Free mutual mate preferences in house mice affect reproductive success and offspring performance

When social constraints on the expression of mate preferences are absent, variation in offspring viability is predicted to favour females and males that display mate preferences. Earlier studies showed that female and male house mice, Mus domesticus, tested individually and mated with preferred (P) partners had higher reproductive success and better progeny performance than individuals mated with nonpreferred (NP) partners. Here we tested the effects of mutual mate preferences on reproductive success, offspring viability and performance. We conducted mate preference tests and created four types of reproductive pairings. One involved females and males that preferred each other (P-P); the second type had females that preferred the male but the male did not prefer the female (P-NP); the third had females that did not prefer the male but the male did prefer the female (NP-P). The last set consisted of females and males that did not prefer each other (NP-NP). We measured components of fitness for breeders (reproductive success) and offspring viability (birth-to-weaning viability and weight variation) as well as measures of offspring performance. There were no statistical differences in reproductive success of breeders or offspring viability and quality (weight variation) among the four types of pairings. There were, however, consistent differences between P-P versus NP-NP matings. The number of pups weaned, time to first litter, birth-to-weaning viability, pup body weight at birth and weaning, and the growth rates for pups of both sexes were consistently greater for progeny from P-P matings than NP-NP matings. Significant differences occurred among the four mating types in dominance of sons during aggression trials, nest construction and predator avoidance. Progeny from P-P matings displayed behaviour associated with higher fitness more often than progeny from NP-NP matings. These data show that breeders produce more highly competent progeny, most likely to survive, when social constraints on the expression of mate preferences in both sexes are relaxed.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Sexual conflict and the evolution of female mate choice and male social dominance

Conflicts between the sexes over control of reproduction are thought to lead to a cost of sexual selection through the evolution of male traits that manipulate female reproductive physiology and behaviour, and female traits that resist this manipulation. Although studies have begun to document negative fitness effects of sexual conflict, studies showing the expected association between sexual conflict and the specific behavioural mechanisms of sexual selection are lacking. Here we experimentally manipulated the opportunity for sexual conflict in the cockroach. Nauphoeta cinerea and showed that, for this species, odour cues in the social environment influence the behavioural strategies and fitness of males and females during sexual selection. Females provided with the opportunity for discriminating between males but not necessarily mating with preferred males produced fewer male offspring than females mated at random. The number of female offspring produced was not affected, nor was the viability of the offspring. Experimental modification of the composition of the males' pheromone showed that the fecundity effects were caused by exposure to the pheromone component that makes males attractive to females but also makes males less likely to be dominant. Female mate choice therefore carries a demographic cost but functions to avoid male manipulation and aggression. Male-male competition appears to function to circumvent mate choice rather than directly manipulating females, as the mate choice can be cryptic. The dynamic struggle between the sexes for control of mating opportunities and outcomes in N. cinerea therefore reveals a unique role for sexual conflict in the evolution of the behavioural components of sexual selection.     

Evolutionarily stable oviposition and sex ratio in parasitoid wasps with single‐sex broods

Abstract 1. The flexibility of hymenopteran sex ratios is well documented, particularly in structured populations featuring sib mating. 2. Using game theoretic models, the present study examines species producing single‐sex broods in which sib mating is unlikely, and focuses on the role of population density in determining evolutionarily stable oviposition strategies. 3. Since only mated females can produce offspring of both sexes while unmated females produce only male offspring, mated females are under selection to produce more females overall to balance the primary sex ratio. 4. As the proportion of all females that are mated should increase with density, offspring sex ratio of mated females is strongly linked to density at low to moderate densities. The present study shows that when density becomes low enough for fewer than half of all females to have mated, then female offspring generate higher fitness. 5. In this low density situation, females may gain a fitness benefit from waiting at their emergence site or from using other costly means to find and mate with males before ovipositing. 6. The predicted correspondence between females waiting at the emergence site and fewer than half of females in the population containing sperm, can be tested empirically, as can the somewhat counter‐intuitive prediction that greater access to males should yield a more male‐biased sex ratio in the offspring of mated females. 7. The present study also indicates how measuring the variance in giving up times by females waiting for males at low density, can provide insight into mechanisms determining waiting times.     

