Kin Avoidance Research Articles

Multiple mechanisms for inbreeding avoidance used simultaneously in a wild ape.

Mating with close kin can have considerable negative fitness consequences, which are expected to result in selective pressure for inbreeding avoidance mechanisms, such as dispersal, mate choice and post-copulatory biases. Captive studies have suggested that inbreeding avoidance through mate choice is far less widespread than expected and may be absent where other mechanisms already limit inbreeding. However, few studies have examined multiple mechanisms of inbreeding avoidance simultaneously, particularly in the wild. We use 13 years of detailed dispersal, copulation and paternity data from mountain gorillas to examine inbreeding avoidance. We find that partial dispersal of both sexes results in high kinship in multimale groups, but that copulations between close kin occur 40% less than expected. We find strong kin discrimination in mate choice, with significant avoidance of maternal kin but more limited avoidance of paternal kin. We find no evidence for post-copulatory inbreeding avoidance. Our analyses support familiarity-based mechanisms of kin identification and age-based avoidance that limits mating between fathers and daughters in their natal group. Our findings demonstrate that multiple complementary mechanisms for inbreeding avoidance can evolve in a single species and suggest that inbreeding avoidance through mate choice may enable more flexible dispersal systems to evolve.

Revisiting the hymenopteran diploid male vortex: a review of avoidance mechanisms and incidence

AbstractAll hymenopterans (bees, ants, wasps, and sawflies) have haplodiploid sex determination. Generally, this involves haploid males developing from unfertilized eggs and diploid females developing from fertilized eggs, but diploid male production (DMP) frequently occurs. Some species have complementary sex determination (CSD), in which heterozygotes of a csd locus or loci are diploid females, hemizygotes are haploid males, and homozygotes are typically sterile diploid males. These diploid males underlie the diploid male vortex (DMV), the phenomenon of inbreeding reducing csd allelic diversity and causing increasingly higher production of sterile diploid males until the population dies out. The DMV has been cited as an extinction risk for many species across the order and a danger to both human‐controlled and natural hymenopteran populations important in biological control, pollination, and endangered species conservation. However, it has been unclear how frequently it occurs. We review the known mechanisms for DMV avoidance. Many of these mechanisms are linked to lifestyle, and so we structure our investigation around eusocial lifestyle and non‐eusocial (solitary or gregarious) species. We also review documented DMV incidence to make an inference about its prevalence. There are many means to avoid inbreeding or diploid male production, including eusocial‐exclusive polygyny, polyandry, and diploid queen execution. For both eusocial and non‐eusocial species these include biological mechanisms such as multi‐locus CSD or non‐CSD sex determination, diploid male inviability or brood removal, partial diploid male fecundity, and mating avoidance of kin or diploid males; or population genetic mechanisms such as gene flow and dispersal, balancing selection of csd alleles (with some being more prominent in eusocial vs. non‐eusocial species). Documented cases of DMV are uncommon, and incidence is often tied to exacerbatory conditions such as habitat fragmentation and host declines. With this review we suggest that due to numerous avoidance mechanisms, DMV risk may not be as high as previously believed, and requires specific circumstances. In doing so we aim to better inform hymenopteran breeding and conservation efforts.

Meta-analytic evidence that animals rarely avoid inbreeding.

Animals are usually expected to avoid mating with relatives (kin avoidance) as incestuous mating can lead to the expression of inbreeding depression. Yet, theoretical models predict that unbiased mating with regards to kinship should be common, and that under some conditions, the inclusive fitness benefits associated with inbreeding can even lead to a preference for mating with kin. This mismatch between empirical and theoretical expectations generates uncertainty as to the prevalence of inbreeding avoidance in animals. Here, we synthesized 677 effect sizes from 139 experimental studies of mate choice for kin versus non-kin in diploid animals, representing 40 years of research, using a meta-analytical approach. Our meta-analysis revealed little support for the widely held view that animals avoid mating with kin, despite clear evidence of publication bias. Instead, unbiased mating with regards to kinship appears widespread across animals and experimental conditions. The significance of a variety of moderators was explored using meta-regressions, revealing that the degree of relatedness and prior experience with kin explained some variation in the effect sizes. Yet, we found no difference in kin avoidance between males and females, choice and no-choice experiments, mated and virgin animals or between humans and animals. Our findings highlight the need to rethink the widely held view that inbreeding avoidance is a given in experimental studies.

