No evidence for divergence in male harmfulness or female resistance in response to changes in the opportunity for dispersal

The outcome of sexual conflict can depend on the social environment, as males respond to changes in the inclusive fitness payoffs of harmfulness and harm females less when they compete with familiar relatives. Theoretical models also predict that if limited male dispersal predictably enhances local relatedness while maintaining global competition, kin selection can produce evolutionary divergences in male harmfulness among populations. Experimental tests of these predictions, however, are rare. We assessed rates of dispersal in female and male seed beetles Callosobruchus maculatus, a model species for studies of sexual conflict, in an experimental setting. Females dispersed significantly more often than males, but dispersing males travelled just as far as dispersing females. Next, we used experimental evolution to test whether limiting dispersal allowed the action of kin selection to affect divergence in male harmfulness and female resistance. Populations of C. maculatus were evolved for 20 and 25 generations under one of three dispersal regimens: completely free dispersal, limited dispersal and no dispersal. There was no divergence among treatments in female reproductive tract scarring, ejaculate size, mating behaviour, fitness of experimental females mated to stock males or fitness of stock females mated to experimental males. We suggest that this is likely due to insufficient strength of kin selection rather than a lack of genetic variation or time for selection. Limited dispersal alone is therefore not sufficient for kin selection to reduce male harmfulness in this species, consistent with general predictions that limited dispersal will only allow kin selection if local relatedness is independent of the intensity of competition among kin.     

No evidence that relatedness or familiarity modulates male harm in Drosophila melanogaster flies from a wild population

Sexual selection frequently promotes the evolution of aggressive behaviors that help males compete against their rivals, but which may harm females and hamper their fitness. Kin selection theory predicts that optimal male–male competition levels can be reduced when competitors are more genetically related to each other than to the population average, contributing to resolve this sexual conflict. Work in Drosophila melanogaster has spearheaded empirical tests of this idea, but studies so far have been conducted in laboratory‐adapted populations in homogeneous rearing environments that may hamper kin recognition, and used highly skewed sex ratios that may fail to reflect average natural conditions. Here, we performed a fully factorial design with the aim of exploring how rearing environment (i.e., familiarity) and relatedness affect male–male aggression, male harassment, and overall male harm levels in flies from a wild population of Drosophila melanogaster, under more natural conditions. Namely, we (a) manipulated relatedness and familiarity so that larvae reared apart were raised in different environments, as is common in the wild, and (b) studied the effects of relatedness and familiarity under average levels of male–male competition in the field. We show that, contrary to previous findings, groups of unrelated‐unfamiliar males were as likely to fight with each other and harass females than related‐familiar males and that overall levels of male harm to females were similar across treatments. Our results suggest that the role of kin selection in modulating sexual conflict is yet unclear in Drosophila melanogaster, and call for further studies that focus on natural populations and realistic socio‐sexual and ecological environments.     

Kin selection and the evolution of sexual conflict

Males and females do not always share the same evolutionary interests. This is particularly true in the case of multiple mating, where male–male competition can often lead to adaptations that are harmful to the female, and females can evolve counter adaptations to reduce the benefits males gain from such traits. Although social evolution has made substantial progress from kin selection theory, most studies of sexual conflict have ignored the effects of genetic relatedness. Here, I use a model of male harm and female resistance to investigate how kin selection affects the evolution of sexual conflict. Building on models of social evolution, I show that relatedness inhibits sexual conflict, in terms of male harm, whereas it has no effect on the evolution female resistance. This study examines a previously neglected mechanism that can potentially help to resolve sexual conflict over mating and highlights the potential importance of considering relatedness in empirical studies of sexual conflict.     

