Hermaphrodite sex role preferences: the role of partner body size, mating history and female fitness in the sea slug Chelidonura sandrana

Costs and benefits associated with matings and the effects of mating frequency on fitness commonly differ between the sexes. As a result, outcrossing simultaneous hermaphrodites may prefer to copulate in the more rewarding sex role, generating conflicts over sperm donation and sperm receipt between mates. Because recent sex role preference models remain controversial, we contrast here some of their assumptions and predictions in the sea slug Chelidonura sandrana. For this hermaphrodite with sperm storage and internal fertilisation, risk-averse models assume that fitness pay-offs are constantly higher in the female than in the male function in any single mating. Moreover, excluding mutual partner assessment, these models predict male mating behaviour to be independent of receiver traits. The competing gender ratio hypothesis assumes that relative fitness pay-offs, and thus the preferred mating roles, vary and may reverse between matings and predicts that ejaculation strategies co-vary with receiver quality. We found that field mating rates of C. sandrana substantially exceeded what is required to maintain female fertility and fecundity, indicating large variation in direct female benefits between matings. We further demonstrate that male copulation duration adaptively increased with partner body size (i.e. fecundity) but decreased with recent partner promiscuity. These findings are compatible with the gender ratio hypothesis but contradict risk-averse models.     

Testes mass in megachiropteran bats varies in accordance with sperm competition theory

Sperm competition is a widespread phenomenon influencing a range of characters, including investment in gonadal tissue. Conspecific proximity is one factor which can influence the risk of sperm competition and hence testicular investment, and decreased confidence of paternity may be one cost of group living. Aspects of female biology may also influence spermatogenic investment and sperm morphology. This study examines the associations between relative testes mass and roost-group size across 17 species of Megachiroptera. Associations between breeding season duration and investment in spermatogenesis are also examined, as are associations between female reproductive tract dimensions and testes mass and dimensions of spermatozoa across all bats. Relative testes mass was significantly positively associated with roost-group size at a species level and after appropriate phylogenetic control (pairwise comparisons and comparison of independent contrasts). There were no significant relationships between breeding season duration and relative testes mass. Across all bats, neither testes mass nor sperm length were significantly related to dimensions of the female tract. The results are discussed in the context of sperm competition. Received: 7 January 1998 / Accepted after revision: 8 August 1998     

Seminal fluid enhances sperm viability in the leafcutter ant Atta colombica

The seminal fluid that accompanies sperm in ejaculates has been shown or suggested to affect sperm competition and paternity success of insects by preventing female remating, inducing oviposition, and forming mating plugs. In Atta leafcutter ants, queens have multiple mates but never remate later in life, although they may live and produce fertilized eggs for several decades. The mating biology and life history of these ants therefore suggests that the major function of seminal fluid is to maximize sperm viability during copulation, sperm transfer, and initial sperm storage. We tested this hypothesis by comparing the viability of testis sperm and ejaculated sperm (mixed with seminal fluid) and found a significant positive effect of seminal fluid on sperm viability. We further quantified this positive effect by adding accessory gland secretion (a major component of seminal fluid) in a dilution series, to show that minute quantities of accessory gland secretion achieve significant increases in sperm viability. Sperm stored by queens for 1 year benefited in a similar way from being exposed to accessory gland compounds after dissection in control saline solution. Our results provide the first empirical evidence that seminal fluid is important for the production of viable ejaculates and that the accessory glands of Atta males—despite their small size—are functional and produce a very potent secretion.     