Change in frequency of a rare mutant allele: A general formula and applications to partial inbreeding models

 We deduce and prove a general formula to approximate the change in frequency of a mutant allele under weak selection, when this allele is introduced in small frequency into a population which was previously at a fixation state. We apply the formula to autosomal genes in partial selfing models and to autosomal as well as sex-linked genes in partial sib mating models. It is shown that the fate of a rare mutant allele depends not only on the selection parameters, the inbreeding coefficient and the reproductive values of the sexes in sex-differentiated populations, but also on coefficients of relatedness between mates. This is interpreted as a kin selection effect caused by inbreeding per se. Received: 3 December 2001 / Revised version: 10 April 2002 / Published online: 19 November 2002 Research supported in part by NSERC of Canada and FCAR of Québec. Mathematics Subject Classification (2000): Primary 60J80, Secondary 92D10, 92D25 Keywords or phrases: Adaptive topography – Partial selfing – Partial sib mating – Kin selection     

Similar Performance of Diploid and Haploid Males in an Ant Species without Inbreeding Avoidance

Under haplodiploidy, a characteristic trait of all Hymenoptera, females develop from fertilised eggs, and males from unfertilised ones. Males are therefore typically haploid. Yet, inbreeding can lead to the production of diploid males that often fail in development, are sterile or are of lower fertility. In most Hymenoptera, inbreeding is avoided by dispersal flights of one or both sexes, leading to low diploid male loads. We investigated causes for the production of diploid males and their performance in a highly inbred social Hymenopteran species. In the ant Hypoponera opacior, inbreeding occurs between wingless sexuals, which mate within the mother nest, whereas winged sexuals outbreed during mating flights earlier in the season. Wingless males mate with queen pupae and guard their mating partners. We found that they mated randomly with respect to relatedness, indicating that males do not avoid mating with close kin. These frequent sib‐matings lead to the production of diploid males, which are able to sire sterile triploid offspring. We compared mating activity and lifespan of haploid and diploid wingless males. As sexual selection acts on the time of emergence and body size in this species, we also investigated these traits. Diploid males resembled haploid ones in all investigated traits. Hence, albeit diploid males cannot produce fertile offspring, they keep up with haploid males in their lifetime mating success. Moreover, by fathering viable triploid workers, they contribute to the colonies' work force. In conclusion, the lack of inbreeding avoidance led to frequent sib‐matings of wingless sexuals, which in turn resulted in the regular production of diploid males. However, in contrast to many other Hymenopteran species, diploid males exhibit normal sexual behaviour and sire viable, albeit sterile daughters.     

Reproductive strategies in snakes

Snakes of both sexes display remarkable flexibility and diversity in their reproductive tactics. Many features of reproduction in female snakes (such as reproductive mode and frequency, seasonality and multiple mating) allow flexible maternal control. For example, females can manipulate not only the genotypes of their offspring (through mate choice or enhanced sperm competition) but also the phenotypes of their offspring (through allocation 'decisions', behavioural and physiological thermoregulation, and nest-site selection). Reliance on stored energy ('capital') to fuel breeding results in low frequencies of female reproduction and, in extreme cases, semelparity. A sophisticated vomeronasal system not only allows male snakes to locate reproductive females by following scent trails, but also facilitates pheromonally mediated mate choice by males. Male-male rivalry takes diverse forms, including female mimicry and mate guarding; combat bouts impose strong selection for large body size in males of some species. Intraspecific (geographical) variation and phenotypic plasticity in a wide array of reproductive traits (offspring size and number; reproductive frequency; incidence of multiple mating; male tactics such as mate guarding and combat; mate choice criteria) provide exceptional opportunities for future studies.     