Paternity analyses in wild‐caught and laboratory‐reared Caribbean cricket females reveal the influence of mating environment on post‐copulatory sexual selection

Polyandry is ubiquitous in insects and provides the conditions necessary for male‐ and female‐driven forms of post‐copulatory sexual selection to arise. Populations of Amphiacusta sanctaecrucis exhibit significant divergence in portions of the male genitalia that are inserted directly into the female reproductive tract, suggesting that males may exercise some post‐copulatory control over fertilization success. We examine the potential for male–male and male–female post‐copulatory interactions to influence paternity in wild‐caught females of A. sanctaecrucis and contrast our findings with those obtained from females reared in a high‐density laboratory environment. We find that female A. sanctaecrucis exercise control by mating multiple times (females mount males), but that male–male post‐copulatory interactions may influence paternity success. Moreover, post‐copulatory interactions that affect reproductive success of males are not independent of mating environment: clutches of wild‐caught females exhibit higher sire diversity and lower paternity skew than clutches of laboratory‐reared females. There was no strong evidence for last male precedence in either case. Most attempts at disentangling the contributions of male–male and male–female interactions towards post‐copulatory sexual selection have been undertaken in a laboratory setting and may not capture the full context in which they take place – such as the relationship between premating and post‐mating interactions. Our results reinforce the importance of designing studies that can capture the multifaceted nature of sexual selection for elucidating the role of post‐copulatory sexual selection in driving the evolution of male and female reproductive traits, especially when different components (e.g. precopulatory and post‐copulatory interactions) do not exert independent effects on reproductive outcomes.     

Mating system, philopatry and patterns of kinship in the cooperatively breeding subdesert mesite Monias benschi

In the first molecular study of a member of the threatened avian family, Mesitornithidae, we used nine polymorphic microsatellite loci to elucidate parentage, patterns of within-group kinship and occurrence of extra-group paternity in the subdesert mesite Monias benschi, of southwest Madagascar. We found this cooperatively breeding species to have a very fluid mating system. There was evidence of genetic monogamy and polygynandry: of the nine groups with multiple offspring, six contained one breeding pair with unrelated helpers and three contained multiple male and female breeders with related helpers. Although patterns of within-group kinship varied, there was a strong positive relationship between group size and relatedness, suggesting that groups form by natal philopatry. There was also a strong positive correlation between within-sex and between-sex relatedness, indicating that unlike most cooperatively breeding birds, philopatry involved both sexes. In contrast to predictions of kin selection and reproductive skew models, all monogamous groups contained unrelated individuals, while two of the three polygynandrous groups were families. Moreover, although between-group variation in seasonal reproductive success was related to within-group female relatedness, relatedness among males and between the sexes had no bearing on a group's reproductive output. While kin selection may underlie helping behaviour in females, factors such as direct long-term fitness benefits of group living probably determine helping in males. Of the 14 offspring produced by fully sampled groups, at least two were sired by males from neighbouring groups: one by a breeding male and one by a nonbreeding male, suggesting that males may augment their reproductive success through extra-group paternity.     

Does kin selection moderate sexual conflict in Drosophila?

Two recent studies provide provocative experimental findings about the potential influence of kin recognition and cooperation on the level of sexual conflict in Drosophila melanogaster. In both studies, male fruit flies apparently curbed their mate-harming behaviours in the presence of a few familiar or related males, suggesting some form of cooperation mediated by kin selection. In one study, the reduction in agonistic behaviour by brothers apparently rendered them vulnerable to dramatic loss of paternity share when competing with an unrelated male. If these results are robust and generalizable, fruit flies could be a major new focus for the experimental study of kin selection and social evolution. In our opinion, however, the restrictive conditions required for male cooperation to be adaptive in this species make it unlikely to evolve. We investigated these phenomena in two different populations of D. melanogaster using protocols very similar to those in the two previous studies. Our experiments show no evidence for a reduction in mate harm based upon either relatedness or familiarity between males, and no reduction in male reproductive success when two brothers are in the presence of an unfamiliar, unrelated, ‘foreign’ male. Thus, the reduction of sexual conflict owing to male cooperation does not appear to be a general feature of the species, at least under domestication, and these contrasting results call for further investigation: in new populations, in the field and in the laboratory populations in which these phenomena have been reported.     

