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Polyandry blocks gene drive in a wild house mouse population.

ABSTRACT: Gene drives are genetic elements that manipulate Mendelian inheritance ratios in their favour. Understanding the forces that explain drive frequency in natural populations is a long-standing focus of evolutionary research. Recently, the possibility to create artificial drive constructs to modify pest populations has exacerbated our need to understand how drive spreads in natural populations. Here, we study the impact of polyandry on a well-known gene drive, called t haplotype, in an intensively monitored population of wild house mice. First, we show that house mice are highly polyandrous: 47% of 682 litters were sired by more than one male. Second, we find that drive-carrying males are particularly compromised in sperm competition, resulting in reduced reproductive success. As a result, drive frequency decreased during the 4.5 year observation period. Overall, we provide the first direct evidence that the spread of a gene drive is hampered by reproductive behaviour in a natural population.

SUBMITTER: Manser A

PROVIDER: S-EPMC7643059 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Polyandry blocks gene drive in a wild house mouse population.

Manser Andri A König Barbara B Lindholm Anna K AK

Nature communications 20201104 1

Gene drives are genetic elements that manipulate Mendelian inheritance ratios in their favour. Understanding the forces that explain drive frequency in natural populations is a long-standing focus of evolutionary research. Recently, the possibility to create artificial drive constructs to modify pest populations has exacerbated our need to understand how drive spreads in natural populations. Here, we study the impact of polyandry on a well-known gene drive, called t haplotype, in an intensively ...[more]

PMID: 33149121

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Project description:BACKGROUND: Insights into the micro-evolutionary patterns of morphological traits require an assessment of the natural variation of the trait within and between populations and closely related species. The mouse mandible is a particularly suitable morphological trait for such an analysis, since it has long been used as a model to study the quantitative genetics of shape. In addition, many distinct populations, sub-species and closely related species are known for the house mouse. However, morphological comparisons among wild caught animals require an assessment in how far environmental and technical factors could interfere with the shape change measurements. RESULTS: Using geometric morphometrics, we have surveyed mandible shapes in 15 natural populations of the genus Mus, with a focus on the subspecies Mus musculus domesticus. In parallel we have carefully assessed possibly confounding technical and biological factors. We find that there are distinct differences on average between populations, subspecies and species, but these differences are smaller than differences between individuals within populations. Populations from summer-dry regions, although more ancestral, are less distinct from each other than are populations from the more recently colonized northern areas. Populations with especially distinct shapes occur in an area of sympatry of M. m. domesticus and M. spretus and on recently colonized sub-antarctic islands. We have also studied a number of inbred strains to assess in how far their mandible shapes resemble those from the wild. We find that they fall indeed into the shape space of natural variation between individuals in populations. CONCLUSIONS: Although mandible shapes in natural populations can be influenced by environmental variables, these influences are insufficient to explain the average extent of shape differences between populations, such that evolutionary processes must be invoked to explain this level of diversity. We discuss that adaptive evolution may contribute to shape changes between populations, in particular in newly colonized areas. A comparison between inbred strains and wild mice suggests that the laboratory environment has no major systematic effect on the mandible shape and that such strains can be used as representatives of the natural shape differences between individuals.

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

Polyandry blocks gene drive in a wild house mouse population.

Publications

Polyandry blocks gene drive in a wild house mouse population.

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