Male reproductive fitness and queen polyandry are linked to variation in the supergene Gp-9 in the fire ant Solenopsis invicta

Supergenes are clusters of tightly linked loci maintained in specific allelic combinations to facilitate co-segregation of genes governing adaptive phenotypes. In species where strong selection potentially operates at different levels (e.g. eusocial Hymenoptera), positive selection acting within a population to maintain specific allelic combinations in supergenes may have unexpected consequences for some individuals, including the preservation of disadvantageous traits. The nuclear gene Gp-9 in the invasive fire ant Solenopsis invicta is part of a non-recombining, polymorphic supergene region associated with polymorphism in social organization as well as traits affecting physiology, fecundity and behaviour. We show that both male reproductive success and facultative polyandry in queens have a simple genetic basis and are dependent on male Gp-9 genotype. Gp-9(b) males are unable to maintain exclusive reproductive control over their mates such that queens mated to Gp-9(b) males remain highly receptive to remating. Queens mated to multiple Gp-9(B) males are rare. This difference appears to be independent of mating plug production in fertile males of each Gp-9 genotype. However, Gp-9(b) males have significantly lower sperm counts than Gp-9(B) males, which could be a cue to females to seek additional mates. Despite the reduced fitness of Gp-9(b) males, polygyne worker-induced selective mortality of sexuals lacking b-like alleles coupled with the overall success of the polygyne social form act to maintain the Gp-9(b) allele within nature. Our findings highlight how strong worker-induced selection acting to maintain the Gp-9(b) allele in the polygyne social form may simultaneously result in reduced reproductive fitness for individual sexual offspring.     

Bisexual branching processes in a genetic context: rates of growth for Y-linked genes

A multitype bisexual branching process is considered to model the behaviour of a Y-linked gene with two genotypes in a two-sex population. It is assumed perfect fidelity mating with preference of females for the males carrying certain allele of the gene. Under these assumptions, we study the rate of growth of each genotype on the event of non-extinction. The rate of growth of a genotype may depend on whether the other survives or becomes extinct and, in general, both genotype frequencies grow at different rates. We also investigate conditions for the simultaneous explosion of both genotypes to have positive or zero probability.     

Bisexual branching processes to model extinction conditions for Y-linked genes

In a two-sex monogamic population, the evolution of the number of carriers of the two alleles of a Y-linked gene is considered. To this end, a multitype bisexual branching model is presented in which it is assumed that the gene has no influence on the mating process. It is deduced from this model that the average numbers of female and male descendants per mating unit constitute the key to determining the extinction or survival of each allele. Moreover, the destiny of each allele in the population is found not to depend on the behavior of the other.     

Alternative reproductive tactics and courtship in the common goby

In the marine common goby Pomatoschistus microps , males either build nests and attract females to spawn or act as sneakers, forcing themselves into other males' nests during mating, to fertilize some of the eggs in the clutch. The reproductive tactics of small males were studied in the presence of surplus nest material and an excess of gravid females, while a larger, nestholding male spawned with a female. Of 24 small males, 13 only attempted to sneak, seven only courted females and/or spawned in their own nest, and four performed both behaviours. The small males who attracted females successfully were significantly larger than the ones who failed to do so. Females had been courting the small male more often when he subsequently spawned in his own nest, than when he did not get a female. The small males did not court the females very frequently, and their courtship rate did not depend on whether or not they attracted females. Instead, female courtship behaviour may be a cue for a male either to spawn as a nest holder or become a sneaker. The study pointed out the importance of female behaviour for male reproductive tactics, which could be more important in fish than is known currently.     

Proximate mechanisms of the differences in reproductive success of males bearing different alleles of Pgdh – a gene involved in a sexual conflict in bulb mite

Enzyme polymorphism in phosphogluconate dehydrogenase (Pgdh) is a striking example of single gene polymorphism involved in sexual conflict in bulb mite Rhizoglyphus robini. Males homozygous for the S Pgdh allele were shown to achieve higher reproductive success than FF homozygous males, while negatively influencing fecundity of their female partners. Here, we investigate proximate mechanisms responsible for the increased reproductive success of SS males and find that the S allele is associated with shorter time until copulation, higher copulation frequency and increased sperm production. We also show that Pgdh alleles are probably codominant, with SS males gaining the highest reproductive success, FF males – the lowest – and FS‐heterozygous males taking an intermediate position in all fitness parameters differentiating males of different genotypes. Additionally, we confirm the negative effect that S‐bearing males impose on the fecundity of females they mate with, showing a clear pattern of interlocus sexual conflict. We discuss that this effect is probably associated with increased copulation frequency. Whereas, contrary to what we have predicted, the S allele does not cause increased general male mobility, we speculate that the S allele‐bearing males are more efficient in forcing copulation and/or detecting females.     