Kin recognition: Neurogenomic response to mate choice and sib mating avoidance in a parasitic wasp

Sib mating increases homozygosity, which therefore increases the risk of inbreeding depression. Selective pressures have favoured the evolution of kin recognition and avoidance of sib mating in numerous species, including the parasitoid wasp Venturia canescens. We studied the female neurogenomic response associated with sib mating avoidance after females were exposed to courtship displays by i) unrelated males or ii) related males or iii) no courtship (controls). First, by comparing the transcriptional responses of females exposed to courtship displays to those exposed to controls, we saw a rapid and extensive transcriptional shift consistent with social environment. Second, by comparing the transcriptional responses of females exposed to courtship by related to those exposed to unrelated males, we characterized distinct and repeatable transcriptomic patterns that correlated with the relatedness of the courting male. Network analysis revealed 3 modules of specific 'sib-responsive' genes that were distinct from other 'courtship-responsive' modules. Therefore, specific neurogenomic states with characteristic brain transcriptomes associated with different behavioural responses affect sib mating avoidance behaviour.

Cost, risk, and avoidance of inbreeding in a cooperatively breeding bird

Inbreeding is often avoided in natural populations by passive processes such as sex-biased dispersal. But, in many social animals, opposite-sexed adult relatives are spatially clustered, generating a risk of incest and hence selection for active inbreeding avoidance. Here we show that, in long-tailed tits (Aegithalos caudatus), a cooperative breeder that risks inbreeding by living alongside opposite-sex relatives, inbreeding carries fitness costs and is avoided by active kin discrimination during mate choice. First, we identified a positive association between heterozygosity and fitness, indicating that inbreeding is costly. We then compared relatedness within breeding pairs to that expected under multiple mate-choice models, finding that pair relatedness is consistent with avoidance of first-order kin as partners. Finally, we show that the similarity of vocal cues offers a plausible mechanism for discrimination against first-order kin during mate choice. Long-tailed tits are known to discriminate between the calls of close kin and nonkin, and they favor first-order kin in cooperative contexts, so we conclude that long-tailed tits use the same kin discrimination rule to avoid inbreeding as they do to direct help toward kin.

Drone aggregation behavior in the social wasp Vespula germanica (Hymenoptera: Vespidae): Effect of kinship and density

Inbreeding can have negative consequences on population viability because of the reduced fitness of the progeny. In general, most species have developed mechanisms to minimize inbreeding such as dispersal and kin avoidance behavior. In the eusocial Hymenoptera, related individuals typically share a common nest and have relatively short mating periods, this could lead to inbreeding, and because of their single–locus complementary sex determination system, it may generate diploid males that could result in infertile triploid progeny representing a cost for the colony. Vespula germanica, is an eusocial wasp that has invaded many parts of the world, despite likely facing a reduced genetic pool during the arrival phases. We ask whether male wasp display specific aggregation behavior that favors genetic diversity, key to reduce inbreeding. Through a set of laboratory experiments, we investigated the effects of drone nestmateship and density on the aggregation behavior of V. germanica drones. We show that drones avoid aggregating with their nestmates at all densities while non-nestmates are avoided only at high densities. This suggests that lek genetic diversity and density could be regulated through drone behavior and in the long run minimize inbreeding favoring invasion success.

Presence of same-sex kin promotes explorative behavior in subadult cichlid fish

AbstractWhile the importance of kin discrimination, that is, kin recognition and subsequent differential treatment of kin and nonkin, is well established for kin-directed cooperation or altruism, the role of kin discrimination in the context of kin competition and kin avoidance is largely unexplored. Theory predicts that individuals avoiding competition with kin should be favored by natural selection due to indirect fitness benefits. Using an experimental approach, we investigated whether the presence of same-sex kin affects avoidance and explorative behavior in subadult Pelvicachromis taeniatus, a West African cichlid fish with strong intrasexual competition in both sexes. Pelvicachromis taeniatus is capable of recognizing kin using phenotype matching and shows kin discrimination in diverse contexts. When exposed to a same-sex conspecific, both males and females tended to interact less with the related opponent. Moreover, individuals explored a novel environment faster after exposure to kin than to nonkin. This effect was more pronounced in females. Individuals avoiding the proximity of same-sex relatives may reduce kin competition over resources such as mating partners or food.

No evidence for prezygotic postcopulatory avoidance of kin despite high inbreeding depression.

