Detrimental effects of an autosomal selfish genetic element on sperm competitiveness in house mice

Abstract

Female multiple mating (polyandry) is widespread across many animal taxa and indirect genetic benefits are a major evolutionary force favouring polyandry. An incentive for polyandry arises when multiple mating leads to sperm competition that disadvantages sperm from genetically inferior mates. A reduction in genetic quality is associated with costly selfish genetic elements (SGEs), and studies in invertebrates have shown that males bearing sex ratio distorting SGEs are worse sperm competitors than wild-type males.We used a vertebrate model species to test whether females can avoid an autosomal SGE, the t haplotype, through polyandry. The t haplotype inhouse mice exhibits strong drive in t heterozygous males by affecting spermatogenesis and is associated with homozygous in utero lethality. We used controlled matings to test the effect of the t haplotype on sperm competitiveness. Regardless of mating order, t heterozygous males sired only 11% of zygotes when competing against wild-type males, suggesting a very strong effect of the t haplotype on sperm quality. We provide, to our knowledge,the first substantial evidence that polyandry ameliorates the harmful effects of an autosomal SGE arising through genetic incompatibility. We discuss potential mechanisms in our study species and the broader implications for the benefits of polyandry.

Figure 1.

Paternity share of +/t males in sperm competition with +/+ males. Shown are overall paternity share (left chart) and paternity share as a function of the number of ejaculations (right chart). The surface area of grey circles is proportional to the number of observations. Colours of circles represent mating order, with dark grey for trials in which the +/t male was first to mate. Mating order did not have a significant effect on paternity share when accounting for the number of ejaculations and is included for illustrational purposes only. Squares and bars represent mean and approximate 95% confidence interval estimates. The grey dotted line shows equal paternity share for +/+ and +/t males and the grey solid line represents the prediction based on a numerical reduction in functional sperm through drive (see main text). (Online version in colour.)

Figure 2.

+/t paternity share in polyandrous and monandrous females (bottom chart) and consequences for embryo viability (top chart). Monandrous females were mated to either a +/t or a +/+ male (+/t male paternity share 1 and 0, respectively), whereas polyandrous females mated with both a +/t and a +/+ male. Colours and shapes indicate female genotype (+/+ in lighter grey diamonds, +/t in darker grey circles). The surface area of diamonds and circles is proportional to the number of observations. Mean and approximate 95% confidence interval estimates are indicated by points and bars (bottom chart) and lines and shaded areas (top chart), respectively. (Online version in colour.)