Nina Wedell

Sperm competition, male prudence and sperm-limited females

Sperm are produced in astronomical numbers compared with eggs, and there is good evidence that sperm competition is the force behind the evolution of many tiny sperm. However, sperm production inevitably has costs. Recent research shows that male ejaculate expenditure is dynamic in both time and space, and that males are sensitive to risks of sperm competition and can vary ejaculate size accordingly. We focus on studies showing that males assess mating status and relative fecundity of females, and reveal that modulation of ejaculate investment by males can sometimes result in sperm limitation for females.

Genetic compatibility, mate choice and patterns of parentage: invited review.

There is growing interest in the possibility that genetic compatibility may drive mate choice, including gamete choice, particularly from the perspective of understanding why females frequently mate with more than one male. Mate choice for compatibility differs from other forms of choice for genetic benefits (such as ‘good genes’) because individuals are expected to differ in their mate preferences, changing the evolutionary dynamics of sexual selection. Recent experiments designed to investigate genetic benefits of polyandry suggest that mate choice on the basis of genetic compatibility may be widespread. However, in most systems the mechanisms responsible for variation in compatibility are unknown. We review potential sources of variation in genetic compatibility and whether there is any evidence for mate choice driven by these factors. Selfish genetic elements appear to have the potential to drive mate compatibility mate choice, though as yet there is only one convincing example. There is abundant evidence for assortative mating between populations in hybrid zones, but very few examples where this is clearly a result of selection against mating with genetically less compatible individuals. There are also numerous cases of inbreeding avoidance, but little evidence that mate choice or differential fertilization success driven by genetic compatibility occurs between unrelated individuals. The exceptions to this are a handful of situations where both the alleles causing incompatibility and the alleles involved in mate choice are located in a chromosome region where recombination is suppressed. As yet there are only a few potential sources of genetic compatibility which have clearly been shown to drive mate choice. This may reflect limitations in the potential for the evolution of mate choice for genetic compatibility within populations, although the most promising sources of such incompatibilities have received relatively little research.

Polyandrous females avoid costs of inbreeding

Why do females typically mate with more than one male? Female mating patterns have broad implications for sexual selection, speciation and conflicts of interest between the sexes, and yet they are poorly understood. Matings inevitably have costs, and for females, the benefits of taking more than one mate are rarely obvious. One possible explanation is that females gain benefits because they can avoid using sperm from genetically incompatible males, or invest less in the offspring of such males. It has been shown that mating with more than one male can increase offspring viability, but we present the first clear demonstration that this occurs because females with several mates avoid the negative effects of genetic incompatibility. We show that in crickets, the eggs of females that mate only with siblings have decreased hatching success. However, if females mate with both a sibling and a non-sibling they avoid altogether the low egg viability associated with sibling matings. If similar effects occur in other species, inbreeding avoidance may be important in understanding the prevalence of multiple mating.

BENEFITS OF MULTIPLE MATES IN THE CRICKET GRYLLUS BIMACULATUS

Despite the importance of polyandry for sexual selection, the reasons why females frequently mate with several males remain poorly understood. A number of genetic benefits have been proposed, based on the idea that by taking multiple mates, females increase the likelihood that their offspring will be sired by genetically more compatible or superior males. If certain males have intrinsically “good genes,” any female mating with them will produce superior offspring. Alternatively, if some males have genetic elements that are incompatible with a particular female, then she may benefit from polyandry if the sperm of such males are less likely to fertilize her eggs. We examined these hypotheses in the field cricket Gryllus bimaculatus (Orthoptera: Gryllidae). By allocating females identical numbers of matings but different numbers of mates we investigated the influence of number of mates on female fecundity, and both short‐ and long‐term offspring fitness. This revealed no effect of number of mates on number of eggs laid. However, hatching success of eggs increased with number of mates. This effect could not be attributed to nongenetic effects such as the possibility that polyandry reduces variance in the quantity or fertilizing ability of sperm females receive, because a control group receiving half the number of copulations showed no drop in hatching success. Offspring did not differ in survival, adult mass, size, or development time with treatment. When males were mated to several different females there were no repeatable differences between individual males in the hatching success of their mates eggs. This suggests that improved hatching success of polyandrous females is not due to certain males having genes that improve egg viability regardless of their mate. Instead, our results support the hypothesis that certain males are genetically more compatible with certain females, and that this drives polyandry through differential fertilization success of sperm from more compatible males.

Butterflies tailor their ejaculate in response to sperm competition risk and intensity

Males of many insects eclose with their entire lifetime sperm supply and have to allocate their ejaculates at mating prudently. In polyandrous species, ejaculates of rival males overlap, creating sperm competition. Recent models suggest that males should increase their ejaculate expenditure when experiencing a high risk of sperm competition. Ejaculate expenditure is also predicted to vary in relation to sperm competition intensity. During high intensity, where several ejaculates compete for fertilization of the females eggs, ejaculate expenditure is expected to be reduced. This is because there are diminishing returns of providing more sperm. Additionally, sperm numbers will depend on males ability to assess female mating status. We investigate ejaculate allocation in the polyandrous small white butterfly Pieris rapae (Lepidoptera). Males have previously been found to ejaculate more sperm on their second mating when experiencing increased risk of sperm competition. Here we show that males also adjust the number of sperm ejaculated in relation to direct sperm competition. Mated males provide more sperm to females previously mated with mated males (i.e. when competing with many sperm) than to females previously mated to virgin males (competing with few sperm). Virgin males, on the other hand, do not adjust their ejaculate in relation to female mating history, but provide heavier females with more sperm. Although virgin males induce longer non–receptive periods in females than mated males, heavier females remate sooner. Virgin males may be responding to the higher risk of sperm competition by providing more sperm to heavier females. It is clear from this study that males are sensitive to factors affecting sperm competition risk, tailoring their ejaculates as predicted by recent theoretical models.

