Michelle L. Taylor

Attractive males have greater success in sperm competition

Summary While sexual selection is responsible for the rapid evolution of many characters [1,2], the precise relationship between pre- and post-copulatory sexual selection is unclear [3]. In some species, the two are positively associated and reinforce each other, while in others, the two bouts of selection are antagonistic and cancel each other out. Here we assessed the relationship between female preference for males and male fertilization success during sperm competition in the fly Drosophila simulans . We find that attractive males sired more offspring and also find a positive genetic correlation between male attractiveness and siring success.

Polyandry in nature: a global analysis

A popular notion in sexual selection is that females are polyandrous and their offspring are commonly sired by more than a single male. We now have large-scale evidence from natural populations to be able to verify this assumption. Although we concur that polyandry is a generally common and ubiquitous phenomenon, we emphasise that it remains variable. In particular, the persistence of single paternity, both within and between populations, requires more careful consideration. We also explore an intriguing relation of polyandry with latitude. Several recent large-scale analyses of the relations between key population fitness variables, such as heterozygosity, effective population size (Ne), and inbreeding coefficients, make it possible to examine the global effects of polyandry on population fitness for the first time.

Multiple mating increases female fitness in Drosophila simulans

While polyandry is essentially ubiquitous across the animal kingdom, the net fitness consequences of multiple mating remain the subject of much debate. In some taxa the costs of multiple mating outweigh potential benefits, and large direct costs are unlikely to be compensated for by indirect benefits. Nevertheless, direct and indirect benefits potentially provide females with substantial fitness returns, and these are manifest in some species. We investigated some fitness costs and benefits of multiple mating in the fly Drosophila simulans. We compared the longevity and lifetime reproductive success of females with intermittent or continual exposure to males with those of singly mated females housed alone or housed with virgin females. We also compared the same fitness components in females mated once, twice and three times. We found no difference in the lifetime reproductive success of females housed intermittently with males and those housed continually with males, but females in these treatments produced more offspring than singly mated females (housed alone or with virgin females). However, females that were continually exposed to males died younger than females from any other treatment. We also found that females who mated more than once had higher lifetime reproductive success, and that number of matings had no influence on residual longevity. These results contrast somewhat with findings from Drosophila melanogaster, and suggest that while polyandry is beneficial for female D. simulans, male harassment can be costly.

Sexual selection and female fitness in Drosophila simulans

There is a current debate over the net fitness consequences of sexual selection. Do preferred males increase female fitness or are these males manipulating females for their own benefit? The evidence is mixed. Some studies find that mating with attractive males increases female fitness components, while others show that preferred males decrease measures of female fitness. In this study, we examined some of the fitness consequences of pre-copulatory sexual selection in Drosophila simulans. Virgin females were either paired with one male and given an opportunity for one copulation or were exposed simultaneously to two males. This allowed us to compare female preference (copulation latency) and fitness (longevity, lifetime productivity and rate of offspring production) both with and without the influence of male–male competition. When females had access to a single male, neither female longevity, productivity, nor short-term rate of productivity were associated with female preference, and although females mated more quickly with larger males, male size was also not associated with any female fitness measure. Inclusion of male–male competition showed that female longevity was negatively affected by preference, while productivity and rate of productivity was unaffected. This latter experiment also indicated that females preferred larger males, but again, male size was not associated with female fitness. These results indicate that females may not benefit from mating with preferred males, but they may incur survival costs.

Does polyandry control population sex ratio via regulation of a selfish gene

The extent of female multiple mating (polyandry) can strongly impact on the intensity of sexual selection, sexual conflict, and the evolution of cooperation and sociality. More subtly, polyandry may protect populations against intragenomic conflicts that result from the invasion of deleterious selfish genetic elements (SGEs). SGEs commonly impair sperm production, and so are likely to be unsuccessful in sperm competition, potentially reducing their transmission in polyandrous populations. Here, we test this prediction in nature. We demonstrate a heritable latitudinal cline in the degree of polyandry in the fruitfly Drosophila pseudoobscura across the USA, with northern population females remating more frequently in both the field and the laboratory. High remating was associated with low frequency of a sex-ratio-distorting meiotic driver in natural populations. In the laboratory, polyandry directly controls the frequency of the driver by undermining its transmission. Hence we suggest that the cline in polyandry represents an important contributor to the cline in sex ratio in nature. Furthermore, as the meiotic driver causes sex ratio bias, variation in polyandry may ultimately determine population sex ratio across the USA, a dramatic impact of female mating decisions. As SGEs are ubiquitous it is likely that the reduction of intragenomic conflict by polyandry is widespread.