Genetic consequences of sex-biased dispersal in a solitary carnivore: Yellowstone cougars

Male-biased dispersal is a common trait in mammals, including carnivores, but its genetic consequences at the population level have been rarely considered for solitary species. We used long-term genetic data from cougars (Puma concolor) in and around Yellowstone National Park to test predictions based on differences in dispersal behaviour among males and females. Consistent with frequent long-distance dispersal of males, we found support for our prediction of less than expected allele sharing in pair-wise comparisons. In contrast, female residents present at the same time and females separated by few generations failed to share more alleles than expected, contrary to our predictions based on limited female dispersal. However, we find that genetic contributions of females with higher reproductive success were still noticeable in subsequent generations, consistent with female offspring showing fidelity to their natal area. These results highlight the importance of male dispersal for inbreeding avoidance, but do not indicate that short-distance dispersal or philopatry in female cougars results in spatial clustering of related individuals.     

Dimorphic Males Display Alternative Reproductive Strategies in the Marine Amphipod Jassa marmorata Holmes (Corophioidea: Ischyroceridae)

Discrete dimorphism of males within a species is often the result of selection for alternative reproductive strategies, and these strategies may be evolutionarily stable (ESS). An ESS may be either mixed (genetically fixed differences) or conditional (flexible differences related to varying environmental conditions) (PARKER 1984). Mature males of the marine amphipod Jassa marmorata are dimorphic. Large ‘major’ males have a greatly enlarged thumb (propodus) on their 2nd gnathopods, while small ‘minor’ males exhibit thumbs that are reduced, and CONIAN (1989) suggested that minors may exhibit a different mating strategy from majors. Ratios of males and females fluctuate seasonally (FRANZ 1989) and female body size is inversely correlated with temperature (FRANZ 1989) so male dimorphism could be a flexible response to varying environmental conditions. I sampled a natural population of J. marmorata over a 1-yr period, quantified major and minor morphology, and measured male behaviour and mating success in experimental arenas that contained varying proportions of male morphs and females. Morphology of the two morphs is discrete; female body size varies with season with significantly smaller individuals in summer and fall; body size predicts morph type; and ratios of majors, minors and females fluctuate seasonally. Finally I showed that majors and minors use different mating tactics to gain access to receptive females, and that these behaviours depend on the male's own morphology and on the environmental setting that it finds itself in. Major males fight, display and attempt to evict other males to mate with receptive females. Minors never fight with, display to or attempt to evict majors, but they infrequently display to and attempt to evict other minor males. Furthermore, mating success of the two morphs was not significantly different and may depend on whether males are with a majority or minority of their own type. These data support the conclusion that major and minor male J. marmorata display evolutionarily stable alternative reproductive strategics, but more work should address the nature of this ESS.     

Comparison of reproductive investment in native and non‐native populations of common wall lizards reveals sex differences in adaptive potential

Non‐native animals can encounter very different environments than those they are adapted to. Functional changes in morphology, physiology and life‐history following introduction show that organisms can adapt both fast and efficiently. It remains unclear, however, if female reproductive characters and male sexually selected behaviour show the same adaptive potential. Furthermore, the invasion success and evolutionary trajectory of non‐native species might often depend on the ability of the sexes to coordinate shifts in characters associated with reproductive strategy. The common wall lizard, Podarcis muralis, has been repeatedly introduced from southern Europe to England over the past 80 years. Lizards in England experience a cool, seasonal climate that effectively restricts recruitment to the first clutch of the season, whereas in their native range up to three clutches per season recruit. As a consequence, both females and males in non‐native populations should benefit from reducing or even eliminating their reproductive investment in second clutches. Using a combination of field data and experiments, we show that non‐native females produce relatively larger and heavier first seasonal clutches and smaller and lighter second seasonal clutches compared to native females. In contrast, non‐native and native males do not differ in their territorial and sexual behaviour later in the season. An adaptive shift in male seasonal reproductive investment may be constrained because males use breeding females as cues for sexual behaviour. If this is so, we expect a general pattern across climatic regimes whereby female reproductive investment evolves first, with responses in males lagging behind.     

Population regulation in the Wood Mouse Apodemus sylvaticus (L.)