Certainty of paternity covaries with paternal care in birds

Summary Male investment in parental care has been hypothesized to be affected or not to be affected by their certainty of paternity, depending on the particular assumptions of theoretical models. We used data on paternal care and extra-pair paternity from 52 bird species to determine whether male parental care was related to certainity of paternity. Paternal care was measured as the relative male contribution to nest building, courtship feeding, incubation, and feeding of nestlings, respectively. Males of avian taxa did not provide less parental care during nest building, courtship feeding and incubation if the frequency of extra-pair paternity was high. However, male participation in feeding of offspring was significantly negatively related to the frequency of extra-pair paternity. This was also the case when the effects of potentially confounding variables such as developmental mode of offspring (which may result in males being freed from parental duties), extent of polygyny (which may result in less paternal care), and the frequency of multiple clutches during one breeding season (which may increase the probability of finding fertile females during the nestling period) were controlled statistically. These results suggest that the extent of paternal care has been affected by certainty of paternity, and that sex roles during the energetically most expensive parts of reproduction have been shaped by sperm competition.     

Sperm competition or sperm selection: no evidence for female influence over paternity in yellow dung flies Scatophaga stercoraria

Recent studies of non-random paternity have suggested that sperm selection by females may influence male fertilization success. Here we argue that the problems originally encountered in partitioning variation in non-random mating between male competition and female choice are even more pertinent to interpreting patterns of non-random paternity because of intense sperm competition between males. We describe an experiment with the yellow dung fly, Scatophaga stercoraria, designed to partition variance in the proportion of offspring sired by the second male, P ₂, between males and females, and to control for sperm competition. Large males were shown to have a higher P ₂ than small males but P ₂ was independent of the size of the female’s first mate. This result might suggest an absolute female preference for large males via sperm selection. However, large males have a higher constant rate of sperm transfer and displacement. After controlling for this effect of sperm competition, large males did not achieve higher paternity than small males. We argue that a knowledge of the mechanism of sperm competition is essential so that male effects can be controlled before conclusions are made regarding the influence of sperm selection by females in generating non-random paternity. Received: 4 April 1995 / Accepted after revision: 17 October 1995     

Female choice on male quantitative traits in lizards — why is it so rare?

Female choice on the basis of male traits has been described in an array of taxa but has rarely been demonstrated in reptiles. In the sand lizard (Lacerta agilis), and possibly in other non-territorial reptiles, a male's contribution to a female's fitness is restricted to his genes. In order to choose males of high genetic quality, females have to trade the fitness gain against the costs of active choice. In a Swedish population of sand lizards, long-lived males sired offspring with higher embryonic survival compared to offspring sired by short-lived males. In spite of this female sand lizards did not mate selectively with older and/or larger males. There appeared to be mo reliable cues to male longevity; age-specific male body size was highly variable. Furthermore, estimates of male nuptial coloration did not covary with ectoparasite load and, hence, females cannot use male coloration as a cue to heritable resistance to pathogenic parasite effects. When cues to male genetic quality are poor, or inaccurate, and males make no parental investment, we predict that female choice will be rare. Sand lizard females mating with many partners lay clutches with higher hatching success. Thus, females may obtain good genes for their young by multiple mating, thereby avoiding costs associated with mate choice.     

Why do male Callosobruchus maculatus beetles inseminate so many sperm?

Male Callosobruchus maculatus F. (Coleoptera: Bruchidae) inseminate more sperm than females can effectively store in their spermathecae. This study examines the adaptive significance of excess sperm transfer by measuring components of male and female reproductive success in response to manipulating the number of sperm inseminated. The number of sperm transferred during copulation was reduced from 56,000 ±4,462 to 8,700±1,194 by sequentially mating males to virgin females. Reducing the number of sperm inseminated by the first male to mate had no effect on the extent of sperm precedence, but reducing the number of sperm inseminated by the second male resulted in a significant reduction in the extent of sperm precedence. When large numbers of sperm are inseminated the remating refractory period of females is increased. These results indicate that males transferring large numbers of sperm during copulation have a two-fold advantage at fertilization; they are more effective at preempting previously stored sperm and they are likely to father more offspring by delaying the time of female remating. The transfer of excess sperm does not appear to serve as nonpromiscuous male mating effort; the number of eggs laid, their fertility and the subsequent survival of zygotes were unaffected by manipulating the number of sperm inseminated. The underlying mechanisms of sperm precedence were also examined. Simple models of sperm displacement failed to accurately predict the patterns of sperm precedence observed in this species. However, the results do not provide conclusive evidence against the models but rather serve to highlight our limited understanding of the movement of sperm within the female's reproductive tract.     