Attractive males do not sire superior daughters

Much of the recent work on the evolution of female choice has focused on the relative influence of direct and indirect benefits, and particularly whether direct costs can be offset by indirect benefits. Studies investigating whether attractive males benefit females by increasing the viability of their offspring often report mating advantages to sons consistent with the Fisher process, while detecting no or weak viability benefits. One potential reason for this is that sons may trade-off viability benefits with investment in costly traits that enhance mating success, leading to the suggestion that viability benefits may be better detected by examining daughters’ fitness. Here we investigate the relationship between male attractiveness and daughters’ fitness in Drosophila simulans. We measured daughter (and dam) lifetime reproductive success and longevity. We found no evidence that attractive males sire high fitness daughters. Additionally, neither daughters nor dams gained direct benefits from mating with attractive males. However, aspects of daughters’ fitness were related to dam characters.

No Evidence for Heritability of Male Mating Latency or Copulation Duration across Social Environments in Drosophila melanogaster

A key assumption underpinning major models of sexual selection is the expectation that male sexual attractiveness is heritable. Surprisingly, however, empirical tests of this assumption are relatively scarce. Here we use a paternal full-sib/half-sib breeding design to examine genetic and environmental variation in male mating latency (a proxy for sexual attractiveness) and copulation duration in a natural population of Drosophila melanogaster. As our experimental design also involved the manipulation of the social environment within each full-sibling family, we were able to further test for the presence of genotype-by-environment interactions (GEIs) in these traits, which have the potential to compromise mate choice for genetic benefits. Our experimental manipulation of the social environment revealed plastic expression of both traits; males exposed to a rival male during the sensitive period of adult sexual maturation exhibited shorter mating latencies and longer copulation durations than those who matured in isolation. However, we found no evidence for GEIs, and no significant additive genetic variation underlying these traits in either environment. These results undermine the notion that the evolution of female choice rests on covariance between female preference and male displays, an expectation that underpins indirect benefit models such as the good genes and sexy sons hypotheses. However, our results may also indicate depletion of genetic variance in these traits in the natural population studied, thus supporting the expectation that traits closely aligned with reproductive fitness can exhibit low levels of additive genetic variance.

Opposite environmental and genetic influences on body size in North American Drosophila pseudoobscura

BackgroundPopulations of a species often differ in key traits. However, it is rarely known whether these differences are associated with genetic variation and evolved differences between populations, or are instead simply a plastic response to environmental differences experienced by the populations. Here we examine the interplay of plasticity and direct genetic control by investigating temperature-size relationships in populations of Drosophila pseudoobscura from North America. We used 27 isolines from three populations and exposed them to four temperature regimes (16°C, 20°C, 23°C, 26°C) to examine environmental, genetic and genotype-by-environment sources of variance in wing size.ResultsBy far the largest contribution to variation in wing size came from rearing temperature, with the largest flies emerging from the coolest temperatures. However, we also found a genetic signature that was counter to this pattern as flies originating from the northern, cooler population were consistently smaller than conspecifics from more southern, warmer populations when reared under the same laboratory conditions.ConclusionsWe conclude that local selection on body size appears to be acting counter to the environmental effect of temperature. We find no evidence that local adaptation in phenotypic plasticity can explain this result, and suggest indirect selection on traits closely linked with body size, or patterns of chromosome inversion may instead be driving this relationship.

Sexual selection in flies: a comparison of Drosophila simulans and D. melanogaster

The traditional view of sexual selection via female mate choice is that female preference for certain males either has no net fitness cost or is beneficial to overall female fitness. A more contemporary view is that preferred males can at times reduce female fitness. This view has arisen from the realisation that conflict between the sexes is an inevitable feature of sexual reproduction, as each sex necessarily has a different agenda for maximizing fitness. Despite the hailing of sexual conflict as a paradigm shift and its prevalence in the recent sexual selection literature, compelling evidence that attractive males reduce female fitness remains taxonomically restricted. Here we review the findings of a series of investigations into the fitness consequences of female preference in the fly Drosophila simulans and compare them with its sibling species, D. melanogaster. We show that there are stark differences in the fitness consequences of mating with preferred males in the two species and discuss this contrast with reference to the current debates in the sexual selection literature.

Winter is coming: hibernation reverses the outcome of sperm competition in a fly

Sperm commonly compete within females to fertilize ova, but research has focused on short‐term sperm storage: sperm that are maintained in a female for only a few days or weeks before use. In nature, females of many species store sperm for months or years, often during periods of environmental stress, such as cold winters. Here we examine the outcome of sperm competition in the fruit fly Drosophila pseudoobscura, simulating the conditions in which females survive winter. We mated females to two males and then stored the female for up to 120 days at 4°C. We found that the outcome of sperm competition was consistent when sperm from two males was stored for 0, 1 or 30 days, with the last male to mate fathering most of the offspring. However, when females were stored in the cold for 120 days, the last male to mate fathered less than 5% of the offspring. Moreover, when sperm were stored long term the first male fathered almost all offspring even when he carried a meiotic driving sex chromosome that drastically reduces sperm competitive success under short‐term storage conditions. This suggests that long‐term sperm storage can radically alter the outcome of sperm competition.