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Contrasting patterns of X-chromosome divergence underlie multiple sex-ratio polymorphisms in stalk-eyed flies.

ABSTRACT: Sex-linked segregation distorters cause offspring sex ratios to differ from equality. Theory predicts that such selfish alleles may either go to fixation and cause extinction, reach a stable polymorphism or initiate an evolutionary arms race with genetic modifiers. The extent to which a sex ratio distorter follows any of these trajectories in nature is poorly known. Here, we used X-linked sequence and simple tandem repeat data for three sympatric species of stalk-eyed flies (Teleopsis whitei and two cryptic species of T. dalmanni) to infer the evolution of distorting X chromosomes. By screening large numbers of field and recently laboratory-bred flies, we found no evidence of males with strongly female-biased sex ratio phenotypes (SR) in one species but high frequencies of SR males in the other two species. In the two species with SR males, we find contrasting patterns of X-chromosome evolution. T. dalmanni-1 shows chromosome-wide differences between sex-ratio (XSR ) and standard (XST ) X chromosomes consistent with a relatively old sex-ratio haplotype based on evidence including genetic divergence, an inversion polymorphism and reduced recombination among XSR chromosomes relative to XST chromosomes. In contrast, we found no evidence of genetic divergence on the X between males with female-biased and nonbiased sex ratios in T. whitei. Taken with previous studies that found evidence of genetic suppression of sex ratio distortion in this clade, our results illustrate that sex ratio modification in these flies is undergoing recurrent evolution with diverse genomic consequences.

SUBMITTER: Paczolt KA

PROVIDER: S-EPMC5585051 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Contrasting patterns of X-chromosome divergence underlie multiple sex-ratio polymorphisms in stalk-eyed flies.

Paczolt K A KA Reinhardt J A JA Wilkinson G S GS

Journal of evolutionary biology 20170804 9

Sex-linked segregation distorters cause offspring sex ratios to differ from equality. Theory predicts that such selfish alleles may either go to fixation and cause extinction, reach a stable polymorphism or initiate an evolutionary arms race with genetic modifiers. The extent to which a sex ratio distorter follows any of these trajectories in nature is poorly known. Here, we used X-linked sequence and simple tandem repeat data for three sympatric species of stalk-eyed flies (Teleopsis whitei and ...[more]

PMID: 28688201

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Project description:Throughout their evolutionary history, genomes acquire new genetic material that facilitates phenotypic innovation and diversification. Developmental processes associated with reproduction are particularly likely to involve novel genes. Abundant gene creation impacts the evolution of chromosomal gene content and general regulatory mechanisms such as dosage compensation. Numerous studies in model organisms have found complex and, at times contradictory, relationships among these genomic attributes highlighting the need to examine these patterns in other systems characterized by abundant sexual selection. Therefore, we examined the association among novel gene creation, tissue-specific gene expression, and chromosomal gene content within stalk-eyed flies. Flies in this family are characterized by strong sexual selection and the presence of a newly evolved X chromosome. We generated RNA-seq transcriptome data from the testes for three species within the family and from seven additional tissues in the highly dimorphic species,Teleopsis dalmanni Analysis of dipteran gene orthology reveals dramatic testes-specific gene creation in stalk-eyed flies, involving numerous gene families that are highly conserved in other insect groups. Identification of X-linked genes for the three species indicates that the X chromosome arose prior to the diversification of the family. The most striking feature of this X chromosome is that it is highly masculinized, containing nearly twice as many testes-specific genes as expected based on its size. All the major processes that may drive differential sex chromosome gene content-creation of genes with male-specific expression, development of male-specific expression from pre-existing genes, and movement of genes with male-specific expression-are elevated on the X chromosome ofT. dalmanni This masculinization occurs despite evidence that testes expressed genes do not achieve the same levels of gene expression on the X chromosome as they do on the autosomes.

Dataset Information

Contrasting patterns of X-chromosome divergence underlie multiple sex-ratio polymorphisms in stalk-eyed flies.

Publications

Contrasting patterns of X-chromosome divergence underlie multiple sex-ratio polymorphisms in stalk-eyed flies.

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