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Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait.

ABSTRACT: Theory shows how sexual selection can exaggerate male traits beyond naturally selected optima and also how natural selection can ultimately halt trait elaboration. Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. Here we use experimental evolution of replicate populations of broad-horned flour beetles to test for effects of sex-specific predation on an exaggerated sexually selected male trait (the mandibles), while also testing for effects on female lifetime reproductive success. We find that populations subjected to male-specific predation evolve smaller sexually selected mandibles and this indirectly increases female fitness, seemingly through intersexual genetic correlations we document. Predation solely on females has no effects. Our findings support fundamental theory, but also reveal unforseen outcomes-the indirect effect on females-when natural selection targets sex-limited sexually selected characters.

SUBMITTER: Okada K

PROVIDER: S-EPMC8187464 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait.

Okada Kensuke K Katsuki Masako M Sharma Manmohan D MD Kiyose Katsuya K Seko Tomokazu T Okada Yasukazu Y Wilson Alastair J AJ Hosken David J DJ

Nature communications 20210608 1

Theory shows how sexual selection can exaggerate male traits beyond naturally selected optima and also how natural selection can ultimately halt trait elaboration. Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. Here we use experimental evolution of replicate populations of broad-horned flour beetles to test for effects of sex-spec ...[more]

PMID: 34103535

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Project description:BackgroundExaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of exaggerated secondary sexual phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the limited availability of representative genomes and associated tissue and sex transcriptomes to study the development of these traits. Here we present the genome and developmental transcriptomes, focused on the legs, of the water strider Microvelia longipes, a species where males exhibit strikingly long third legs compared to females, which they use as weapons.ResultsWe generated a high-quality genome assembly with 90% of the sequence captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in both sex-biased and leg-biased genes, indicating a specific signature of gene expression in association with trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. By contrast to male-biased genes, female-biased genes that are expressed in the third legs, but not the other legs, are over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed also that they arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration.ConclusionOur findings indicate how directional sexual selection may drive sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.

Dataset Information

Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait.

Publications

Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait.

Similar Datasets

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