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Hybridization enables the fixation of selfish queen genotypes in eusocial colonies

A eusocial colony typically consists of two main castes: queens that reproduce and sterile workers that help them. This division of labor, however, is vulnerable to genetic elements that favor the development of their carriers into queens. Several factors, such as intracolonial relatedness, can modu...

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Detalles Bibliográficos
Autores principales: Weyna, Arthur, Romiguier, Jonathan, Mullon, Charles
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8645202/
https://www.ncbi.nlm.nih.gov/pubmed/34917398
http://dx.doi.org/10.1002/evl3.253
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author Weyna, Arthur
Romiguier, Jonathan
Mullon, Charles
author_facet Weyna, Arthur
Romiguier, Jonathan
Mullon, Charles
author_sort Weyna, Arthur
collection PubMed
description A eusocial colony typically consists of two main castes: queens that reproduce and sterile workers that help them. This division of labor, however, is vulnerable to genetic elements that favor the development of their carriers into queens. Several factors, such as intracolonial relatedness, can modulate the spread of such caste‐biasing genotypes. Here we investigate the effects of a notable yet understudied ecological setting: where larvae produced by hybridization develop into sterile workers. Using mathematical modeling, we show that the coevolution of hybridization with caste determination readily triggers an evolutionary arms race between nonhybrid larvae that increasingly develop into queens, and queens that increasingly hybridize to produce workers. Even where hybridization reduces worker function and colony fitness, this race can lead to the loss of developmental plasticity and to genetically hard‐wired caste determination. Overall, our results may help understand the repeated evolution toward remarkable reproductive systems (e.g., social hybridogenesis) observed in several ant species.
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spelling pubmed-86452022021-12-15 Hybridization enables the fixation of selfish queen genotypes in eusocial colonies Weyna, Arthur Romiguier, Jonathan Mullon, Charles Evol Lett Letters A eusocial colony typically consists of two main castes: queens that reproduce and sterile workers that help them. This division of labor, however, is vulnerable to genetic elements that favor the development of their carriers into queens. Several factors, such as intracolonial relatedness, can modulate the spread of such caste‐biasing genotypes. Here we investigate the effects of a notable yet understudied ecological setting: where larvae produced by hybridization develop into sterile workers. Using mathematical modeling, we show that the coevolution of hybridization with caste determination readily triggers an evolutionary arms race between nonhybrid larvae that increasingly develop into queens, and queens that increasingly hybridize to produce workers. Even where hybridization reduces worker function and colony fitness, this race can lead to the loss of developmental plasticity and to genetically hard‐wired caste determination. Overall, our results may help understand the repeated evolution toward remarkable reproductive systems (e.g., social hybridogenesis) observed in several ant species. John Wiley and Sons Inc. 2021-09-16 /pmc/articles/PMC8645202/ /pubmed/34917398 http://dx.doi.org/10.1002/evl3.253 Text en © 2021 The Authors. Evolution Letters published by Wiley Periodicals LLC on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB). https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Letters
Weyna, Arthur
Romiguier, Jonathan
Mullon, Charles
Hybridization enables the fixation of selfish queen genotypes in eusocial colonies
title Hybridization enables the fixation of selfish queen genotypes in eusocial colonies
title_full Hybridization enables the fixation of selfish queen genotypes in eusocial colonies
title_fullStr Hybridization enables the fixation of selfish queen genotypes in eusocial colonies
title_full_unstemmed Hybridization enables the fixation of selfish queen genotypes in eusocial colonies
title_short Hybridization enables the fixation of selfish queen genotypes in eusocial colonies
title_sort hybridization enables the fixation of selfish queen genotypes in eusocial colonies
topic Letters
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8645202/
https://www.ncbi.nlm.nih.gov/pubmed/34917398
http://dx.doi.org/10.1002/evl3.253
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AT romiguierjonathan hybridizationenablesthefixationofselfishqueengenotypesineusocialcolonies
AT mulloncharles hybridizationenablesthefixationofselfishqueengenotypesineusocialcolonies