Sexual selection favours male parental care, when females can choose

Explaining the evolution of male care has proved difficult. Recent theory predicts that female promiscuity and sexual selection on males inherently disfavour male care. In sharp contrast to these expectations, male-only care is often found in species with high extra-pair paternity and striking variation in mating success, where current theory predicts female-only care. Using a model that examines the coevolution of male care, female care and female choice; I show that inter-sexual selection can drive the evolution of male care when females are able to bias mating or paternity towards parental males. Surprisingly, female choice for parental males allows male care to evolve despite low relatedness between the male and the offspring in his care. These results imply that predicting how sexual selection affects parental care evolution will require further understanding of why females, in many species, either do not prefer or cannot favour males that provide care.     

Higher relatedness mitigates mortality in a nematode with lethal male fighting

According to kin selection theory, individuals show less aggression towards their relatives. Limited dispersal promotes interactions among relatives but also increases competition among them. The evolution of cooperation in viscous populations has been subject of mainly theoretical exploration. We investigated the influence of relatedness on aggression in males of entomopathogenic nematode Steinernema longicaudum that engage in lethal fighting. In a series of in vitro experiments, we found that both competitor male group size and relatedness influence male mortality rates. Higher relatedness led to progressively lower rates of male mortality. In experimentally infected insects, wherein large numbers of males and females interact, the proportion of dead and paralysed (= terminally injured) males was higher when infection was established by infective juveniles originating from a mixture of three lines than in those infected by a single line. The results collectively show that Steinernema longicaudum males recognize their kin and consequently male mortality rates are lower in groups consisting of more related males. Furthermore, this monotonic negative relationship between aggression and relatedness suggests that kin selection benefits are still substantial even under extreme competition. Our experiments also suggest that kin recognition in entomopathogenic nematodes has a genetic basis rather than being strictly based on environmental cues. We discuss our findings within the theoretical context of the evolution of altruistic/cooperative behaviour in structured populations.     

Relatedness Does not Affect Competitive Behavior of Rival Males or Offspring Growth in Multiply Sired Litters of Bank Voles (Myodes glareolus)

Kin selection operates through the fitness of an organism's relatives. In the polyandry context, kin selection may be observable on the one hand in competition between rival males and, on the other hand, in competition between litter mates. Sperm competition theory predicts that males should invest less into mating when competing for fertilizations against a close relative as compared to an unrelated male. We tested this hypothesis with bank voles (Myodes glareolus) by mating each focal male to two females: one of which had previously mated with a full sibling of the focal male and the other one with a male unrelated to the focal male. However, we found no effect of rival male relatedness on mating behavior or proportion of offspring sired by the 2nd male to mate. Possibly, the probability of successive mating of related males with the same female is too low in natural bank vole populations for selection to have fine‐tuned mating behavior in relation to rival male relatedness. Further, polyandry often results in litters sired by multiple males. Litter mates of such litters have a reduced relatedness and are thus expected to be less cooperative during gestation and lactation, which may impair growth. Following double matings with either two full‐sibling males or two unrelated males, we compared offspring growth at birth and during lactation. Against our prediction, there was no difference in growth between litters sired either by two full‐sibling males or by two unrelated males. Either the conflict was not severe enough to be visible with our sample size (N = 16) or it may have been resolved by maternal control of offspring provisioning.     

The kin selection hypothesis in a lekking mole cricket: assessing nested patterns of relatedness

Loosely defined, a lek is a male mating aggregation visited by females primarily for the purpose of fertilization. No consensus has been forged that successfully explains how and why leks have evolved across the full breadth of lekking taxa. The two major conceptual explanations (cooperation and competition) are both intricately intertwined in any given system and exhibit varying levels of plasticity based on an organism's environment and life history. The kin selection hypothesis suggests that if females prefer larger leks (as is often the case), unattractive males may aggregate with their attractive relatives in order to boost the latter's reproductive success, while effectively sacrificing any opportunities of their own. Here we develop microsatellite markers to genetically evaluate the kin selection hypothesis by measuring relatedness and precise spatial locations of males in a population of the lekking prairie mole cricket (Gryllotalpa major Saussure). Results indicate that neighbouring males are often highly related, suggesting that kin selection may play some role in this system. However, because leks are comprised of multiple kin groups, if kin selection is operating it is likely doing so at a smaller scale than predicted by the kin selection hypothesis of lek formation. The high levels of subgroup relatedness within this species likely occurs as a passive process due to male viscosity, but the functional implications of this interesting genetic organization remain unknown.     