Offspring resulting from mating among close relatives can suffer from impaired fitness through the expression of recessive alleles with deleterious effects. Postcopulatory sperm selection (a prezygotic mechanism of cryptic female choice) has been suggested to be an effective way to avoid inbreeding. To investigate whether postcopulatory female choice allows the avoidance of fertilization by close kin, we performed artificial inseminations in a promiscuous bird, the houbara bustard (Chlamydotis undulata undulata). Females were inseminated with a mix of sperm from triads of males, each constituted of a male genetically unrelated to the female, a first cousin and a half-sibling. When counting the number of eggs sired by unrelated males, cousins or half-siblings, we found a significant deviation from the expected random distribution, with more eggs sired by unrelated males. However, offspring sired by cousins, and especially by half-siblings suffered from high prehatching mortality, suggesting that the observed paternity skew towards unrelated males might reflect differential offspring mortality rather than sperm selection. In agreement with this hypothesis, within-triad siring success was similar for the three parental relatedness categories, but the relationship between siring and hatching success differed across categories. In clutches with high hatching success, unrelated males had the highest success while in clutches with high failure rate, half-siblings had the highest success. Offspring sired by half-siblings also suffered from reduced growth rate during the first three months and higher posthatching mortality. Hence, despite substantial fitness costs associated with fertilization by close relatives, females do not seem to select sperm of unrelated males.

Age and Pubertal Status-Related Changes in Reports of Perception of Personal Odors.

As previously suggested, preferences for kin body odor might undergo an adaptive change over the course of puberty in order to avoid potential inbreeding, resulting in aversion to body odor of the opposite-gender kin as individuals mature sexually. However, studies based on mutual body odor aversion are rather inconclusive. We therefore investigated whether children's reports of individuals smelling good or bad differed as a function of age and pubertal status. We asked 219 children (94 male) aged 10 to 15 years to assess their pubertal development using a standardized measure and to name individuals they thought smelled good or bad. Results of the present study show that the older the girls were, the more likely they were to name males than females among nice-smelling people. Further, in both girls and boys alike, children with higher puberty scores were more likely to name children than adults. Neither in girls nor in boys did we observe any concurrent effect of age or pubertal status on children's reports of persons thought to smell bad. Irrespective of whether these changes are driven by age itself or age-related phenomena, these results suggest a shift toward a more general positive attitude to peers rather than active kin avoidance.

The scent of a hatchling: intra-species variation in the use of chemosensory cues by neonate freshwater turtles

Chemosensory cues transmit information about the sender's species, sex, reproductive status, health, and genetic relatedness, moderating social behaviour. Adaptations for chemosensory communication and social interactions are well studied in some vertebrate taxa but have been historically discounted in others. For example, chemosensory communication in Testudines was only recently documented, and these studies are largely limited to adults. In the present study, we test the hypothesis that hatchling freshwater turtles can identify conspecific hatchlings and close kin through chemosensory cues and we also investigate potential variation in the use of chemosensory cues among species with different habitat preferences. Hatchling of semi-aquatic species (Emydoidea blandingii and Graptemys geographica) showed no significant preference for conspecific-scented water over unscented water. However, hatchlings of a strictly aquatic species (Apalone spinifera) preferred water scented by conspecific hatchlings to unscented water, and preferred water scented by distantly-related conspecifics to water scented by close kin. Hatchlings of aquatic species may rely more on water-borne chemosensory cues than hatchlings of semi-aquatic species. This is the first evidence of kin recognition in Testudines, and provides an intriguing example of the avoidance of close kin. Increasing the chemical pollution of wetland habitats may impact the ‘chemoscape’ of turtles and other aquatic species, and this potential threat merits further investigation.

The role of relatedness in mate choice by an arboreal marsupial in the presence of fine-scale genetic structure

Where dispersal distances are restricted or generations overlap, kin may remain spatially clustered, leading to positive spatial genetic structure and the potential for inbreeding. In such circumstances, post-dispersal behavioral mechanisms may be required if individuals are to avoid mating with kin. Here, we conducted an empirical investigation of mate choice in the presence of fine-scale genetic structure. We assessed the potential for mating among relatives using genetic spatial autocorrelation analysis among adult mountain brushtail possums (Trichosurus cunninghami). There was significant positive spatial genetic structure among opposite-sexed adults (on a scale of 200 m), suggesting that kin remained spatially clustered after dispersal. Despite this, no genetic evidence of inbreeding was found. We assessed whether females may potentially avoid inbreeding: (1) by seeking distant mates and/or (2) by the active avoidance of kin in mate choice. Individuals did not choose distant mates, as 97 % of pairs that mated were separated by <200 m. We identified two distinct patterns of mate choice within the one population. Approximately half of the females sampled were socially monogamous (pair-bonded), and there was no evidence that these individuals chose mates on the basis of genetic dissimilarity. By contrast, the remaining (non-pair-bonded) females were more likely to select genetically dissimilar mates. This dual mate choice pattern demonstrates that the role of genetic relatedness in mate choice can be dependent on social context and dispersal patterns.