Watts 1969 described the population cycle of the Wood Mouse Apodemus sylvaticus as a decline in numbers in spring, a stable period in summer and an increase phase in autumn. Aggression by adult males was considered an important aspect of population regulation limiting male survival in spring and juvenile recruitment in summer. However, recent studies of range behaviour and experimental investigations suggest that male A. sylvaticus are not relevant in population regulation and that the principal regulating factors act on female reproductive success. Female reproductive activity is determined by spatial interactions which, in turn, are determined primarily by the density of females and the proportion of female immigrants in the population. The only impact adult males may have on population size is through infanticide and competition with the females for food.     

Fitness effects of X chromosome drive in the stalk-eyed fly, Cyrtodiopsis dalmanni

Sex-ratio (SR) males produce predominantly female progeny because most Y chromosome sperm are rendered nonfunctional. The resulting transmission advantage of XSR chromosomes should eventually cause population extinction unless segregation distortion is masked by suppressors or balanced by selection. By screening male stalk-eyed flies, Cyrtodiopsis dalmanni, for brood sex ratio we found unique SR alleles at three X-linked microsatellite loci and used them to determine if SR persists as a balanced polymorphism. We found that XSR/XST females produced more offspring than other genotypes and that SR males had lower sperm precedence and exhibited lower fertility when mating eight females in 24 h. Adult survival was independent of SR genotype but positively correlated with eye span. We infer that the SR polymorphism is likely maintained by a combination of weak overdominance for female fecundity and frequency dependent selection acting on male fertility. Our discovery of two SR haplotypes in the same population in a 10-year period further suggests that this SR polymorphism may be evolving rapidly.     

Pheromones exchanged during mating: a mechanism for mate assessment in Drosophila

Many insect species are sexually dimorphic for volatile compounds associated with the cuticle. In these species, females may acquire volatile compounds from males through direct contact with males during mating. In some cases, these compounds function as antiaphrodisiacs, which inhibit subsequent male precopulatory behaviour. During mating, males may also acquire female compounds, which normally stimulate males to court. Contact during mating thus results in a mutual exchange of compounds usually found primarily, or exclusively, on one or the other sex. Drosophila melanogaster is a sexually dimorphic dipteran species in which predominant male and female cuticular hydrocarbons are mutually exchanged during mating. Using synthetic compounds, the effect of this exchange on the post-mating sexual attractiveness of both males and females was tested. The sex-predominant hydrocarbons acquired during mating decreased the attractiveness of both males and females to members of the other sex. Mated females are courted less actively than virgins, and are usually unwilling to re-mate. Similarly, recently mated males are less attractive to females than virgin males are, and may be less fertile. Thus, cuticular hydrocarbons acquired by the other sex during mating could allow both males and females to assess the immediate reproductive potential of prospective mates.     

Environmental conditions affect spatial genetic structures and dispersal patterns in a solitary rodent

The study of the spatial distribution of relatives in a population under contrasted environmental conditions provides critical insights into the flexibility of dispersal behaviour and the role of environmental conditions in shaping population relatedness and social structure. Yet few studies have evaluated the effects of fluctuating environmental conditions on relatedness structure of solitary species in the wild. The aim of this study was to determine the impact of interannual variations in environmental conditions on the spatial distribution of relatives [spatial genetic structure (SGS)] and dispersal patterns of a wild population of eastern chipmunks (Tamias striatus), a solitary rodent of North America. Eastern chipmunks depend on the seed of masting trees for reproduction and survival. Here, we combined the analysis of the SGS of adults with direct estimates of juvenile dispersal distance during six contrasted years with different dispersal seasons, population sizes and seed production. We found that environmental conditions influences the dispersal distances of juveniles and that male juveniles dispersed farther than females. The extent of the SGS of adult females varied between years and matched the variation in environmental conditions. In contrast, the SGS of males did not vary between years. We also found a difference in SGS between males and females that was consistent with male‐biased dispersal. This study suggests that both the dispersal behaviour and the relatedness structure in a population of a solitary species can be relatively labile and change according to environmental conditions.     

Meiotic drive and evolution of female choice.

As a special version of the good-genes hypothesis, it was recently proposed that females could benefit from choosing drive-resistant males in a meiotic drive system. Here, we examine with a three-locus, six-allele population genetic model whether female choice for drive resistance can evolve. An allele leading to female preference for drive-resistant males was introduced at low frequency into a population polymorphic for meiotic drive and drive resistance. Our simulations show that female choice of drive-resistant males is disadvantageous when resistance is Y-linked. This disadvantage occurs because, at equilibrium, drive-resistant males have lower reproductive success than drive-susceptible males. Thus, female choice of drive-susceptible males can evolve when resistance is Y-linked. When resistance is autosomal, selection on female choice for drive resistance is less strong and depends on the frequency of choice: female preference of resistant males is favoured when choice is rare and disadvantageous when choice is frequent, leading to a stable equilibrium at a low frequency of the choice allele. Independent of the location of drive resistance alleles, males with the non-driving allele always have above average reproductive success. Female choice is therefore beneficial when choosy females prefer males with the non-driving allele.     