Increased sperm numbers in the vas deferens of meadow voles, <Emphasis Type="Italic">Microtus pennsylvanicus,</Emphasis> in response to odors of conspecific males

Sperm competition occurs when the sperm of two or more males compete to fertilize the egg/s of a particular female. Males of some species respond to a high risk of sperm competition by increasing the number of sperm in their ejaculates. Males may accomplish such a response by increasing the intensity or duration of contraction of the cauda epididymidis and vas deferens. During emission (first phase of the ejaculatory process), the vas deferens receives sperm from the cauda epididymidis and propels the sperm to the urethra. In this paper, we tested the hypothesis that males exposed to a high risk of sperm competition mobilize larger numbers of sperm from the cauda epididymidis to the vas deferens before initiation of copulatory behavior. This accumulation of sperm in the vas deferens would result in a larger number of sperm in the ejaculate. To test this hypothesis, we exposed male meadow voles, Microtus pennsylvanicus, to either low or high risks of sperm competition using soiled bedding of conspecific individuals. At three different times after this exposure (15, 30, or 60 min), we removed both vasa deferentia and counted the sperm within them. We found a significant increase in sperm numbers in the vas deferens of males after 30 min of being exposed to a high risk of sperm competition. The lower sperm numbers after 15 and 60 min of exposure suggest that the observed response is relatively slow and that sperm mobilized to the vasa deferentia may return to the cauda epididymides if ejaculation does not occur some time after the observed response. Our results indicate that the physiological response that may result in high sperm numbers in the ejaculate in relation to high risk of sperm competition can occur before initiation of copulatory behavior.     

Effects of frequent mating on sex allocation in the simultaneously hermaphroditic great pond snail (Lymnaea stagnalis)

Simultaneous hermaphrodites have the opportunity to control the allocation of resources to the male and female function depending on the circumstances. Such flexibility also provides the possibility to influence sex allocation in the mating partner. To investigate this idea, we measured egg production (female investment) and sperm production as well as prostate gland size (both are part of male investment) under different mating regimes in the great pond snail Lymnaea stagnalis. We find no evidence for the prediction from sex allocation theory that sperm production increases with mating frequency. However, we do find that animals with more mating opporunities develop smaller prostate glands, in which seminal fluid is produced. Moreover, repeated mating increases egg production, thus shifting allocation towards the female function, and probably decreases growth. So, our data hint at a three-way trade-off between part of the male function (prostate gland), female function, and growth. Interestingly, sex allocation seems to be shifted in the opposite direction from the one predicted by theory. We discuss how this feminization is suggestive of a direct manipulation by the sperm donor, probably to stimulate immediate sperm use.     

Patterns of sperm use in the scorpionfly Panorpa germanica L. (Mecoptera: Panorpidae)

Sperm competition can be a powerful selective force in the evolution of reproductive strategies and mating systems. In studies on sperm competition, patterns of sperm use are typically reported as the mean species value of P ₂, determined as the proportion of offspring sired by the second male to copulate with a doubly mated female. However, the within-species variance in P ₂ has mostly been ignored, although taking this variance into account may be crucial for understanding the underlying mechanisms of sperm competition. Paternity analysis among the offspring of doubly mated females of Panorpa germanica (Mecoptera, Panorpidae) revealed a relationship between relative copulation durations of both males and the proportion of offspring each male will sire. This correlation between proportional copulation durations and paternity suggests mixing of sperm from different males inside the female’s spermatheca. Yet, sperm mixing appears to be incomplete, as paternity was overall slightly shifted towards the second male on average fathering a higher proportion of the offspring than its relative copulation duration would predict in case of complete sperm mixing. For individual males, however, the outcome of sperm competition is rather unpredictable as the intraspecific variance in P ₂ was found to be very high, irrespective of copulation durations. Possible causes of the observed variance in P ₂ and the partial last male sperm precedence are discussed.