Social Organization Is Associated With Relaxed Selection on Worker Genes in Highly Polygyne Ants

ABSTRACT Ants display a diversity of social structures reflected by differences in caste, nest, and colony organization. Previous research has shown that highly eusocial insects (Hymenoptera) exhibit genome‐wide signatures of relaxed selection due to their smaller effective population sizes. However...

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Main Authors: Kailey Ferger, Neil D. Tsutsui
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.71696
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author Kailey Ferger
Neil D. Tsutsui
author_facet Kailey Ferger
Neil D. Tsutsui
author_sort Kailey Ferger
collection DOAJ
description ABSTRACT Ants display a diversity of social structures reflected by differences in caste, nest, and colony organization. Previous research has shown that highly eusocial insects (Hymenoptera) exhibit genome‐wide signatures of relaxed selection due to their smaller effective population sizes. However, it is unknown how the colony structure itself may shape the evolution of eusocial species through its effects on the worker caste. Worker ants are typically sterile or produce only male offspring, so traits affecting their behavior evolve mainly through kin selection. Kin selection is predicted to be strongest when relatedness within the colony is high, as in species with a single queen per colony (monogyne). In these cases, the reproductive individuals who are the recipients of worker helping behavior are more likely to carry the same allele for that behavior, with probability proportional to relatedness between worker and reproductive. In contrast, in species with multiple queens and lower relatedness, like weakly or highly polygyne ants, there is a higher chance that altruistic behavior benefits non‐relatives. These colony structures are predicted to weaken kin selection, leading to more relaxed selection on worker‐biased genes. We find some evidence in highly polygyne species that genes with worker‐biased expression experience more relaxed selection compared to queen‐biased or non‐differentially expressed genes. However, this pattern does not appear to hold consistently across species with lower or more variable queen numbers, where the degree of relaxed selection in worker genes shows no clear association with average queen number per nest. This may point to possible compensatory mechanisms present in these contexts to counteract relaxed selection in workers or that these predicted patterns are too subtle to be detected with current methods, highlighting areas of future study.
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spelling doaj-art-07fc6af66bf8489696d909f1d01e339e2025-08-20T03:08:40ZengWileyEcology and Evolution2045-77582025-07-01157n/an/a10.1002/ece3.71696Social Organization Is Associated With Relaxed Selection on Worker Genes in Highly Polygyne AntsKailey Ferger0Neil D. Tsutsui1Center for Computational Biology University of California Berkeley California USADepartment of Environmental Science, Policy, & Management University of California Berkeley California USAABSTRACT Ants display a diversity of social structures reflected by differences in caste, nest, and colony organization. Previous research has shown that highly eusocial insects (Hymenoptera) exhibit genome‐wide signatures of relaxed selection due to their smaller effective population sizes. However, it is unknown how the colony structure itself may shape the evolution of eusocial species through its effects on the worker caste. Worker ants are typically sterile or produce only male offspring, so traits affecting their behavior evolve mainly through kin selection. Kin selection is predicted to be strongest when relatedness within the colony is high, as in species with a single queen per colony (monogyne). In these cases, the reproductive individuals who are the recipients of worker helping behavior are more likely to carry the same allele for that behavior, with probability proportional to relatedness between worker and reproductive. In contrast, in species with multiple queens and lower relatedness, like weakly or highly polygyne ants, there is a higher chance that altruistic behavior benefits non‐relatives. These colony structures are predicted to weaken kin selection, leading to more relaxed selection on worker‐biased genes. We find some evidence in highly polygyne species that genes with worker‐biased expression experience more relaxed selection compared to queen‐biased or non‐differentially expressed genes. However, this pattern does not appear to hold consistently across species with lower or more variable queen numbers, where the degree of relaxed selection in worker genes shows no clear association with average queen number per nest. This may point to possible compensatory mechanisms present in these contexts to counteract relaxed selection in workers or that these predicted patterns are too subtle to be detected with current methods, highlighting areas of future study.https://doi.org/10.1002/ece3.71696comparative genomicskin selectionrelaxed selectionsocial evolutionworker caste
spellingShingle Kailey Ferger
Neil D. Tsutsui
Social Organization Is Associated With Relaxed Selection on Worker Genes in Highly Polygyne Ants
Ecology and Evolution
comparative genomics
kin selection
relaxed selection
social evolution
worker caste
title Social Organization Is Associated With Relaxed Selection on Worker Genes in Highly Polygyne Ants
title_full Social Organization Is Associated With Relaxed Selection on Worker Genes in Highly Polygyne Ants
title_fullStr Social Organization Is Associated With Relaxed Selection on Worker Genes in Highly Polygyne Ants
title_full_unstemmed Social Organization Is Associated With Relaxed Selection on Worker Genes in Highly Polygyne Ants
title_short Social Organization Is Associated With Relaxed Selection on Worker Genes in Highly Polygyne Ants
title_sort social organization is associated with relaxed selection on worker genes in highly polygyne ants
topic comparative genomics
kin selection
relaxed selection
social evolution
worker caste
url https://doi.org/10.1002/ece3.71696
work_keys_str_mv AT kaileyferger socialorganizationisassociatedwithrelaxedselectiononworkergenesinhighlypolygyneants
AT neildtsutsui socialorganizationisassociatedwithrelaxedselectiononworkergenesinhighlypolygyneants