Polyandry blocks gene drive in a wild house mouse population

Andri Manser,Barbara König,Anna K Lindholm

doi:10.1038/s41467-020-18967-8

Andri Manser, Barbara König + Show 1 more

Open Access

https://doi.org/10.1038/s41467-020-18967-8

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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.

Highlights

Gene drives are genetic elements that manipulate Mendelian inheritance ratios in their favour
We here examined the role of gene drive on sperm competitive ability in a natural population of house mice (Mus musculus domesticus) that harboured a gene drive system called t haplotype
We have elucidated key aspects of the relationship between polyandry and gene drive in a natural population of house mice

Summary

Introduction

Gene drives are genetic elements that manipulate Mendelian inheritance ratios in their favour. Many known natural drive systems manipulate spermatogenesis in males, which typically involves the killing of sperm that do not carry the driver While this selective targeting of non-carrier sperm gives the gene drive advantage against the rival chromosome within a male (causing the drive effect), empirical data collected over the past decade has demonstrated that such sperm killing compromises the sperm competitiveness of drive males in competition against other males. We currently do not know whether these sperm competitive effects are relevant for gene drive systems in a natural context To fill this gap, we here examined the role of gene drive on sperm competitive ability in a natural population of house mice (Mus musculus domesticus) that harboured a gene drive system called t haplotype. A number of studies have further demonstrated that house mice are actively polyandrous both under laboratory and natural conditions[17,18,19,20]

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