Meiotic drive does not impede success in sperm competition in the stalk-eyed fly, Teleopsis dalmanni

Abstract

In male X-linked meiotic drive systems, the driver causes degeneration of Y-bearing sperm, leading to female-biased offspring sex ratios. This potentially leads to a two-fold transmission advantage to drive chromosomes. However, drive-bearing sperm often do poorly in sperm competition, limiting their ability to spread. We use the stalk-eyed fly, Teleopsis dalmanni, to investigate the success of the X-linked Sex Ratio (SR) meiotic drive system. In this species, polyandrous matings, where a female mates with multiple males, are common. Recent findings demonstrate SR males transfer the same numbers of viable sperm as wildtype (ST) males during mating, implying that they do not necessarily have reduced fertility under sperm competition. Reciprocal mating trials were performed to measure the success of SR and ST sperm in double mated females, with either a SR or ST male mated first followed by a male of the alternative genotype. There was no significant difference in the number of offspring sired by SR and ST males. This equivalence held regardless of whether the SR male mated first or second. We show these results are consistent with previous studies that suggested SR male sperm do poorly in sperm competition. Future experiments will determine whether the competitive ability of SR males is maintained under higher stress conditions likely to be experienced in nature, in which females mate repeatedly with multiple males. The results from the current study helps to explain the high meiotic drive frequency of around 20% in wild populations in this species. Impact SummaryMeiotic drive genes are selfish genetic elements that distort Mendelian patterns of inheritance to bias transmission in their favour. We use the stalk-eyed fly, Teleopsis dalmanni, to investigate the fitness effects associated with a meiotic drive gene called Sex Ratio (SR), which is linked to the X chromosome. In males, SR destroys Y-bearing sperm, meaning only X-bearing sperm are viable, and females who mate with drive males sire all-female broods. This confers a two-fold transmission advantage to the SR gene, as it is transmitted to all offspring. We recently discovered that drive males have evolved compensatory mechanisms to cope with the sperm destruction caused by meiotic drive. They have greatly enlarged testes, allowing them to produce more sperm. When drive males mate with females, they deliver as many sperm and sire as many offspring as wildtype males. Building on this finding, we measured how drive male sperm performs against sperm from a non-carrier male in sperm competition - where the sperm from different males compete to fertilise an egg. Double mating trials were performed, where a single female was mated once to a drive and once to a non-carrier male. By genotyping offspring, we show that the number of offspring sired by the drive male was not different from the number sired by the non-carrier competitor. These findings contrast with those in other species. Typically, drive males do poorly in sperm competition and their spread is severely restricted by sperm competition. In stalk-eyed flies, female multiple mating with many males is the norm, but this does not appear to inhibit the fertility of drive males. The success of drive under sperm competition helps to explain the high frequency of drive around 20% in natural populations of T. dalmanni.