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Divergence patterns of genic copy number variation in natural populations of the house mouse (Mus musculus domesticus) reveal three conserved genes with major population-specific expansions.

ABSTRACT: Copy number variation represents a major source of genetic divergence, yet the evolutionary dynamics of genic copy number variation in natural populations during differentiation and adaptation remain unclear. We applied a read depth approach to genome resequencing data to detect copy number variants (CNVs) ?1 kb in wild-caught mice belonging to four populations of Mus musculus domesticus. We complemented the bioinformatics analyses with experimental validation using droplet digital PCR. The specific focus of our analysis is CNVs that include complete genes, as these CNVs could be expected to contribute most directly to evolutionary divergence. In total, 1863 transcription units appear to be completely encompassed within CNVs in at least one individual when compared to the reference assembly. Further, 179 of these CNVs show population-specific copy number differences, and 325 are subject to complete deletion in multiple individuals. Among the most copy-number variable genes are three highly conserved genes that encode the splicing factor CWC22, the spindle protein SFI1, and the Holliday junction recognition protein HJURP. These genes exhibit population-specific expansion patterns that suggest involvement in local adaptations. We found that genes that overlap with large segmental duplications are generally more copy-number variable. These genes encode proteins that are relevant for environmental and behavioral interactions, such as vomeronasal and olfactory receptors, as well as major urinary proteins and several proteins of unknown function. The overall analysis shows that genic CNVs contribute more to population differentiation in mice than in humans and may promote and speed up population divergence.

SUBMITTER: Pezer Z

PROVIDER: S-EPMC4509996 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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Divergence patterns of genic copy number variation in natural populations of the house mouse (Mus musculus domesticus) reveal three conserved genes with major population-specific expansions.

Pezer Željka Ž Harr Bettina B Teschke Meike M Babiker Hiba H Tautz Diethard D

Genome research 20150706 8

Copy number variation represents a major source of genetic divergence, yet the evolutionary dynamics of genic copy number variation in natural populations during differentiation and adaptation remain unclear. We applied a read depth approach to genome resequencing data to detect copy number variants (CNVs) ≥1 kb in wild-caught mice belonging to four populations of Mus musculus domesticus. We complemented the bioinformatics analyses with experimental validation using droplet digital PCR. The spec ...[more]

PMID: 26149421

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Project description:Copy-number variants (CNVs) may play an important role in early adaptations, potentially facilitating rapid divergence of populations. We describe an approach to study this question by investigating CNVs present in natural populations of mice in the early stages of divergence and their involvement in selective sweeps. We have analyzed individuals from two recently diverged natural populations of the house mouse (Mus musculus domesticus) from Germany and France using custom, high-density, comparative genome hybridization arrays (CGH) that covered almost 164 Mb and 2444 genes. One thousand eight hundred and sixty one of those genes we previously identified as differentially expressed between these populations, while the expression of the remaining genes was invariant. In total, we identified 1868 CNVs across all 10 samples, 200 bp to 600 kb in size and affecting 424 genic regions. Roughly two thirds of all CNVs found were deletions. We found no enrichment of CNVs among the differentially expressed genes between the populations compared to the invariant ones, nor any meaningful correlation between CNVs and gene expression changes. Among the CNV genes, we found cellular component gene ontology categories of the synapse overrepresented among all the 2444 genes tested. To investigate potential adaptive significance of the CNV regions, we selected six that showed large differences in frequency of CNVs between the two populations and analyzed variation in at least two microsatellites surrounding the loci in a sample of 46 unrelated animals from the same populations collected in field trappings. We identified two loci with large differences in microsatellite heterozygosity (Sfi1 and Glo1/Dnahc8 regions) and one locus with low variation across the populations (Cmah), thus suggesting that these genomic regions might have recently undergone selective sweeps. Interestingly, the Glo1 CNV has previously been implicated in anxiety-like behavior in mice, suggesting a differential evolution of a behavioral trait.

Project description:Abstract: Background:Communal nursing in house mice is an example of cooperation where females pool litters in the same nest and indiscriminately nurse own and other offspring despite potential exploitation. The direct fitness benefits associated with communal nursing shown in laboratory studies suggest it to be a selected component of female house mice reproductive behaviour. However, past studies on communal nursing in free-living populations have debated whether it is a consequence of sharing the same nest or an active choice. Here using data from a long-term study of free-living, wild house mice we investigated individual nursing decisions and determined what factors influenced a female's decision to nurse communally. Results:Females chose to nurse solitarily more often than expected by chance, but the likelihood of nursing solitarily decreased when females had more partners available. While finding no influence of pairwise relatedness on partner choice, we observed that females shared their social environment with genetically similar individuals, suggesting a female's home area consisted of related females, possibly facilitating the evolution of cooperation. Within such a home area females were more likely to nest communally when the general relatedness of her available options was relatively high. Females formed communal nests with females that were familiar through previous associations and had young pups of usually less than 5 days old. Conclusions:Our findings suggest that communal nursing was not a by-product of sharing the same nesting sites, but females choose communal nursing partners from a group of genetically similar females, and ultimately the decision may then depend on the pool of options available. Social partner choice proved to be an integrated part of cooperation among females, and might allow females to reduce the conflict over number of offspring in a communal nest and milk investment towards own and other offspring. We suggest that social partner choice may be a general mechanism to stabilize costly cooperation.

Dataset Information

Divergence patterns of genic copy number variation in natural populations of the house mouse (Mus musculus domesticus) reveal three conserved genes with major population-specific expansions.

Publications

Divergence patterns of genic copy number variation in natural populations of the house mouse (Mus musculus domesticus) reveal three conserved genes with major population-specific expansions.

Similar Datasets

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