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Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast-Z effect in Heliconius.

ABSTRACT: Sex chromosomes have different evolutionary properties compared to autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution for a group of butterflies. First, we improve the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then, we analyse RNA from male and female whole abdomens and sequence female ovary and gut tissue to identify sex- and tissue-specific gene expression profiles in H. melpomene. Using these expression profiles, we compare (a) sequence divergence and polymorphism; (b) the strength of positive and negative selection; and (c) rates of adaptive evolution, for Z and autosomal genes between two species of Heliconius butterflies, H. melpomene and H. erato. We show that the rate of adaptive substitutions is higher for Z than autosomal genes, but contrary to expectation, it is also higher for male-biased than female-biased genes. Additionally, we find no significant increase in the rate of adaptive evolution or purifying selection on genes expressed in ovary tissue, a heterogametic-specific tissue. Our results contribute to a growing body of literature from other ZW systems that also provide mixed evidence for a fast-Z effect where hemizygosity influences the rate of adaptive substitutions.

SUBMITTER: Pinharanda A

PROVIDER: S-EPMC6850379 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast-Z effect in Heliconius.

Pinharanda Ana A Rousselle Marjolaine M Martin Simon H SH Hanly Joe J JJ Davey John W JW Kumar Sujai S Galtier Nicolas N Jiggins Chris D CD

Journal of evolutionary biology 20190111 3

Sex chromosomes have different evolutionary properties compared to autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution for a group of butterflies. First, we improve the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then, we analyse RNA ...[more]

PMID: 30523653

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Project description:Sexually dimorphic traits are by definition exaggerated in one sex, which may arise from a history of sex-specific selection â in males, females, or both. If this exaggeration comes at a cost, exaggeration is expected to be greater in higher condition individuals (condition-dependent). Although studies using small numbers of morphological traits are generally supportive, this prediction has not been examined at a larger scale. We test this prediction across the trancriptome by determining the condition-dependence of sex-biased (dimorphic) gene expression. We find that high-condition populations are more sexually dimorphic in transcription than low-condition populations. High condition populations have more male-biased genes and more female-biased genes, and a greater degree of sexually dimorphic expression in these genes. Also, condition-dependence in male-biased genes was greater than in a set of unbiased genes. Interestingly, male-biased genes expressed in the testes were not more condition-dependent than those in the soma. By contrast, increased female-biased expression under high condition may be have occurred because of the greater contribution of the ovary-specific transcripts to the entire mRNA pool. We did not find any genomic signatures distinguishing the condition-dependent sex-biased genes. The degree of condition-dependent sexual dimorphism (CDSD) did not differ between the autosomes and the X-chromosome. There was only weak evidence that rates of evolution correlated with CDSD. We suggest that the sensitivity of both female-biased genes and male-biased genes to condition may be akin to the overall heightened sensitivity to condition that life-history and sexually selected traits tend to exhibit. Our results demonstrate that through condition-dependence, early life experience has dramatic effects on sexual dimorphism in the adult transcriptome. There were 8 biologically distinct samples. Each was replicated 6 times for a total of 48 biological samples on 24 arrays. There was no reference or control sample as a loop design was used. Each of the 48 samples are represented separately.

Dataset Information

Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast-Z effect in Heliconius.

Publications

Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast-Z effect in Heliconius.

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