No evidence of mate discrimination against males carrying a sex ratio distorter in Drosophila pseudoobscura

Abstract

Selfish genetic elements (SGEs) that spread by manipulating spermatogenesis often have highly deleterious effects on males that carry them. Females that mate with male carriers of SGEs can also suffer significant costs: they receive fewer and poorer-quality sperm, their offspring will inherit the deleterious allele, and the sex ratio of their offspring will be biased towards the more common sex. To counter these costs, females are therefore expected to prefer to mate with males that do not carry sex ratio distorters or other deleterious selfish genetic elements. However, despite the potential costs, there are few examples of female choice against males carrying SGEs. We searched for evidence of a female preference in fruit fly Drosophila pseudoobscura against males carrying a costly meiotic driving X-chromosome Sex Ratio (SR). In a series of five non-competitive mate preference experiments, we find no evidence that females prefer to mate with non-SR males. Our use of five separate experiments, involving more than 800 females, makes it unlikely that this lack of a difference was due to low power or simple chance. We suggest that the lack of female choice against SGE-carrying males may be due to strong selection on SGEs to be indistinguishable from alternative alleles. Furthermore, polyandry, either in direct response to receiving an ejaculate from an SGE-carrying male or carried out indiscriminately when at risk of mating with carriers, may be an alternative response by females to limit the exposure of their offspring to SGEs.

The consequences of polyandry for population viability, extinction risk and conservation

“…Females in experimental populations containing the selfish genetic element evolved higher levels of polyandry [13], and populations prevented from being polyandrous were more likely to be driven extinct by a shortage of males caused by the spread of the selfish genetic element [80]. Post-copulatory screening against carrier males is especially important because females appear to be unable to distinguish between carrier and non-carrier males prior to mating [107]. Selfish genetic elements that harm male fertility may be common, suggesting a taxonomically widespread benefit of polyandry to population persistence [108].…”

The dynamic relationship between polyandry and selfish genetic elements

“…Frequency-dependent selection maintains this gene as individuals with two copies of Xmrk have reduced viability. However, the majority of cases examining the potential for SGE-based mate choice have failed to find any conclusive evidence, despite severe fitness consequences of not discriminating against SGE-carrying individuals [54,57]. The reason for the general lack of avoidance of SGE-carriers may be the problem of recombination breaking up any association between an ornament and the SGE, and a potential preference allele allowing for SGE-based mate choice to evolve [58].…”

“…In females, SR has no consistent effect. Despite being an ancient drive system of approximately 70 000 years, there is no genetic resistance or suppression of SR drive in D. pseudoobscura [67], and females cannot distinguish male carriers from normal males [57]. Moreover, there is considerable variation in the frequency of SR, which has remained remarkably stable for more than 50 years [68].…”

Sex Chromosome Drive

“…Environmental factors such as climate have long been invoked as a determinant of SR distribution (e.g., in D. pseudoobscura) because several drivers show latitudinal clines in frequency (Sturtevant and Dobzhansky 1936). Temperature-related fertility differences do not seem to impact the distribution of D. pseudoobscura SR (Price et al 2012), although this could explain the high correlation between climate variables and SR frequency in D. neotestacea (Dyer 2012). Moreover, the mechanisms by which ecological variables could influence the maintenance of polymorphism is difficult to determine and may be indirect.…”

“…In the stalk-eyed fly Cyrtodiopsis dalmanni, males show a dimorphism in eye-stalk span that is genetically linked with drive and suppression, and females have evolved preferences for long eye stalks in the presence of SR (Wilkinson et al 1998;Cotton et al 2014). This process appears to be rare (Price et al 2012) and requires the suppression of recombination between meiotic drive and the male sexual character loci (Lande and Wilkinson 1999).…”