Lack of behavioural evidence for kin avoidance in mate choice in a hymenopteran parasitoid (Hymenoptera: Braconidae)

Mechanisms for inbreeding avoidance should be prevalent in insects that reproduce by arrhenotokous haplodiploidy because of the higher potential production of unviable diploid males in inbred matings. Few studies have focused on mating strategies in insect parasitoids and even less on kinship relationships during mate choice. In this study we tested avoidance of kin as mate in the parasitic wasp Aphidius matricariae (Hymenoptera: Braconidae) using an ethological approach. Key mating parameters, such as male wing fanning, latent period before genitalia contact and duration of copulation were measured. No evidence for kin avoidance in mate choice in both A. matricariae males and females was observed in our behaviour (no choice or choice tests) tests. This lack of ethological sib mating avoidance could be due to different factors such as sex determination rule different than the single locus complementary sex determination, making lower the proportion of diploid males in case of sib matings and thus its negative consequence. The existence of other inbreeding avoidance strategies and mechanisms that reduce the probability of 2 receptive relatives meeting in nature may be common, for example, inbred mating may be rare through differential dispersal, delayed maturation, or protandry.     

Monogamous male mice bias behaviour towards females according to very small differences in kinship

To the extent that relatedness between mates predicts their reproductive success, individuals are expected to bias their behaviours towards opposite-sex conspecifics according to differences in kinship. Here we show that monogamous male oldfield mice, Peromyscus polionotus rhoadsi, bias their social behaviour towards unfamiliar, distantly related females according to an average 1.3% difference in their kinship to these potential mates. Males in the present study favoured less-related females. Previous empirical investigations have not demonstrated behavioural biases based on such small kinship differences. Consequently, these small differences in kinship have been considered inadequate to drive the evolution of mate choice, particularly by males. Even a small incremental difference in mate quality, however, may significantly affect male reproductive success, especially for monogamous species or those that require maternal care. This study has demonstrated that the social preferences of male oldfield mice are distributed between females according to small differences in their kinship to these potential mates. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

No evidence for inbreeding avoidance in a great reed warbler population

Inbreeding depression may drive the evolution of inbreedingavoidance through dispersal and mate choice. In birds, manyspecies show female-biased dispersal, which is an effectiveinbreeding avoidance mechanism. In contrast, there is scarceevidence in birds for kin discriminative mate choice, whichmay, at least partly, reflect difficulties detecting it. First,kin discrimination may be realized as dispersal, and this isdifficult to distinguish from other causes of dispersal. Second,even within small, isolated populations, it is often difficultto determine the potential candidates available to a femalewhen choosing a mate. We sought evidence for inbreeding avoidancevia kin discrimination in a breeding population of great reedwarblers (Acrocephalus arundinaceus) studied over 17 years.Inbreeding depression is strong in the population, suggestingthat it would be adaptive to avoid relatives as mates. Detaileddata on timing of settlement and mate search movements madeit possible to identify candidate mates for each female, andlong-term pedigrees and resolved parentage enabled us to estimaterelatedness between females and their candidate mates. We foundno evidence for kin discrimination: mate choice was random withrespect to relatedness when all mate-choice events were considered,and, after correction for multiple tests, also in all breedingyears. We suggest that dispersal is a sufficient inbreedingavoidance mechanism in most situations, although the lack ofkin discriminative mate choice has negative consequences forsome females, because they end up mating with closely relatedmales that lowers their fitness.     

Effect of kinship on social behaviors in Brandt's voles (<Emphasis Type="Italic">Microtus brandti</Emphasis>)

The roles of kinship in agonistic behavior and mate choice were evaluated in Brandt's voles (Microtus brandti). In chambers bedded with familiar or unfamiliar substrates, the aggressive behavior and social investigation towards adult unfamiliar same-sex siblings and non-siblings were examined, and no significant kin bias was found. Males sniffed and followed unfamiliar unrelated females significantly more than unfamiliar sibling sisters, but males did not show significant preferences in copulatory behavior and agonistic behavior. Females spent significantly more time copulating with unfamiliar unrelated males than with their unfamiliar sibling brothers, while they did not show a significant preference in social investigation between them. Our study shows that kinship might play a role in the inbreeding avoidance based on preweaning familiarity or/and phenotype matching, but the role of kinship in agonistic behavior remains unclear.     