Sex‐specific recombination rates and allele frequencies affect the invasion of sexually antagonistic variation on autosomes

The introduction and persistence of novel, sexually antagonistic alleles can depend upon factors that differ between males and females. Understanding the conditions for invasion in a two‐locus model can elucidate these processes. For instance, selection can act differently upon the sexes, or sex linkage can facilitate the invasion of genetic variation with opposing fitness effects between the sexes. Two factors that deserve further attention are recombination rates and allele frequencies – both of which can vary substantially between the sexes. We find that sex‐specific recombination rates in a two‐locus diploid model can affect the invasion outcome of sexually antagonistic alleles and that the sex‐averaged recombination rate is not necessarily sufficient to predict invasion. We confirm that the range of permissible recombination rates is smaller in the sex benefitting from invasion and larger in the sex harmed by invasion. However, within the invasion space, male recombination rate can be greater than, equal to or less than female recombination rate in order for a male‐benefit, female‐detriment allele to invade (and similarly for a female‐benefit, male‐detriment allele). We further show that a novel, sexually antagonistic allele that is also associated with a lowered recombination rate can invade more easily when present in the double heterozygote genotype. Finally, we find that sexual dimorphism in resident allele frequencies can impact the invasion of new sexually antagonistic alleles at a second locus. Our results suggest that accounting for sex‐specific recombination rates and allele frequencies can determine the difference between invasion and non‐invasion of novel, sexually antagonistic alleles in a two‐locus model.     

How to go extinct by mating too much: population consequences of male mate choice and efficiency in a sexual–asexual species complex

Selection acting on individuals is not predicted to maximize population persistence, yet examples that explicitly quantify conflicts between individual and population level benefits are scarce. One such conflict occurs over sexual reproduction because of the cost of sex: sexual populations that suffer the cost of producing males have only half the growth rate compared to asexuals. Male behaviour can additionally impact population dynamics in a variety of ways, and here we study an example where the impact is unusually clear: the riddle of persistence of sperm‐dependent sexual–asexual species complexes. Here, a sexually reproducing host species coexists with an ameiotically reproducing all‐female sperm parasite. Sexual–asexual coexistence should not be stable because the proportion of asexually reproducing females will rapidly increase and the relative abundance of the sexually reproducing host species will decline. A severe shortage of males will lead to sperm limitation for sexual and asexual females and the system collapses. Male mate choice could reduce the reproductive potential of the asexual species and thus potentially prevent the collapse. In the gynogenetic (sperm‐dependent parthenogenetic) Amazon molly Poecilia formosa and its host (P. latipinna or P. mexicana), males discriminate against asexual females to some extent. Using a population‐dynamical model, we examine the population dynamics of this species complex with varying strengths of male discrimination ability and efficiency with which they locate females and produce sperm. The sexual species would benefit from stronger discrimination, thus preventing being displaced by the asexual females. However, males would be required to evolve preferences that are probably too strong to be purely based upon selection acting on individuals. We conclude that male behaviour does not fully prevent but delays extinction, yet this is highly relevant because low local extinction rates strongly promote coexistence as a metapopulation.     

A dominant allele controls development into female mimic male and diminutive female ruffs

Maintaining polymorphisms for genes with effects of ecological significance may involve conflicting selection in males and females. We present data from a captive population of ruffs (Philomachus pugnax) showing that a dominant allele controls development into both small, ‘female mimic’ males (‘faeders’), and a previously undescribed class of small ‘female faeders’. Most male ruffs have elaborate breeding plumage and display behaviour, but 0.5–1.5% are faeders, which lack both. Females from a captive population previously lacking faeders were bred with two founder faeder males and their faeder sons. The faeders’ offspring had a quadrimodal size distribution comprising normal-sized males and females, faeders and atypically small females. By contrast, ornamented males fathered only normal-sized offspring. We conclude that both founding faeders were heterozygous for a faeder allele absent from the original population. This allele is dominant to previously described genes that determine development into independent versus satellite ornamented males. Unlike those genes, the faeder allele is clearly expressed in females. Small body size is a component of the male faeder mating strategy, but provides no obvious benefit to females. Bisexual expression of the gene provides the opportunity to quantify the strength of sexually antagonistic selection on a Mendelian trait.     

