for changes in breeding systems: Predicted and observed trait changes during artificial selection for male and female allocation in a gynodioecious species
title_fullStr Genetic potential for changes in breeding systems: Predicted and observed trait changes during artificial selection for male and female allocation in a gynodioecious species
title_full_unstemmed Genetic potential for changes in breeding systems: Predicted and observed trait changes during artificial selection for male and female allocation in a gynodioecious species
title_short Genetic potential for changes in breeding systems: Predicted and observed trait changes during artificial selection for male and female allocation in a gynodioecious species
title_sort genetic potential for changes in breeding systems: predicted and observed trait changes during artificial selection for male and female allocation in a gynodioecious species
topic Special Issue Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9828115/
https://www.ncbi.nlm.nih.gov/pubmed/36380502
http://dx.doi.org/10.1002/ajb2.16096
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