Variation in ant aggression and kin discrimination ability within and between colonies

Significant variation in aggressiveness and kin discrimination ability occurs between different laboratory colonies of the ant Rhytidoponera confusa.Different colonies show consistently high (or low) levels of aggression toward nonnestmates over 4–19 weeks. Earlier studies excluded colony size and the natural presence or absence of the queen in colonies and differences in hunger as possible sources of variation. The present study excluded the number of larvae in colonies and the time of the light period of the light cycle when recognition tests were carried out. Highly significant variation occurs between the kin discrimination ability of individual workers in any particular colony. Approximately 28% of the workers in colonies of R. confusashowed very poor kin discrimination. Much of the colony's kin discrimination is carried out by a small number of highly aggressive workers.     

Female rhesus macaques discriminate unfamiliar paternal sisters in playback experiments: support for acoustic phenotype matching

Widespread evidence exists that when relatives live together, kinship plays a central role in shaping the evolution of social behaviour. Previous studies showed that female rhesus macaques (Macaca mulatta) recognize familiar maternal kin using vocal cues. Recognizing paternal kin might, however, be more difficult as rhesus females mate promiscuously during the possible conception period, most probably concealing paternity. Behavioural observations indicate that semi free-ranging female rhesus macaques prefer to associate with their paternal half-sisters in comparison to unrelated females within the same group, particularly when born within the same age cohort. However, the cues and mechanism/s used in paternal kin discrimination remain under debate. Here, we investigated whether female rhesus macaques use the acoustic modality to discriminate between paternal half-sisters and non-kin, and tested familiarity and phenotype matching as the underlying mechanisms. We found that test females responded more often to calls of paternal half-sisters compared with calls of unrelated females, and that this discrimination ability was independent of the level of familiarity between callers and test females, which provides, to our knowledge, the first evidence for acoustic phenotype matching. Our study strengthens the evidence that female rhesus macaques can recognize their paternal kin, and that vocalizations are used as a cue.     

Female‐biased dispersal alone can reduce the occurrence of inbreeding in black grouse (Tetrao tetrix)

Although inbreeding depression and mechanisms for kin recognition have been described in natural bird populations, inbreeding avoidance through mate choice has rarely been reported suggesting that sex‐biased dispersal is the main mechanism reducing the risks of inbreeding. However, a full understanding of the effect of dispersal on the occurrence of inbred matings requires estimating the inbreeding risks prior to dispersal. Combining pairwise relatedness measures and kinship assignments, we investigated in black grouse whether the observed occurrence of inbred matings was explained by active kin discrimination or by female‐biased dispersal. In this large continuous population, copulations between close relatives were rare. As female mate choice was random for relatedness, females with more relatives in the local flock tended to mate with genetically more similar males. To quantify the initial risks of inbreeding, we measured the relatedness to the males of females captured in their parental flock and virtually translocated female hatchlings in their parental and to more distant flocks. These tests indicated that dispersal decreased the likelihood of mating with relatives and that philopatric females had higher inbreeding risks than the actual breeding females. As females do not discriminate against relatives, the few inbred matings were probably due to the variance in female dispersal propensity and dispersal distance. Our results support the view that kin discrimination mate choice is of little value if dispersal effectively reduces the risks of inbreeding.     

No Evidence of Intersexual Kin Recognition by Males of the Neotropical Paper Wasp <Emphasis Type="Italic">Polistes versicolor</Emphasis>

We investigated the effect of kinship on mate selection by males of the neotropical primitively eusocial paper wasp Polistes versicolor. By conducting short-time, paired, consecutive, dyadic encounters, in which a male was randomly introduced separately to a related and an unrelated female in a small glass arena, we were able to observe and measure the male sexual display. We found that male sexual interest toward a female was not affected by kinship, even after controlling the differences in female behavior. Despite our finding that males were as eager to harass females, regardless of kinship, previous evidence suggested that incestuous copulation (inbreeding) in natural populations of P. versicolor appeared to be avoided. We suggest that in the natural mating habitat of the native population that we studied, in which many colonies were able to produce males and reproductive females in a short time window, the probability of finding related sexual partners was low, hence, intersexual kin discrimination did not evolve.     