Differential allocation in a lekking bird: females lay larger eggs and are more likely to have male chicks when they mate with less related males

The differential allocation hypothesis predicts increased investment in offspring when females mate with high-quality males. Few studies have tested whether investment varies with mate relatedness, despite evidence that non-additive gene action influences mate and offspring genetic quality. We tested whether female lekking lance-tailed manakins (Chiroxiphia lanceolata) adjust offspring sex and egg volume in response to mate attractiveness (annual reproductive success, ARS), heterozygosity and relatedness. Across 968 offspring, the probability of being male decreased with increasing parental relatedness but not father ARS or heterozygosity. This correlation tended to diminish with increasing lay-date. Across 162 offspring, egg volume correlated negatively with parental relatedness and varied with lay-date, but was unrelated to father ARS or heterozygosity. Offspring sex and egg size were unrelated to maternal age. Comparisons of maternal half-siblings in broods with no mortality produced similar results, indicating differential allocation rather than covariation between female quality and relatedness or sex-specific inbreeding depression in survival. As males suffer greater inbreeding depression, overproducing females after mating with related males may reduce fitness costs of inbreeding in a system with no inbreeding avoidance, while biasing the sex of outbred offspring towards males may maximize fitness via increased mating success of outbred sons.     

Cryptic female choice favours sperm from major histocompatibility complex-dissimilar males

Cryptic female choice may enable polyandrous females to avoid inbreeding or bias offspring variability at key loci after mating. However, the role of these genetic benefits in cryptic female choice remains poorly understood. Female red junglefowl, Gallus gallus, bias sperm use in favour of unrelated males. Here, we experimentally investigate whether this bias is driven by relatedness per se, or by similarity at the major histocompatibility complex (MHC), genes central to vertebrate acquired immunity, where polymorphism is critical to an individual''s ability to combat pathogens. Through experimentally controlled natural matings, we confirm that selection against related males'' sperm occurs within the female reproductive tract but demonstrate that this is more accurately predicted by MHC similarity: controlling for relatedness per se, more sperm reached the eggs when partners were MHC-dissimilar. Importantly, this effect appeared largely owing to similarity at a single MHC locus (class I minor). Further, the effect of MHC similarity was lost following artificial insemination, suggesting that male phenotypic cues might be required for females to select sperm differentially. These results indicate that postmating mechanisms that reduce inbreeding may do so as a consequence of more specific strategies of cryptic female choice promoting MHC diversity in offspring.     

Absence of Mate Choice and Postcopulatory Benefits in a Species with Extreme Sexual Size Dimorphism

Most hypotheses related to the evolution of female‐biased extreme sexual size dimorphism (SSD) attribute the differences in the size of each sex to selection for reproduction, either through selection for increased female fecundity or selection for male increased mobility and faster development. Very few studies, however, have tested for direct fitness benefits associated with the latter – small male size. Mecaphesa celer is a crab spider with extreme SSD, whose males are less than half the size of females and often weigh 10 times less. Here, we test the hypotheses that larger size in females and smaller size in males are sexually selected through differential pre‐ and postcopulatory reproductive benefits. To do so, we tested the following predictions: matings between small males and large females are more likely to occur due to mate choice; females mated to small males are less likely to accept second copulation attempts; and matings between small males and large females will result in larger clutches of longer‐lived offspring. Following staged mating trials in the laboratory, we found no support for any of our predictions, suggesting that SSD in M. celer may not be driven by pre‐ or post‐reproductive fitness benefits to small males.     