Size‐dependent mating pattern in a nuptial gift‐giving insect

The reproductive interests of females and males often diverge in terms of the number of mating partners, an individual’s phenotype, origin, genes, and parental investment. This conflict may lead to a variety of sex‐specific adaptations and also affect mate choice in both sexes. We conducted an experiment with the bush‐cricket Pholidoptera griseoaptera (Orthoptera, Tettigoniidae), a species in which females receive direct nutritional benefits during mating. Mated individuals could be assigned due to the genotype of male spermatodoses, which are stored in the female’s spermatheca. After 3 weeks of possible copulations in established mating groups which were random replications with four females and males we did not find consistent assortative mating preference regarding to body size of mates. However, our results showed that the frequency of within‐pair copulations (192 analyzed mating events in 128 possible pairwise combinations) was positively associated with the body size of both mated individuals with significant interaction between sexes (having one mate very large, association between body size and the number of copulations has weaken). Larger individuals also showed a higher degree of polygamy. This suggests that body size of this nuptial gift‐giving insect species is an important sexual trait according to which both sexes choose their optimal mating partner.     

Impaired sperm quality,delayed mating but no costs for offspring fitness in crickets winning a fight

The outcome of male–male contest competition is known to affect male mating success and is believed to confer fitness benefits to females through preference for dominant males. However, by mating with contest winners, females can incur significant costs spanning from decreased fecundity to negative effects on offspring. Hence, identifying costs and benefits of male dominance on female fitness is crucial to unravel the potential for a conflict of interests between the sexes. Here, we investigated males' pre‐ and post‐copulatory reproductive investment and its effect on female fitness after a single contest a using the field cricket Gryllus bimaculatus. We allowed males to fight and immediately measured their mating behaviour, sperm quality and offspring viability. We found that males experiencing a fight, independently of the outcome, delayed matings, but their courtship effort was not affected. However, winners produced sperm of lower quality (viability) compared to losers and to males that did not experience fighting. Results suggest a trade‐off in resource allocation between pre‐ and post‐mating episodes of sexual selection. Despite lower ejaculate quality, we found no fitness costs (fecundity and viability of offspring) for females mated to winners. Overall, our findings highlight the importance of considering fighting ability when assessing male reproductive success, as winners may be impaired in their competitiveness at a post‐mating level.     

Wolbachia affects oviposition and mating behaviour of its spider mite host

Wolbachia bacteria are transmitted from mother to offspring via the cytoplasm of the egg. When mated to males infected with Wolbachia bacteria, uninfected females produce unviable offspring, a phenomenon called cytoplasmic incompatibility (CI). Current theory predicts that ‘sterilization’ of uninfected females by infected males confers a fitness advantage to Wolbachia in infected females. When the infection is above a threshold frequency in a panmictic population, CI reduces the fitness of uninfected females below that of infected females and, consequently, the proportion of infected hosts increases. CI is a mechanism that benefits the bacteria but, apparently, not the host. The host could benefit from avoiding incompatible mates. Parasite load and disease resistance are known to be involved in mate choice. Can Wolbachia also be implicated in reproductive behaviour? We used the two‐spotted spider mite – Wolbachia symbiosis to address this question. Our results suggest that uninfected females preferably mate to uninfected males while infected females aggregate their offspring, thereby promoting sib mating. Our data agrees with other results that hosts of Wolbachia do not necessarily behave as innocent bystanders – host mechanisms that avoid CI can evolve.     

The sex lives of parasites: Investigating the mating system and mechanisms of sexual selection of the human pathogen Schistosoma mansoni

The mating systems of internal parasites are inherently difficult to investigate although they have important implications for the evolutionary biology of the species, disease epidemiology, and are important considerations for control measures. Using parentage analyses, three topics concerning the mating biology of Schistosoma mansoni were investigated: the number of mates per adult male and female, variance in reproductive success among individuals, and the potential role for sexual selection on male body size and also mate choice for genetically dissimilar individuals. Results indicated that schistosomes were mostly monogamous, and evidence of only one mate change occurred over a period of 5-6 weeks. One male was polygynous and contained two females in its gynecophoral canal although offspring were only detected for one of the females. Even though they were primarily monogamous and the sex ratio near even, reproductive success was highly variable, indicating a potential role for sexual selection. Male body size was positively related to reproductive success, consistent with sexual selection via male-male competition and female choice for large males. However, relatedness of pairs was not associated with their reproductive success. Finally, genetically identical individuals differed significantly in their reproductive output and identical males in their body size, indicating important partner and environmental effects on these traits.     