Kinship and mate choice in a historic eastern Blue Ridge community, Madison County, Virginia

Potential mates analysis is difficult to apply to small historic populations that lack clear boundaries or regular vital event registration. Here I analyze the actual mate pool as an alternative way to identify causes of nonrandom mating when unmarried members are unknown. Factors influencing mate choice within a historic eastern Blue Ridge community in Madison County, Virginia, are examined for four marriage cohorts: 1850-1879, 1880-1899, 1900-1919, and 1920-1939. These factors include nuclear kin avoidance, preferred age differences between mates, and preferences for more distant kin. A simulation is used to recombine members of the cohort-specific pools of married individuals to generate the probabilities of various types of kin marriages. The pedigree and vital statistics data are derived from first-time marriage licenses filled by community members in Madison County from 1794 to 1939. The numbers of marriages examined for each cohort are 88, 120, 132, and 132, respectively; the mate pools constructed from the samples are viewed from the female perspective. The results generated by simulation on the actual mate pools consist of mean kinship coefficients, numbers of marriages between "allowed" kin types, and probabilities of these values when marriage is random with respect to kinship. The results indicate significantly high levels of inbreeding in all four marriage cohorts, primarily because of high levels of first-cousin marriages in the first three cohorts and of first-cousin once-removed marriages in the 1920 cohort. The observed mating patterns are discussed in terms of the social history of the Blue Ridge community and restrictions of the data.     

Paternal kin discrimination: the evidence and likely mechanisms

One of the most important assumptions of kin selection theory is that individuals behave differently towards kin than non-kin. In mammals, there is strong evidence that maternal kin are distinguished from non-kin via familiarity. However, little is known about whether or not mammals can also recognize paternal kin as many female mammals, including primates, mate with multiple males near the time of conception, potentially concealing paternal kinship. Genetic data in several mammalian species with a promiscuous mating system and male-biased dispersal reveal a high skew in male reproduction which leads to co-residing paternal half-siblings. In most primates, individuals also form stable bisexual groups creating opportunities for males to interact with their offspring. Here I consider close paternal kin co-resident in the same social group, such as father-offspring and paternal half-siblings (i.e. animals sharing the same father but who were born to different mothers) and review mammalian studies of paternal kin discrimination. Furthermore, I summarize the most likely mechanisms of paternal kin discrimination (familiarity and phenotype matching). When familiarity is the underlying mechanism, mothers and/or the sire could mediate familiarity among paternal half-siblings as well as between fathers and offspring assuming mothers and/or fathers can assess paternity. When animals use phenotype matching, they might use their fathers' template (when the father is present) or self (when the father is absent) to assess paternal kinship in others. Available evidence suggests that familiarity and phenotype matching might be used for paternal kin discrimination and that both mechanisms might apply to a wide range of social mammals characterized by a high skew in male reproduction and co-residence of paternal kin. Among primates, suggested evidence for phenotype matching can often have an alternative explanation, which emphasizes the crucial importance of controlling for familiarity as a potential confounding variable. However, the mechanism/s used to identify paternal kin might differ within a species (as a function of each individual's specific circumstances) as well as among species (depending upon the key sensory modalities of the species considered). Finally, I discuss the possible cues used in paternal kin discrimination and offer suggestions for future studies.     

Low relatedness among cooperatively breeding workers of the greenhead ant Rhytidoponera metallica

The greenhead ant Rhytidoponera metallica has long been recognized as posing a potential challenge to kin selection theory, because it has large queenless colonies where apparently many of the morphological workers are mated and reproducing. However, this species has never been studied genetically and important elements of its breeding system and kin structure remain uncertain. We used microsatellite markers to measure the relatedness among nestmates, unravel the fine‐scale population genetic structure, and infer the breeding system of R. metallica. The genetic relatedness among worker nestmates is very low but significantly greater than zero (r=0.082 ± 0.015), which demonstrates that nests contain many distantly related breeders. The inbreeding coefficient is very close to and not significantly different from zero, indicating random mating and lack of microgeographic genetic differentiation. On average, closely located nests are not more similar genetically than distant nests, which is surprising, as new colonies form by budding and female dispersal is restricted. Lack of inbreeding and absence of population viscosity indicates high gene flow mediated by males. Overall, the genetic pattern detected in R. metallica suggests that a high number of moderately related workers mate with unrelated males from distant nests. This breeding system results in the lowest relatedness among nestmates reported for social insect species where breeders and helpers are not morphologically differentiated.     

