Traditionally it was thought that fitness-related traits such as male mating frequency, with a history of strong directional selection, should have little additive genetic variance and thus respond asymmetrically to bidirectional artificial selection. However, recent findings and theory suggest that a balance between selection for increased male mating frequency and opposing selection pressures on physiologically linked traits will cause male mating frequency to have high additive genetic variation and hence respond symmetrically to selection. We tested these hypotheses in the stalk-eyed fly, Cyrtodiopsis dalmanni, in which males hold harems comprising many females and so have the opportunity to mate at extremely high frequencies. We subjected male stalk-eyed flies to artificial selection for increased ('high') and decreased ('low') mating frequency in the presence of ecologically realistic, high numbers of females. High line males mated significantly more often than control or low line males. The direct response to selection was approximately symmetric in the high and low lines, revealing high additive genetic variation for, and no significant genetic constraints on, increased male mating frequency in C. dalmanni. In order to investigate trade-offs that might constrain male mating frequency under natural conditions we examined correlated responses to artificial selection. We measured accessory gland length, testis length and eyespan after 7 and 14 generations of selection. High line males had significantly larger accessory glands than low line males. No consistent correlated responses to selection were found in testis length or eyespan. Our results suggest that costs associated with the production and maintenance of large accessory glands, although yet to be identified, are likely to be a major constraint on mating frequency in natural populations of C. dalmanni.
Meiotic drive systems are associated with low-frequency chromosomal inversions. These are expected to accumulate deleterious mutations due to reduced recombination and low effective population size. We test this prediction using the 'sex-ratio' (SR) meiotic drive system of the Malaysian stalk-eyed fly Teleopsis dalmanni. SR is associated with a large inversion (or inversions) on the X chromosome. In particular, we study eyespan in males carrying the SR chromosome, as this trait is a highly exaggerated, sexually dimorphic trait, known to have heightened condition-dependent expression. Larvae were raised in low and high larval food stress environments. SR males showed reduced eyespan under the low and high stress treatments, but there was no evidence of a condition-dependent decrease in eyespan under high stress. Similar but more complex patterns were observed for female eyespan, with evidence of additivity under low stress and heterosis under high stress. These results do not support the hypothesis that reduced sexual ornament size in meiotic drive males is due to a condition-dependent response to the putative increase in mutation load. Instead, reduced eyespan likely reflects compensatory resource allocation to different traits in response to drive-mediated destruction of sperm.
A number of species are affected by Sex-Ratio (SR) meiotic drive, a selfish genetic element located on the X-chromosome that causes dysfunction of Y-bearing sperm. SR is transmitted to up to 100% of offspring, causing extreme sex ratio bias. SR in several species is found in a stable polymorphism at a moderate frequency, suggesting there must be strong frequency-dependent selection resisting its spread. We investigate the effect of SR on female and male egg-to-adult viability in the Malaysian stalk-eyed fly, Teleopsis dalmanni. SR meiotic drive in this species is old, and appears to be broadly stable at a moderate (approx. 20%) frequency. We use large-scale controlled crosses to estimate the strength of selection acting against SR in female and male carriers. We find that SR reduces the egg-to-adult viability of both sexes. In females, homozygous females experience greater reduction in viability (sf = 0.242) and the deleterious effects of SR are additive (h = 0.511). The male deficit in viability (sm = 0.214) is not different from that in homozygous females. The evidence does not support the expectation that deleterious side effects of SR are recessive or sex-limited. We discuss how these reductions in egg-to-adult survival, as well as other forms of selection acting on SR, may maintain the SR polymorphism in this species.
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.