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.
Polyandry, female mating with multiple males, is widespread across many taxa and almost ubiquitous in insects. This conflicts with the traditional idea that females are constrained by their comparatively large investment in each offspring, and so should only need to mate once or a few times. Females may need to mate multiply to gain sufficient sperm supplies to maintain their fertility, especially in species in which male promiscuity results in division of their ejaculate among many females. Here, we take a novel approach, utilizing wild‐caught individuals to explore how natural variation among females and males influences fertility gains for females. We studied this in the Malaysian stalk‐eyed fly species Teleopsis dalmanni. After an additional mating, females benefit from greatly increased fertility (proportion fertile eggs). Gains from multiple mating are not uniform across females; they are greatest when females have high fecundity or low fertility. Fertility gains also vary spatially, as we find an additional strong effect of the stream from which females were collected. Responses were unaffected by male mating history (males kept with females or in male‐only groups). Recent male mating may be of lesser importance because males in many species, including T. dalmanni, partition their ejaculate to maintain their fertility over many matings. This study highlights the importance of complementing laboratory studies with data on wild‐caught populations, where there is considerable heterogeneity between individuals. Future research should focus on environmental, demographic and genetic factors that are likely to significantly influence variation in individual female fecundity and fertility.
The sex ratio (SR) X-linked meiotic drive system in stalk-eyed flies destroys Y-bearing sperm. Unlike other SR systems, drive males do not suffer fertility loss. They have greatly enlarged testes which compensate for gamete killing. We predicted that enlarged testes arise from extended development with resources re-allocated from the accessory glands, as these tend to be smaller in drive males. To test this, we tracked the growth of the testes and accessory glands of wild-type and drive males over 5–6 weeks post-eclosion before males attained sexual maturity. Neither of the original predictions is supported by these data. Instead, we found that the drive male testes were enlarged at eclosion, reflecting a greater allocation of resources to the testes during pupation. Testes grow at a higher rate during early adult development in drive males, but there was no evidence that this retards the growth of the accessory glands. Further experiments are proposed to investigate whether smaller accessory glands only arise in drive males post-copulation or when flies are subjected to nutritional stress. Our experimental findings support the idea that enlarged testes in drive males arise as an adaptive allocation of resources to traits that enhance male reproductive success.
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.
The sex-ratio "SR" X-linked meiotic drive system in stalk-eyed flies destroys all Y-bearing sperm. Unlike other SR systems, drive males do not suffer fertility loss. They have greatly enlarged testes, which compensate for gamete killing. We predicted that enlarged testes arise from extended development with resources re-allocated from the accessory glands, as these tend to be smaller in drive males. To test this, we tracked the growth of the testes and accessory glands of wildtype and drive males over 5-6 weeks post-eclosion before males attained sexual maturity. Neither of the original predictions are supported by this data. Instead, we found that the drive-male testes were enlarged at eclosion, reflecting a greater allocation of resources to the testes during pupation. In addition, there was no evidence that the greater allocation of resources to the testes during adult development retarded accessory gland growth. There was evidence of a general trade-off with eyespan, as males with larger relative eyespan had larger accessory glands but smaller testes. These findings support the idea that enlarged testes in drive males arise as an adaptive allocation of resources to traits that enhance male reproductive success.
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