Optional gamergates in the queenright ponerine ant Gnamptogenys striatula Mayr

Summary: Ponerine ants display a number of social structures to which particular behaviours are associated. In the ponerine ant species Gnamptogenys striatula Mayr, queens occur and queenright colonies are functionally polygynous. However, some workers are capable to mate and to produce their own worker offspring. These gamergates appear several days after the queens are experimentally removed, allowing some workers to adopt a sexual calling posture inside the nest. At that time, other workers get outside the nest to collect males in the arena and carry them back into the colony. There, these males are groomed before they can mate with sexual calling workers. As for queens, several gamergates may coexist in a same colony. The social profile of gamergates is similar to those of nurses and they stay closer to the egg piles.     

Are you my mother? Kin recognition in the ant Formica fusca

In social insects, workers trade personal reproduction for indirect fitness returns from helping their mother rear collateral kin. Colony membership is generally used as a proxy for kin discrimination, but the question remains whether recognition allows workers to discriminate between kin and nonkin regardless of colony affiliation. We investigated whether workers of the ant Formica fusca can identify their mother when fostered with their mother, their sisters, a hetero‐colonial queen or hetero‐colonial workers. We found that workers always displayed less aggression towards both their mother and their foster queen, as compared to an unfamiliar hetero‐colonial queen. In support of this finding, workers maintain their colony hydrocarbon profile regardless of foster regime, yet show modifications when exposed to different environments. This indicates that recognition entails environmental and genetic components, which allow both discrimination of kin in the absence of prior contact and learning of recognition cues based on group membership.     

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.     

Absence of Within‐Colony Kin Discrimination in a Multiple‐Queen Ant,Leptothorax acervorum

Inclusive fitness theory predicts that, other things equal, individuals within social groups should direct altruistic behaviour towards their most highly related group‐mates to maximise indirect fitness benefits. In the social insects, most previous studies have shown that within‐colony kin discrimination (nepotism) is absent or weak. However, the number of studies that have investigated within‐colony kin discrimination at the level of individual behaviour remains relatively small. We tested for within‐colony kin discrimination in the facultatively multiple‐queen (polygynous) ant, Leptothorax acervorum. Specifically, we tested whether workers within polygynous colonies treated queens differently as a function of their relatedness to them. Colonies containing two egg‐laying queens were filmed to measure the rate at which individually marked workers antennated and groomed or fed each queen. Relatedness between individual queens and workers was calculated from their genotypes at four microsatellite loci. The results showed there were no differences in the rates at which workers antennated or groomed/fed their more related queen and their less related queen. Workers interacted preferentially with their potential mother queen with respect to grooming/feeding but not with respect to antennation. However, because of high queen turnover, the frequency of adult workers with their potential mother queen still present within the colony was relatively low. Overall, therefore, we found no evidence for within‐colony kin discrimination in the context of the average worker's treatment of queens in polygynous L. acervorum colonies.     

Female‐biased sex allocation and lack of inbreeding avoidance in Cubitermes termites

Sexually reproducing organisms face a strong selective pressure to find a mate and ensure reproduction. An important criterion during mate‐selection is to avoid closely related individuals and subsequent potential fitness costs of resulting inbred offspring. Inbreeding avoidance can be active through kin recognition during mate choice, or passive through differential male and female‐biased sex ratios, which effectively prevents sib‐mating. In addition, sex allocation, or the resources allotted to male and female offspring, can impact mating and reproductive success. Here, we investigate mate choice, sex ratios, and sex allocation in dispersing reproductives (alates) from colonies of the termite Cubitermes tenuiceps. Termites have a short time to select a mate for life, which should intensify any fitness consequences of inbreeding. However, alates did not actively avoid inbreeding through mate choice via kin recognition based on genetic or environmental cues. Furthermore, the majority of colonies exhibited a female‐biased sex ratio, and none exhibited a male‐bias, indicating that differential bias does not reduce inbreeding. Sex allocation was generally female‐biased, as females also were heavier, but the potential fitness effect of this costly strategy remains unclear. The bacterium Wolbachia, known in other insects to parasitically distort sex allocation toward females, was present within all alates. While Wolbachia is commonly associated with termites, parasitism has yet to be demonstrated, warranting further study of the nature of the symbiosis. Both the apparent lack of inbreeding avoidance and potential maladaptive sex allocation implies possible negative effects on mating and fitness.     

Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate

The widespread belief that kin selection is necessary for the evolution of cooperative breeding in vertebrates has recently been questioned. These doubts have primarily arisen because of the paucity of unequivocal evidence for kin preferences in cooperative behaviour. Using the cooperative breeding system of long-tailed tits (Aegithalos caudatus) in which kin and non-kin breed within each social unit and helpers are failed breeders, we investigated whether helpers preferentially direct their care towards kin following breeding failure. First, using observational data, we show that not all failed breeders actually become helpers, but that those that do help usually do so at the nest of a close relative. Second, we confirm the importance of kinship for helping in this species by conducting a choice experiment. We show that potential helpers do not become helpers in the absence of close kin and, when given a choice between helping equidistant broods belonging to kin and non-kin within the same social unit, virtually all helped at the nest of kin. This study provides strong evidence that kinship plays an essential role in the maintenance of cooperative breeding in this species.     

Kinship alters the effects of forced cohabitation on body weight,mate choice and fitness in the rat-like hamster Tscheskia triton

It has been documented that social isolation imparts deleterious effects on gregarious rodents species,but caging in group imparts such effects on solitary rodents. This study was attempted at examining how kinship to affect body weight,behavioral interaction,mate choice and fitness when we caged male and female rat-like hamsters Tscheskia triton in pair,a solitary species. We found that females paired with nonsibling males became heavier than the females paired with sibling males,but both agonistic and amicable behavior between paired males and females did not differ between sibling and nonsibling groups. This indicated that kinship might reduce females' obesity in response to forced cohabitation,and dissociation might exist between physiological and behavioral responses. Furthermore,binary choice tests revealed that social familiarity between either siblings or nonsiblings decreased their investigating time spent in opposite sex conspecific of cage mates and/or their scents as compared with those of nonmates,suggesting effects of social association on mate and kin selection of the hamsters. On the other side,both females and males caged in pair with siblings show a preference between unfamiliar siblings or their scents and the counterparts of nonsiblings after two month separation,indicating that the kin recognition of the hamsters might also rely on phenotype matching. In addition,cohabitation (or permanent presence of fathers) elicited a lower survival of pups in nonsibling pairs than sibling pairs,but did not affect litter size,suggesting that kinship affects fitness when housing male and female ratlike hamsters together. Therefore,inbreeding might be adapted for rare and endangered animals.     

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.     

Distribution of Affiliative Behavior Across Kin Classes and Their Fitness Consequences in Mandrills

Multimale–multifemale primate groups are ideal models to study the impact of kinship on the evolution of sociality. Indeed, the frequent combination of female philopatry and male reproductive skew produces social systems where both maternal and paternal kin are co‐resident. Several primates are known to bias their behavior toward both maternal and paternal kin. Moreover, allocation of affiliation toward paternal kin has been shown to depend on the availability in maternal kin: Female baboons invest more in paternal kin after the loss of preferred maternal kin. Here, we examined how affiliation co‐varies across kin classes in juvenile mandrills (Mandrillus sphinx), an Old World primate living in a multimale–multifemale society. While affiliation levels observed with the mother and with maternal half‐sibs co‐varied positively, especially in young females, we found that levels of affiliation among paternal half‐sibs correlated negatively with levels of affiliation among individuals from the same matriline (distant kin), possibly as a result of kin availability. In addition, in social species, social bonds between individuals have been linked to differentiated fitness consequences: More socially integrated individuals generally enjoy higher fitness. We therefore also tested whether affiliation during early life impacts fitness. We showed that the global amount of affiliation during juvenescence translated into possible reproductive benefits: Females who were more socially integrated gave birth on average a year before females that were less socially integrated. However, age at first reproduction was not predicted by the amount of affiliation exchanged with any particular kin class. These results add to the growing body of evidence demonstrating differential investment in bonding and possible social adjustments among different kin categories and emphasizing once more the adaptive value of sociality.