Paternal indirect genetic effects on offspring viability and the benefits of polyandry

Although females are expected to maximize their reproductive success with only one or a few matings, the females of many species mate with multiple partners. Experimental studies have found evidence for an increase in egg or embryo viability when females mate polyandrously. These studies have been interpreted in the context of genetic-benefit models that propose that multiple mating increases offspring viability because it allows females to select male genotypes that influence viability directly or because it allows females to avoid genetic incompatibility. However, no studies have examined directly the precise mechanisms by which parents influence embryo viability. Using a morphological marker that enabled us to determine paternity and survival of embryos sired by individual male crickets in both sperm-competitive and -noncompetitive situations, we show that males inducing high embryo viability enhance the viability of embryos sired by inferior males. These results indicate that paternal effects and interacting phenotypes determine embryo viability. They show that a male's reproductive success is modified by the interaction between indirect genetic effects of sperm competitors. Importantly, our findings show that the benefits accruing to offspring of multiply mated females need not be transmitted genetically.     

Banded mongooses avoid inbreeding when mating with members of the same natal group

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard–female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate‐guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.     

Male house mice produce fewer offspring with lower viability and poorer performance when mated with females they do not prefer

We report experimental results consistent with the hypothesis that constraints on the expression of male mating preferences affect breeder fitness, offspring viability and performance. If constraints on the expression of mating preferences are common, tests of fitness variation associated with mate preferences must eliminate as many constraints on mate preferences as possible. We tested whether male mate preferences influenced breeder fitness, offspring performance and viability in typically polygynous house mice, Mus domesticus, from a feral source population. Our ‘free mate choice’ trials not only eliminated female preferences, male-male and female-female competition, but also our best guesses of the traits mediating choosers' preferences. Males mated with their preferred (P) females sired more litters than males mated with their nonpreferred (NP) females. Offspring viability was significantly lower when males' reproduced with females they did not prefer compared with females they did prefer. Adult sons of males that mated with their P females were socially dominant to sons of males that mated with their NP females. Adult offspring from P pairings built better nests than offspring from NP pairings. The slope of the survivorship curve for P offspring was significantly higher than for NP offspring. These results showed (1) males' mate preferences affected their fitness, (2) males that mated with females they preferred produced more litters than males that mated with females they did not prefer, and (3) their offspring were significantly more viable and performed significantly better on standardized performance tests. This is the first demonstration of fitness benefits of male choice behaviour in a mammal species with typical paternal investment. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

The female perspective of mating in A. femoralis, a territorial frog with paternal care--a spatial and genetic analysis

The adaptive significance of sequential polyandry is a challenging question in evolutionary and behavioral biology. Costs and benefits of different mating patterns are shaped by the spatial distribution of individuals and by genetic parameters such as the pairwise relatedness between potential mating partners. Thus, females should become less choosy as costs of mating and searching for mates increase. We used parentage assignments to investigate spatial and genetic patterns of mating across a natural population of the Neotropical frog Allobates femoralis, a species characterized by male territoriality and care and female iteroparity. There was no correlation between genetic and spatial distances between adult individuals across the population. In 72% of cases, females mated with males available within a radius of 20 m. Mean pairwise relatedness coefficients of successful reproducers did not differ from random mating but had a lower variance than expected by chance, suggesting maximal reproductive output at intermediate genetic divergence. We also found evidence for selection in favor of more heterozygous individuals between the embryo and adult stage. The level of sequential polyandry significantly increased with the number of spatially available males. Females that had more candidate males also produced more adult progeny. We hypothesize that the benefits associated with female multiple mating outweigh the costs of in- and outbreeding depression, and consequently precluded the evolution of 'choosy' mate selection in this species.     

