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The Recombination Landscape in Wild House Mice Inferred Using Population Genomic Data.

ABSTRACT: Characterizing variation in the rate of recombination across the genome is important for understanding several evolutionary processes. Previous analysis of the recombination landscape in laboratory mice has revealed that the different subspecies have different suites of recombination hotspots. It is unknown, however, whether hotspots identified in laboratory strains reflect the hotspot diversity of natural populations or whether broad-scale variation in the rate of recombination is conserved between subspecies. In this study, we constructed fine-scale recombination rate maps for a natural population of the Eastern house mouse, Mus musculus castaneus We performed simulations to assess the accuracy of recombination rate inference in the presence of phase errors, and we used a novel approach to quantify phase error. The spatial distribution of recombination events is strongly positively correlated between our castaneus map, and a map constructed using inbred lines derived predominantly from M. m. domesticus Recombination hotspots in wild castaneus show little overlap, however, with the locations of double-strand breaks in wild-derived house mouse strains. Finally, we also find that genetic diversity in M. m. castaneus is positively correlated with the rate of recombination, consistent with pervasive natural selection operating in the genome. Our study suggests that recombination rate variation is conserved at broad scales between house mouse subspecies, but it is not strongly conserved at fine scales.

SUBMITTER: Booker TR

PROVIDER: S-EPMC5586380 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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The Recombination Landscape in Wild House Mice Inferred Using Population Genomic Data.

Booker Tom R TR Ness Rob W RW Keightley Peter D PD

Genetics 20170727 1

Characterizing variation in the rate of recombination across the genome is important for understanding several evolutionary processes. Previous analysis of the recombination landscape in laboratory mice has revealed that the different subspecies have different suites of recombination hotspots. It is unknown, however, whether hotspots identified in laboratory strains reflect the hotspot diversity of natural populations or whether broad-scale variation in the rate of recombination is conserved bet ...[more]

PMID: 28751421

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Project description:BackgroundThrough human-aided dispersal over the last ~ 10,000 years, house mice (Mus musculus) have recently colonized diverse habitats across the globe, promoting the emergence of new traits that confer adaptive advantages in distinct environments. Despite their status as the premier mammalian model system, the impact of this demographic and selective history on the global patterning of disease-relevant trait variation in wild mouse populations is poorly understood.ResultsHere, we leveraged 154 whole-genome sequences from diverse wild house mouse populations to survey the geographic organization of functional variation and systematically identify signals of positive selection. We show that a significant proportion of wild mouse variation is private to single populations, including numerous predicted functional alleles. In addition, we report strong signals of positive selection at many genes associated with both complex and Mendelian diseases in humans. Notably, we detect a significant excess of selection signals at disease-associated genes relative to null expectations, pointing to the important role of adaptation in shaping the landscape of functional variation in wild mouse populations. We also uncover strong signals of selection at multiple genes involved in starch digestion, including Mgam and Amy1. We speculate that the successful emergence of the human-mouse commensalism may have been facilitated, in part, by dietary adaptations at these loci. Finally, our work uncovers multiple cryptic structural variants that manifest as putative signals of positive selection, highlighting an important and under-appreciated source of false-positive signals in genome-wide selection scans.ConclusionsOverall, our findings highlight the role of adaptation in shaping wild mouse genetic variation at human disease-associated genes. Our work also highlights the biomedical relevance of wild mouse genetic diversity and underscores the potential for targeted sampling of mice from specific populations as a strategy for developing effective new mouse models of both rare and common human diseases.

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

The Recombination Landscape in Wild House Mice Inferred Using Population Genomic Data.

Publications

The Recombination Landscape in Wild House Mice Inferred Using Population Genomic Data.

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