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Genetic architecture and sex-specific selection govern modular, male-biased evolution of doublesex.

ABSTRACT: doublesex regulates early embryonic sex differentiation in holometabolous insects, along with the development of species-, sex-, and morph-specific adaptations during pupal stages. How does a highly conserved gene with a critical developmental role also remain functionally dynamic enough to gain ecologically important adaptations that are divergent in sister species? We analyzed patterns of exon-level molecular evolution and protein structural homology of doublesex from 145 species of four insect orders representing 350 million years of divergence. This analysis revealed that evolution of doublesex was governed by a modular architecture: Functional domains and female-specific regions were highly conserved, whereas male-specific sequences and protein structures evolved up to thousand-fold faster, with sites under pervasive and/or episodic positive selection. This pattern of sex bias was reversed in Hymenoptera. Thus, highly conserved yet dynamic master regulators such as doublesex may partition specific conserved and novel functions in different genic modules at deep evolutionary time scales.

SUBMITTER: Baral S

PROVIDER: S-EPMC6506240 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Genetic architecture and sex-specific selection govern modular, male-biased evolution of doublesex.

Baral Saurav S Arumugam Gandhimathi G Deshmukh Riddhi R Kunte Krushnamegh K

Science advances 20190508 5

doublesex regulates early embryonic sex differentiation in holometabolous insects, along with the development of species-, sex-, and morph-specific adaptations during pupal stages. How does a highly conserved gene with a critical developmental role also remain functionally dynamic enough to gain ecologically important adaptations that are divergent in sister species? We analyzed patterns of exon-level molecular evolution and protein structural homology of doublesex from 145 species ...[more]

PMID: 31086812

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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

Genetic architecture and sex-specific selection govern modular, male-biased evolution of doublesex.

Publications

Genetic architecture and sex-specific selection govern modular, male-biased evolution of <i>doublesex</i>.

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