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

Sperm killing is typically associated with fitness costs that arise from the destruction of wildtype sperm and collateral damage to maturing drive sperm, resulting in poor success under sperm competition. We investigate X-linked meiotic drive fertility in the stalk-eyed fly, Teleopsis dalmanni. Drive male paternity was measured in double mating trials under sperm competition against a wildtype male. Drive males sired the same number of offspring as wildtype males, both when mated first or second. This is the first evidence that drive males can compete equally with non-drive males in double matings, challenging the assumption that drive males inevitably suffer reduced fertility.

The finding is in accord with previous work showing that the number of sperm per ejaculate transferred to females during non-competitive single matings does not differ between drive and wildtype males, which is likely due to the adaptive evolution of enlarged testes in drive males. Future experiments will determine whether the competitive ability of drive males is maintained under higher rates of female remating likely to be experienced in nature.

Introduction

Meiotic drive causes the unequal transmission of genes to the next generation, violating Mendelian laws of segregation (Gershenson, 1928; Sandler & Novitski, 1957). In the extreme, the driver entirely excludes wildtype alleles and is transmitted to all offspring (Searle & de Villena, 2022; Wolf et al., 2022). X-linked drivers are common among Diptera species and lead to dysfunction of Y-bearing sperm and the production of female-only broods (Hurst & Pomiankowski, 1991; James & Jaenike, 1990; Jiggins et al., 1999; Newton et al., 1976; Policansky, 1974; Presgraves et al., 1997). Such a significant transmission advantage could potentially lead to population extinction due to the lack of males (Hamilton, 1967; Hatcher et al., 1999; Mackintosh et al., 2021). However, the fitness costs associated with carrying drive genes often result in negative frequency-dependent selection, which limits their spread (Finnegan et al., 2019; Lindholm et al., 2016).

One factor that strongly impacts the spread of meiotic drive genes is reduced fertility (Zanders & Unckless, 2019). Males with drive not only lose wildtype gametes but typically suffer pleiotropic “collateral damage” that reduces the activity or number of mature drive sperm, leading to poor outcomes, especially under sperm competition (Price & Wedell, 2008). This deficit is likely to be prominent in insects that possess reproductive organs specialized for long-term storage of viable sperm, increasing interactions between ejaculates (Parker, 1970). Evidence from sperm competition studies of X-linked meiotic drive systems in Drosophila species supports this prediction. In Drosophila pseudoobscura, SR drive males sire fewer offspring than standard males in double mating trials (Price et al., 2008a). Drive males have a disproportionally lower success both in their ability to defend against other sperm as the first (P1) male or to displace sperm already in storage as the second (P2) male (Price et al., 2008a). A similar pattern occurs in Drosophila simulans with reduced success in P1 and P2 positions for drive males, and preferential drive male sperm ejection from the female reproductive tract even without competition from the second male’s sperm (Angelard et al., 2008; Atlan et al., 2004). It has been suggested that increased female polyandry evolves to undermine the success of drive sperm and an experimental evolution study in D. pseudoobscura and a double mating experiment in Drosophila recens support this possibility, linking the frequency of drive with the rate of multiple mating (Courret et al., 2019; Dyer & Hall, 2019; Haig & Bergstrom, 1995; Price et al., 2008b; Zeh & Zeh, 1997).

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