Female brown-headed cowbirds', Molothrus ater, organization and behaviour reflects male social dynamics

In four large aviaries, we studied social assortment and reproductive behaviour of female brown-headed cowbirds housed with males differing in age class and in corresponding levels of intrasexual interaction. Juvenile and adult females resided with either (1) adult males, (2) juvenile males, (3) adult and juvenile males, or (4) no males. We observed social behaviour of males and females from September 1999 through to the 2000 breeding season. Throughout the year, males in the different conditions showed different levels of social interaction, with adult males being most engaged in male-male interactions and juvenile males being least engaged in male-male interactions. Females in the four conditions differed in their associations with males and with other females. In conditions with adult males, females spent more time near males, approached males more often, and associated with females less. During the breeding season, females in conditions with more adult males copulated more and produced more fertile and viable eggs. In the condition where females were housed with juvenile males, they copulated less, laid fewer eggs and destroyed more of their eggs. Results indicate that throughout the year, females are sensitive to male age and behaviour in their social group, and that this sensitivity can have reproductive consequences. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Sperm competition and the dynamics of X chromosome drive: stability and extinction

Several empirical studies of sperm competition in populations polymorphic for a driving X chromosome have revealed that Sex-ratio males (those carrying a driving X) are at a disadvantage relative to Standard males. Because the frequency of the driving X chromosome determines the population-level sex ratio and thus alters male and female mating rates, the evolutionary consequences of sperm competition for sex chromosome meiotic drive are subtle. As the SR allele increases in frequency, the ratio of females to males also increases, causing an increase in the male mating rate and a decrease in the female mating rate. While the former change may exacerbate the disadvantage of Sex-ratio males during sperm competition, the latter change decreases the incidence of sperm competition within the population. We analyze a model of the effects of sperm competition on a driving X chromosome and show that these opposing trends in male and female mating rates can result in two coexisting locally stable equilibria, one corresponding to a balanced polymorphism of the SR and ST alleles and the second to fixation of the ST allele. Stochastic fluctuations of either the population sex ratio or the SR frequency can then drive the population away from the balanced polymorphism and into the basin of attraction for the second equilibrium, resulting in fixation of the SR allele and extinction of the population.     

Effects of avpr1a length polymorphism on male social behavior and reproduction in semi‐natural populations of prairie voles (Microtus ochrogaster)

Intraspecific variation in sociosexual behavior has typically been investigated in the context of its relationship with environmental factors, but neurogenetic factors can also influence sociosexual behavior. In laboratory studies of prairie voles (Microtus ochrogaster), length polymorphism of microsatellite DNA within the gene (avpr1a) encoding the vasopressin 1a receptor is correlated with variation in male sociosexual behavior. However, field studies of prairie voles have found the relationship between male avpr1a microsatellite allele length and sociosexual behavior to be more ambiguous, possibly because most males had alleles of intermediate length. We tested the hypothesis that avpr1a microsatellite allele length mediates male sociosexual behavior in field settings by releasing voles into field enclosures where every male possessed two avpr1a microsatellite alleles at least one standard error longer or shorter than the mean length in their population of origin. Voles from an Illinois and Kansas population were examined separately as social monogamy appears more prevalent in the Illinois population. Illinois males with long avpr1a microsatellite alleles had smaller home ranges and overlapped a greater proportion of the home range of the female that they overlapped the most. Kansas males showed the opposite pattern. Illinois, but not Kansas, males with long avpr1a microsatellite alleles sired offspring with more females and sired more litters. Our results support the hypothesis that genetic variation associated with the avpr1a gene plays a role in mediating male prairie vole sociosexual behavior in nature. However, the relationship between specific male behaviors and male avpr1a microsatellite allele length sometimes differed significantly between Kansas and Illinois voles, suggesting relationships between specific male sociosexual behaviors and polymorphism associated with the avpr1a locus are complex, possibly involving specific nucleotide sequences or other population‐specific genetic differences.     

Individual MHC class I and MHC class IIB diversities are associated with male and female reproductive traits in the three-spined stickleback

Genes of the major histocompatibility complex (MHC) are indispensable for pathogen defence in vertebrates. With wild-caught three-spined sticklebacks (Gasterosteus aculeatus) we conducted the first study to relate individual reproductive parameters to both MHC class I and II diversities. An optimal MHC class IIB diversity was found for male nest quality. However, male breeding colouration was most intense at a maximal MHC class I diversity. One MHC class I allele was associated with male redness. Similarly, one MHC class IIB allele was associated with continuous rather than early female reproduction, possibly extending the reproductive period. Both alleles occurred more frequently with increasing individual allele diversity. We suggest that if an allele is currently not part of the optimum, it had not been propagated by choosy females. The parasite against which this allele provides resistance is therefore unlikely to have been predominant the previous year - a step to negative frequency-dependent selection.