Abstract
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.
Highlights
Meiotic drive genes are segregation distorters which manipulate the products of gametogenesis so as to bias transmission in their favour (Burt and Trivers 2006; Lindholm et al 2016)
In a second set of experiments, we measured sperm transferred to the ventral receptacle (VR), the site of egg fertilisation
Half the gametes are disabled (Burt and Trivers 2006; Price and Wedell 2008). Whilst this is beneficial to the drive element itself because it excludes non-carrier sperm, in many systems it leads to a reduction in the fertility of drive males (Peacock and Erickson 1965; Jaenike 1996; Atlan et al 2004; Wilkinson et al 2006; Angelard et al 2008; Price et al 2012; Pinzone and Dyer 2013), under conditions of sperm competition (Wilkinson and Fry 2001; Atlan et al 2004; Angelard et al 2008; Price et al 2008)
Summary
Meiotic drive genes are segregation distorters which manipulate the products of gametogenesis so as to bias transmission in their favour (Burt and Trivers 2006; Lindholm et al 2016). Drive males are sub-fertile in the sense that a proportion of the sperm they produce are non-functional and their drivecarrying sperm may be damaged as a by-product of the action of drive (Newton et al 1976; Nasuda et al 1998; Price and Wedell 2008) In both theoretical cases, there is no longer a straightforward expectation that drive males should deliver smaller ejaculates or have lower fertility per copulation. Sperm are transferred and stored in three sclerotised sacs (a singlet and doublet) that make up the spermathecae (Kotrba 1995; Presgraves et al 1999) These are long-term sperm storage organs, and female T. dalmanni continue to lay fertilised eggs for around three weeks after a single mating (Rogers et al 2006). In a final pair of experiments, males were mated sequentially to three females and we examined sperm numbers in the spermathecae, to test whether SR males become sperm depleted sooner than ST males
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