Insects and incest: Sib‐mating tolerance in natural populations of a parasitoid wasp

Sib‐mating avoidance is a pervasive behaviour that is expected to evolve in species subject to inbreeding depression. Although laboratory studies provide elegant demonstrations, small‐scaled bioassays minimize the costs of mate finding and choice, and thus may produce spurious findings. We therefore combined laboratory experiments with field observations to examine the existence of inbreeding avoidance using the parasitoid wasp Venturia canescens. In the laboratory, our approach consisted of mate‐choice experiments to assess kin discrimination in population cages with competitive interactions. A higher mating probability after sib rejections suggested that females could discriminate their sibs; however, in contrast to previous findings, sib‐mating avoidance was not observed. To compare our laboratory results to field data, we captured 241 individuals from two populations. Females laid eggs in the lab, and 226 daughters were obtained. All individuals were genotyped at 18 microsatellite loci, which allowed inference of the genotype of each female's mate and subsequently the relatedness within each mating pair. We found that the observed rate of sib‐mating did not differ from the probability that sibs encountered one another at random in the field, which is consistent with an absence of sib‐mating avoidance. In addition, we detected a weak but significant male‐biased dispersal, which could reduce encounters between sibs. We also found weak fitness costs associated with sib‐mating. As such, the sex‐biased dispersal that we found is probably sufficient to mitigate these costs. These results imply that kin discrimination has probably evolved for purposes other than mate choice, such as superparasitism avoidance.     

Evolutionary significance of promiscuity in an aphidophagous ladybird, Propylea dissecta (Coleoptera: Coccinellidae)

The short- and long-term consequences of monogamy and promiscuity in an aphidophagous ladybird, Propylea dissecta (Mulsant) in terms of reproductive performance and offspring fitness were investigated. Promiscuous females were more fecund and laid more viable eggs than monogamous ones. Amongst promiscuous females, those mated with multiple males (freedom for mate choice) had significantly higher reproductive output than those mated daily with a new unmated male. The increased reproductive output of females mated with an unmated male each day in comparison to monogamous ones might possibly be a result of their increased ejaculate size. The further increase in reproductive output, when a female was allowed to choose a mate, may be because of repeated preferential mating with the fitter males. Results on long-term consequences of promiscuity revealed faster development and increased survival in offspring of promiscuous females at 25, 27 and 30 degrees C. The percent adult emergence was more strongly influenced than development by the mating regime. There were no statistically significant differences in survival of offspring of promiscuous females (mate choice) at the three temperatures, while the percent survival of offspring of monogamous females differed significantly. Offspring of promiscuous females (mate choice) were fittest in terms of development and survival, which indicates their probable better genetic constitution and subsequently that of chosen mates. Thus, promiscuity has both short- and long-term benefits and is advantageous to ladybirds. The presence of long-term benefits in terms of fitter offspring probably indicates the evolutionary rationale behind the prevalence of promiscuity in ladybirds.     

Detection of female mating status using chemical signals and cues

Males of many species choose their mate according to the female's reproductive status, and there is now increasing evidence that male fitness can depend on this discrimination. However, females will also aim to regulate their mating activity so as to maximize their own fitness. As such, both sexes may attempt to dictate the frequency and timing of female mating, reflecting the potentially different costs of female signaling to both sexes. Here, I review evidence that chemical cues and signals are used widely by males to discriminate between mated and unmated females, and explore the mechanisms by which female odour changes post‐mating. There is substantial empirical evidence that mated and unmated females differ in their chemical profile, and that this variation provides males with information on a female's mating status. Although there appears to be large variation among species regarding the mechanisms by which female odour is altered post‐mating, the transfer of male substances to females during or subsequent to copulation appear to play a major role. This transfer of substances by males may be part of their strategy to suppress reproduction by competing males, particularly in species where females mate more than once.     