RAPID LOSS OF BEHAVIORAL PLASTICITY AND IMMUNOCOMPETENCE UNDER INTENSE SEXUAL SELECTION

Phenotypic plasticity allows animals to maximize fitness by conditionally expressing the phenotype best adapted to their environment. Although evidence for such adjustment in reproductive tactics is common, little is known about how phenotypic plasticity evolves in response to sexual selection. We examined the effect of sexual selection intensity on phenotypic plasticity in mating behavior using the beetle Callosobruchus maculatus. Male genital spines harm females during mating and females exhibit copulatory kicking, an apparent resistance trait aimed to dislodge mating males. After exposing individuals from male‐ and female‐biased experimental evolution lines to male‐ and female‐biased sociosexual environments, we examined behavioral plasticity in matings with standard partners. While females from female‐biased lines kicked sooner after exposure to male‐biased sociosexual contexts, in male‐biased lines this plasticity was lost. Ejaculate size did not diverge in response to selection history, but males from both treatments exhibited plasticity consistent with sperm competition intensity models, reducing size as the number of competitors increased. Analysis of immunocompetence revealed reduced immunity in both sexes in male‐biased lines, pointing to increased reproductive costs under high sexual selection. These results highlight how male and female reproductive strategies are shaped by interactions between phenotypically plastic and genetic mechanisms of sexual trait expression.     

Kin‐bias,breeding site selection and female fitness in a cannibalistic Neotropical frog

Resource availability influences sexual selection within populations and determines whether behaviours such as territoriality or resource sharing are adaptive. In Thoropa taophora, a frog endemic to the Atlantic Coastal Rainforest of Brazil, males compete for and defend limited breeding sites while females often share breeding sites with other females; however, sharing breeding sites may involve costs due to cannibalism by conspecific tadpoles. We studied a breeding population of T. taophora to determine (i) whether this species exhibits polygynous mating involving female choice for territorial males and limited breeding resources; (ii) whether limited breeding resources create the potential for male–male cooperation in defence of neighbouring territories; and (iii) whether females sharing breeding sites exhibit kin‐biased breeding site choice, possibly driven by fitness losses due to cannibalism among offspring of females sharing sites. We used microsatellites to reconstruct parentage and quantify relatedness at eight breeding sites in our focal population, where these sites are scarce, and in a second population, where sites are abundant. We found that at localities where the appropriate sites for reproduction are spatially limited, the mating system for this species is polygynous, with typically two females sharing a breeding site with a male. We also found that females exhibit negative kin‐bias in their choice of breeding sites, potentially to maximize their inclusive fitness by avoiding tadpole cannibalism of highly related kin. Our results indicate that male territorial defence and female site sharing are likely important components of this mating system, and we propose that kinship‐dependent avoidance in mating strategies may be more general than previously realized.     

The consequences of sexual selection in well‐adapted and maladapted populations of bean beetles†

Whether sexual selection generally promotes or impedes population persistence remains an open question. Intralocus sexual conflict (IaSC) can render sexual selection in males detrimental to the population by increasing the frequency of alleles with positive effects on male reproductive success but negative effects on female fecundity. Recent modeling based on fitness landscape theory, however, indicates that the relative impact of IaSC may be reduced in maladapted populations and that sexual selection therefore might promote adaptation when it is most needed. Here, we test this prediction using bean beetles that had undergone 80 generations of experimental evolution on two alternative host plants. We isolated and assessed the effect of maladaptation on sex‐specific strengths of selection and IaSC by cross‐rearing the two experimental evolution regimes on the alternative hosts and estimating within‐population genetic (co)variance for fitness in males and females. Two key predictions were upheld: males generally experienced stronger selection compared to females and maladaptation increased selection in females. However, maladaptation consistently decreased male‐bias in the strength of selection and IaSC was not reduced in maladapted populations. These findings imply that sexual selection can be disrupted in stressful environmental conditions, thus reducing one of the potential benefits of sexual reproduction in maladapted populations.     

Wasp sex ratios when females on a patch are related

Optimality theory of sex allocation in structured populations has proved remarkably successful in explaining patterns of facultative sex ratio behaviour in numerous species. Extensions to the basic theory have included more specific aspects of species biology, including the relatedness of interacting individuals. We considered the sex ratio decisions made by female Nasonia vitripennis wasps when they were ovipositing on a patch with either relatives or nonrelatives. Theory predicts that females should produce more female-biased sex ratios when ovipositing with relatives, for example sisters, than with unrelated females. This is because related females should limit the level of local mate competition between their sons for female partners. Contrary to theory, two experiments showed that female sex ratio behaviour was unaffected by the relatedness of their oviposition partner, and was also unrelated to an environmental cue that could signal relatedness, i.e. whether females responded differently to sisters emerging from the same or a different host. Instead, in both experiments, we found that only wasp strain significantly influenced sex ratio. A meta-analysis of studies conducted on a range of species on the effects of the relatedness of oviposition partners on sex ratio failed to show the predicted pattern. We discuss why females appear to behave in a maladaptive way when allocating sex under these conditions, and suggest that weak selection and/or conflict between females over optimal sex ratios may influence the evolution of kin discrimination.     

