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Faster-X adaptive protein evolution in house mice.

ABSTRACT: The causes of the large effect of the X chromosome in reproductive isolation and speciation have long been debated. The faster-X hypothesis predicts that X-linked loci are expected to have higher rates of adaptive evolution than autosomal loci if new beneficial mutations are on average recessive. Reproductive isolation should therefore evolve faster when contributing loci are located on the X chromosome. In this study, we have analyzed genome-wide nucleotide polymorphism data from the house mouse subspecies Mus musculus castaneus and nucleotide divergence from Mus famulus and Rattus norvegicus to compare rates of adaptive evolution for autosomal and X-linked protein-coding genes. We found significantly faster adaptive evolution for X-linked loci, particularly for genes with expression in male-specific tissues, but autosomal and X-linked genes with expression in female-specific tissues evolve at similar rates. We also estimated rates of adaptive evolution for genes expressed during spermatogenesis and found that X-linked genes that escape meiotic sex chromosome inactivation (MSCI) show rapid adaptive evolution. Our results suggest that faster-X adaptive evolution is either due to net recessivity of new advantageous mutations or due to a special gene content of the X chromosome, which regulates male function and spermatogenesis. We discuss how our results help to explain the large effect of the X chromosome in speciation.

SUBMITTER: Kousathanas A

PROVIDER: S-EPMC3982706 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

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Faster-X adaptive protein evolution in house mice.

Kousathanas Athanasios A Halligan Daniel L DL Keightley Peter D PD

Genetics 20131220 4

The causes of the large effect of the X chromosome in reproductive isolation and speciation have long been debated. The faster-X hypothesis predicts that X-linked loci are expected to have higher rates of adaptive evolution than autosomal loci if new beneficial mutations are on average recessive. Reproductive isolation should therefore evolve faster when contributing loci are located on the X chromosome. In this study, we have analyzed genome-wide nucleotide polymorphism data from the house mous ...[more]

PMID: 24361937

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Project description:Changes in gene regulation have long been appreciated as a driving force of adaptive evolution, however the relative contributions of cis- and trans-acting changes to gene regulation over short evolutionary timescales remain unclear. Instances of recent, parallel phenotypic evolution provide an opportunity to assess whether parallel patterns are seen at the level of gene expression, and to assess the relative contribution of cis- and trans- changes to gene regulation in the early stages of divergence. Here, we studied gene expression in liver and brown adipose tissue in two wild-derived strains of house mice that independently adapted to cold, northern environments, and we compared them to a strain of house mice from a warm, tropical environment. To investigate gene regulatory evolution, we studied expression in parents and allele-specific expression in F1 hybrids of crosses between warm-adapted and cold-adapted strains. First, we found that the different cold-adapted mice showed both unique and shared changes in expression, but that the proportion of shared changes (i.e. parallelism) was greater than expected by chance. Second, we discovered that expression evolution occurred largely at tissue-specific and cis-regulated genes, and that these genes were over-represented in parallel cases of evolution. Finally, we integrated the expression data with scans for selection in natural populations and found substantial parallelism in the two northern populations for genes under selection. Furthermore, selection outliers were associated with cis-regulated genes more than expected by chance; cis-regulated genes under selection influenced phenotypes such as body size, immune functioning, and activity level. These results demonstrate that parallel patterns of gene expression in mice that have independently adapted to cold environments are driven largely by tissue-specific and cis-regulatory changes, providing insight into the mechanisms of adaptive gene regulatory evolution at the earliest stages of divergence.

Dataset Information

Faster-X adaptive protein evolution in house mice.

Publications

Faster-X adaptive protein evolution in house mice.

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