Non-fertile sperm delay female remating

Sperm competition is thought to be responsible for the tremendous inter- and intraspecific variation in sperm number and size. But why several animals produce a range of sperm types,, some of which are incapable of fertilizing the females eggs, has remained unexplained for nearly 100 years. We have found that non-fertile sperm protect a males reproductive investment by delaying female remating in the polyandrous green-veined white butterfly, Pieris napi (Pieridae).

Molecular evidence of post-copulatory inbreeding avoidance in the field cricket Gryllus bimaculatus.

Female promiscuity has broad implications for individual behaviour, population genetics and even speciation. In the field cricket Gryllus bimaculatus, females will mate with almost any male presented to them, despite receiving no recorded direct benefits. Previous studies have shown that female crickets can benefit from polyandry through increased hatching success of their eggs. There is evidence that this effect is driven by the potential of polyandrous females to avoid fertilizing eggs with sperm from genetically incompatible males. We provide direct evidence supporting the hypothesis that polyandry is a mechanism to avoid genetic incompatibilities resulting from inbreeding. Using microsatellite markers we examined patterns of paternity in an experiment where each female mated with both a related and an unrelated male in either order. Overall, unrelated males were more successful in gaining paternity than were related males, but this effect was driven by a much greater success of unrelated males when they were the first to mate.

SUCCESSFUL FATHERS SIRE SUCCESSFUL SONS

The theory of sexual selection holds a central role in evolutionary biology. Its key assumption is the heritability of traits associated with reproductive success. Strong indirect evidence supporting this assumption comes from the numerous studies that have identified heritable traits associated with mating success. However, there remain only a handful of studies that have attempted to demonstrate directly that successful fathers have successful sons. We present the results of an experimental study of the mating success and phenotype of male field crickets Gryllus bimaculatus (Orthoptera: Gryllidae) and their offspring. These reveal that sons of successful males obtain significantly more copulations than sons of unsuccessful males. There was no difference in body size of sons of either group, but sons of successful males had significantly longer development times. This may represent a naturally selected cost to traits associated with success that could balance their sexually selected advantages.

Female receptivity in butterflies and moths.

SUMMARY Female receptivity in butterflies and moths is influenced by a multitude of factors that vary between virgin and mated females, and is often affected by the quality and persistence of courting males. Mated females of polyandrous species frequently display a period of non-receptivity following mating, often resulting from factors transferred by the male at mating. Some of these compounds have a transient effect (e.g. anti-aphrodisiacs and mating plugs), whereas others induce long-term suppression of receptivity (i.e. sperm and seminal factors). Sperm appear to generally induce long-term suppression of female receptivity in both butterflies and moths. In some species, production of non-fertile sperm may function to fill the females sperm storage organ and switch off receptivity, although whether this is a general phenomenon across the Lepidoptera has not yet been examined. Examination of seminal fluids suppressing female receptivity in moths suggests that more than one factor is implicated, but frequently the transfer or stimulation of Juvenile Hormone production is involved. Surprisingly, potential seminal factors influencing female receptivity in butterflies remain largely unexplored. In this review, I summarize the various factors that are known to affect female receptivity in the Lepidoptera to date, and briefly compare the function and similarity of the Pheromone Suppressing Peptide (HezPSP) in moths to that of the Sex Peptide in Drosophila melanogaster (DrmSP). The exciting possibility that seminal peptides in the Lepidoptera and Diptera (e.g. Drosophila melanogaster) may have shared functionality is discussed.

Spermatophore size in bushcrickets : comparative evidence for nuptial gifts as a sperm protection device

During courtship and copulation, males of many insect species provide the female with a nuptial gift of a prey item or synthesized material. These gifts may be explained as a form of paternal investment by increasing female reproductive output, or in terms of mating effort by increasing male fertilization success. These explanations, while not mutually exclusive, are controversial. While experimental studies examine the maintenance of nuptial gifts in single species, comparative studies are required to indicate more general evolutionary trends. Male bushcrickets provide females with a nuptial gift, a spermatophylax, which is transferred to females at mating along with the sperm‐containing ampulla. Analysis of comparative data of 28 species of bushcrickets (Orthoptera: Tettigoniidae), reveals that male spermatophore size (spermatophylax and ampulla weight) is positively correlated with female refractory period, which, in turn, correlates with male fertilization success. Moreover, gift size (the spermatophylax) covaries with ejaculate size (the ampulla), which is consistent with the hypothesis that it serves as a sperm protection device. In contrast, there is no significant correlation between any measure of female fecundity and male spermatophylax size. This indicates that the variation in spermatophore size among bushcrickets is better explained by a mating‐effort function than a paternal investment function.