Limited indirect fitness benefits of male group membership in a lekking species

In group living species, individuals may gain the indirect fitness benefits characterizing kin selection when groups contain close relatives. However, tests of kin selection have primarily focused on cooperatively breeding and eusocial species, whereas its importance in other forms of group living remains to be fully understood. Lekking is a form of grouping where males display on small aggregated territories, which females then visit to mate. As females prefer larger aggregations, territorial males might gain indirect fitness benefits if their presence increases the fitness of close relatives. Previous studies have tested specific predictions of kin selection models using measures such as group‐level relatedness. However, a full understanding of the contribution of kin selection in the evolution of group living requires estimating individuals' indirect fitness benefits across multiple sites and years. Using behavioural and genetic data from the black grouse (Tetrao tetrix), we show that the indirect fitness benefits of group membership were very small because newcomers joined leks containing few close relatives who had limited mating success. Males' indirect fitness benefits were higher in yearlings during increasing population density but marginally changed the variation in male mating success. Kin selection acting through increasing group size is therefore unlikely to contribute substantially to the evolution and maintenance of lekking in this black grouse population.     

Kin association during brood care in a facultatively social bird: active discrimination or by‐product of partner choice and demography?

Intra-group relatedness does not necessarily imply kin selection, a leading explanation for social evolution. An overlooked mechanism for generating population genetic structure is variation in longevity and fecundity, referred to as individual quality, affecting kin structure and the potential for cooperation. Individual quality also affects choosiness in partner choice, a key process explaining cooperation through direct fitness benefits. Reproductive skew theory predicts that relatedness decreases with increasing group size, but this relationship could also arise because of quality-dependent demography and partner choice, without active kin association. We addressed whether brood-rearing eider (Somateria mollissima) females preferentially associated with kin using a 6-year data set with individuals genotyped at 19 microsatellite loci and tested whether relatedness decreased with increasing female group size. We also determined the relationship between local relatedness and indices of female age and body condition. We further examined whether the level of female intracoalition relatedness differed from background relatedness in any year. As predicted, median female intra-group relatedness decreased with increasing female group size. However, the proportion of related individuals increased with advancing female age, and older females prefer smaller brood-rearing coalitions, potentially producing a negative relationship between group size and relatedness. There were considerable annual fluctuations in the level of relatedness between coalition-forming females, and in 1year this level exceeded that expected by random association. Thus, both passive and active mechanisms govern kin associations in brood-rearing eiders. Eiders apparently can discriminate between kin, but the benefits of doing so may vary over time.     

The fitness consequences of kin-biased dispersal in a cooperatively breeding bird

Cooperative alliances among kin may not only lead to indirect fitness benefits for group-living species, but can also provide direct benefits through access to mates or higher social rank. However, the immigrant sex in most species loses any potential benefits of living with kin unless immigrants disperse together or recruit relatives into the group in subsequent years. To look for evidence of small subgroups of related immigrants within social groups (kin substructure), we used microsatellites to assess relatedness between immigrant females of the cooperatively breeding superb starling, Lamprotornis superbus. We determined how timing of immigration led to kin subgroup formation and if being part of one influenced female fitness. Although mean relatedness in groups was higher for males than females, 26% of immigrant females were part of a kin subgroup with a sister. These immigrant sibships formed through kin recruitment across years more often than through coalitions immigrating together in the same year. Furthermore, females were more likely to breed when part of a kin subgroup than when alone, suggesting that female siblings form alliances that may positively influence their fitness. Ultimately, kin substructure should be considered when determining the role of relatedness in the evolution of animal societies.