Meiotic drive genes cause the degeneration of non-carrier sperm to bias transmission in their favour. Males carrying meiotic drive are expected to suffer reduced fertility due to the loss of sperm and associated harmful side-effects of the mechanisms causing segregation distortion. However, sexual selection should promote adaptive compensation to overcome these deleterious effects. We investigate this using SR, an X-linked meiotic drive system in the stalk-eyed fly, Teleopsis dalmanni. Despite sperm destruction caused by drive, we find no evidence that SR males transfer fewer sperm to the female’s spermathecae (long-term storage organs). Likewise, migration from the spermathecae to the ventral receptacle for fertilisation is similar for SR and wildtype male sperm, both over short and long time-frames. In addition, sperm number in storage is similar even after males have mated multiple times. Our study challenges conventional assumptions about the deleterious effects of drive on male fertility. This suggests that SR male ejaculate investment per ejaculate has been adjusted to match sperm delivery by wildtype males. We interpret these results in the light of recent theoretical models that predict how ejaculate strategies evolve when males vary in the resources allocated to reproduction or in sperm fertility. Adaptive compensation is likely in species where meiotic drive has persisted over many generations and predicts a higher stable frequency of drive maintained in wild populations. Future research must determine exactly how drive males compensate for failed spermatogenesis, and how such compensation may trade-off with investment in other fitness traits.

1718 Selfish genetic elements that gain a transmission advantage through the destruction of 19 sperm have grave implications for drive male fertility. We report the first evidence for a 20 male adaptation to this negative consequence of unsuppressed drive. In the X-linked SR 21 meiotic drive system of a stalk-eyed fly, we found that drive males had greatly enlarged 22 testes and so maintained high fertility despite the destruction of half their sperm. This was 23 the case even when males were challenged with fertilising five females. Conversely, we 24 observed an overt trade-off with mating frequency due to reduced allocation of resources 25 to accessory glands. Body size and eyespan were also reduced, which are likely to impair 26 viability, pre-copulatory competition and mating frequency. Gaining an understanding of 27 the extent to which drivers promote the evolution of adaptive responses in the host is 28 essential for predictions of equilibrium frequencies in wild populations. 29

Selfish genetic elements that gain a transmission advantage through the destruction of sperm have grave implications for drive male fertility. In the X-linked SR meiotic drive system of a stalk-eyed fly, we found that drive males have greatly enlarged testes and maintain high fertility despite the destruction of half their sperm, even when challenged with fertilising large numbers of females. Conversely, we observed reduced allocation of resources to the accessory glands that probably explains the lower mating frequency of SR males. Body size and eyespan were also reduced, which are likely to impair viability and precopulatory success. We discuss the potential evolutionary causes of these differences between drive and standard males.