Multiple Mating Increases Fecundity, Fertility and Relative Clutch Mass in the Female Leopard Gecko (Eublepharis macularius)

Females across many taxa may mate with several males or mate more than once with the same male within one reproductive event. Although many researchers have discussed the effects of multiple mating on reproductive success of females, few studies have attempted to disentangle whether the reproductive success of females differs with respect to whether females mate with multiple males or mate more than once with one male. In this study, we hypothesized that female leopard geckos (Eublepharis macularius) increase aspects of their reproductive success, such as fecundity, fertility and relative clutch mass, by mating more than once within one reproductive event, either by mating repeatedly with the same male or multiply mating with different males. We controlled for the potentially confounding variables of mating frequency and mate number by allowing females to mate once with one male, twice with the same male, or twice with two different males. We found that females that mated with more than one male laid more clutches, exhibited increased egg fertility and invested more in clutches relative to females that mated only once with one male, whereas females that mated twice to the same male were intermediate for these variables. Thus, reproductive success is higher among female leopard geckos that mated with more than one male compared to female leopard geckos that mated only once.     

Sexual History Affects Mating Behavior and Mate Choice in the Crayfish Orconectes limosus

Because mating entails both costs and potential benefits to both sexes, males and females should be under selection to make optimal choices from among available potential mates. For example, in some cases, individuals may benefit by using information on potential mates' previous sexual histories to make mate choices. In such cases, the form and direction of these benefits may vary both between the sexes and based on the sexual history of the choosing individuals themselves. We investigated the effects of recent previous sexual history on the mate choice and mating behavior of both males and females of the crayfish Orconectes limosus. In one experiment, we found that opposite‐sex dyads comprising crayfish that had both mated 7–8 d previously with other conspecifics were significantly less likely to mate than dyads in which at least one crayfish was unmated. In a second experiment, we found that, when presented with a choice of tethered (but free to move) opposite‐sex conspecifics, only virgin females discriminated between males based on sexual history, showing a preference for virgin males over recently mated males. Mated females, mated males, and virgin males showed no preferences based on the sexual histories of potential mates. We discuss the implications of these inferences in the context of what was previously known about mating behavior and potential sperm limitation in crustaceans and other taxa.     

Evolution of sex ratios in social hymenoptera: kin selection,local mate competition,polyandry and kin recognition

A model is constructed to study the effects of local mate competition and multiple mating on the optimum allocation of resources between the male and female reproductive brood in social hymenopteran colonies from the ‘points of view’ of the queen (parental manipulation theory) as well as the workers (kin selection theory). Competition between pairs of alleles specifying different sex investment ratios is investigated in a game theoretic frame work. All other things being equal, local mate competition shifts the sex allocation ratio in favour of females both under queen and worker control. While multiple mating has no effect on the queen’s optimum investment ratio, it leads to a relatively male biased investment ratio under worker control. Under queen control a true Evolutionarily Stable Strategy(ess) does not exist but the ‘best’ strategy is merely immune from extinction. A trueess exists under worker control in colonies with singly mated queens but there is an asymmetry between the dominant and recessive alleles so that for some values of sex ratio a recessive allele goes to fixation but a dominant allele with the same properties fails to do so. Under multiple mating, again, a trueess does not exist but a frequency dependent region emerges. The best strategy here is one that is guaranteed fixation against any competing allele with a lower relative frequency. Our results emphasize the need to determine levels of local mate competition and multiple mating before drawing any conclusions regarding the outcome of queen-worker conflict in social hymenoptera. Multiple mating followed by sperm mixing, both of which are known to occur in social hymenoptera, lower average genetic relatedness between workers and their reproductive sisters. This not only shifts the optimum sex ratio from the workers’ ‘point of view’ in favour of males but also poses problems for the kin selection theory. We show that kin recognition resulting in the ability to invest in full but not in half sisters reverts the sex ratio back to that in the case of single mating and thus completely overcomes the hurdles for the operation of kin selection.