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Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species

Elevated rates of evolution in reproductive proteins are commonly observed in animal species, and are thought to be driven by the action of sexual selection and sexual conflict acting specifically on reproductive traits. Whether similar patterns are broadly observed in other biological groups is equ...

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Autores principales: Moyle, Leonie C., Wu, Meng, Gibson, Matthew J. S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8072272/
https://www.ncbi.nlm.nih.gov/pubmed/33912206
http://dx.doi.org/10.3389/fpls.2021.635990
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author Moyle, Leonie C.
Wu, Meng
Gibson, Matthew J. S.
author_facet Moyle, Leonie C.
Wu, Meng
Gibson, Matthew J. S.
author_sort Moyle, Leonie C.
collection PubMed
description Elevated rates of evolution in reproductive proteins are commonly observed in animal species, and are thought to be driven by the action of sexual selection and sexual conflict acting specifically on reproductive traits. Whether similar patterns are broadly observed in other biological groups is equivocal. Here, we examine patterns of protein divergence among wild tomato species (Solanum section Lycopersicon), to understand forces shaping the evolution of reproductive genes in this diverse, rapidly evolving plant clade. By comparing rates of molecular evolution among loci expressed in reproductive and non-reproductive tissues, our aims were to test if: (a) reproductive-specific loci evolve more rapidly, on average, than non-reproductive loci; (b) ‘male’-specific loci evolve at different rates than ‘female’-specific loci; (c) genes expressed exclusively in gametophytic (haploid) tissue evolve differently from genes expressed in sporophytic (diploid) tissue or in both tissue types; and (d) mating system variation (a potential proxy for the expected strength of sexual selection and/or sexual conflict) affects patterns of protein evolution. We observed elevated evolutionary rates in reproductive proteins. However, this pattern was most evident for female- rather than male-specific loci, both broadly and for individual loci inferred to be positively selected. These elevated rates might be facilitated by greater tissue-specificity of reproductive proteins, as faster rates were also associated with more narrow expression domains. In contrast, we found little evidence that evolutionary rates are consistently different in loci experiencing haploid selection (gametophytic-exclusive loci), or in lineages with quantitatively different mating systems. Overall while reproductive protein evolution is generally elevated in this diverse plant group, some specific patterns of evolution are more complex than those reported in other (largely animal) systems, and include a more prominent role for female-specific loci among adaptively evolving genes.
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spelling pubmed-80722722021-04-27 Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species Moyle, Leonie C. Wu, Meng Gibson, Matthew J. S. Front Plant Sci Plant Science Elevated rates of evolution in reproductive proteins are commonly observed in animal species, and are thought to be driven by the action of sexual selection and sexual conflict acting specifically on reproductive traits. Whether similar patterns are broadly observed in other biological groups is equivocal. Here, we examine patterns of protein divergence among wild tomato species (Solanum section Lycopersicon), to understand forces shaping the evolution of reproductive genes in this diverse, rapidly evolving plant clade. By comparing rates of molecular evolution among loci expressed in reproductive and non-reproductive tissues, our aims were to test if: (a) reproductive-specific loci evolve more rapidly, on average, than non-reproductive loci; (b) ‘male’-specific loci evolve at different rates than ‘female’-specific loci; (c) genes expressed exclusively in gametophytic (haploid) tissue evolve differently from genes expressed in sporophytic (diploid) tissue or in both tissue types; and (d) mating system variation (a potential proxy for the expected strength of sexual selection and/or sexual conflict) affects patterns of protein evolution. We observed elevated evolutionary rates in reproductive proteins. However, this pattern was most evident for female- rather than male-specific loci, both broadly and for individual loci inferred to be positively selected. These elevated rates might be facilitated by greater tissue-specificity of reproductive proteins, as faster rates were also associated with more narrow expression domains. In contrast, we found little evidence that evolutionary rates are consistently different in loci experiencing haploid selection (gametophytic-exclusive loci), or in lineages with quantitatively different mating systems. Overall while reproductive protein evolution is generally elevated in this diverse plant group, some specific patterns of evolution are more complex than those reported in other (largely animal) systems, and include a more prominent role for female-specific loci among adaptively evolving genes. Frontiers Media S.A. 2021-04-12 /pmc/articles/PMC8072272/ /pubmed/33912206 http://dx.doi.org/10.3389/fpls.2021.635990 Text en Copyright © 2021 Moyle, Wu and Gibson. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Moyle, Leonie C.
Wu, Meng
Gibson, Matthew J. S.
Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species
title Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species
title_full Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species
title_fullStr Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species
title_full_unstemmed Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species
title_short Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species
title_sort reproductive proteins evolve faster than non-reproductive proteins among solanum species
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8072272/
https://www.ncbi.nlm.nih.gov/pubmed/33912206
http://dx.doi.org/10.3389/fpls.2021.635990
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