Inbreeding avoidance mechanisms: dispersal dynamics in cooperatively breeding southern pied babblers

1. Breeding with kin can reduce individual fitness through the deleterious effects of inbreeding depression. Inbreeding avoidance mechanisms are expected to have developed in most species, and especially in cooperatively breeding species where individuals may delay dispersal until long after sexual maturity. Such potential mechanisms include sex-biased dispersal and avoidance of kin known through associative learning. 2. The investigation of inbreeding avoidance through dispersal dynamics can be enhanced by combining fine-scale population genetic structure data with detailed behavioural observations of wild populations. 3. We investigate possible inbreeding avoidance in a wild population of cooperatively breeding southern pied babblers (Turdoides bicolor). A combination of genetic, geographic and observational data is used to examine fine-scale genetic structure, dispersal (including sex-biased dispersal) and inheritance of dominance in cooperatively breeding groups. 4. Unusually, sex-bias in dispersal distance does not occur. Rather, individuals appear to avoid inbreeding through two routes. First, through dispersal itself: although both males and females disperse locally, they move outside the range within which genetically similar individuals are usually found, going twice as far from natal groups as from non-natal groups. Second, through avoidance of familiar group members as mates: individuals inherit a dominant position in the natal group only when an unrelated breeding partner is present. 5. This study uses spatial genetic analyses to investigate inbreeding avoidance mechanisms in a cooperative breeder and shows that individuals of both sexes can avoid inbreeding through a dispersal distance mechanism. While it appears that dispersal allows most individuals to move beyond the range of closely related kin, matings may still occur between distant kin. Nevertheless, any costs of breeding with a distant relative may be outweighed by the benefits of local dispersal and the immense fitness gains available from attaining a breeding position.

No evidence for inbreeding avoidance through active mate choice in red-billed gulls

Except for cooperative breeders, most studies on wild birds have failed to find evidence for inbreeding avoidance via kin discriminative mate choice. This, together with evidence for kin avoidance through dispersal, has led to the general view that dispersal is often a sufficient inbreeding avoidance mechanism and active discrimination through mate choice is unnecessary. Yet, the study of inbreeding avoidance in the wild is difficult and long-term studies of pedigreed wild populations can provide important insights. We studied the occurrence of inbreeding avoidance in a highly philopatric red-billed gull (Larus novaehollandiae scopulinus) population subject to an individual-based field study since 1958 in Kaikoura, New Zealand. Despite a wealth of breeding and pedigree data, we did not observe a single inbred pair. This observation was a small but significant deviation from the expectation under the null hypothesis of random mating when we looked at annual breeding attempts, suggesting inbreeding avoidance. However, the difference disappeared when we examined pair bonds rather than annual breeding attempts. Our results are consistent with the expectation that close inbreeding occurs rarely in large random-mating populations. They also demonstrate how mating systems, in this case long-term monogamous pair bonds with sex differences both in the age of first breeding and breeding dispersal at natal subcolonies, can reduce the likelihood of inbreeding.

A field test of the effects of familiarity and relatedness on social associations and reproduction in prairie voles

Inbreeding depression is a well-documented phenomenon. In animals, one means of avoiding the costs of inbreeding is through the recognition and avoidance of kin as mates. Prairie voles (Microtus ochrogaster) are short-lived, socially monogamous rodents that demonstrate inbreeding depression in the laboratory. Field data indicate that pair formation in nature is opportunistic but pairing among close relatives seems uncommon. We examined the role of relatedness and familiarity on prairie vole social associations and reproduction by placing adult voles into 0.1-ha enclosures with familiar siblings, unfamiliar siblings, and unrelated, unfamiliar conspecifics. Live-trapping data indicated that indices of social pair bonding were random with respect to relatedness and familiarity. Among females whose litters were sired by a single male, litters were significantly more likely to be sired by unfamiliar than familiar males, but the number of litters sired by males that were unrelated to their partner was not different from the number of litters sired by males that were related to their partner. Additionally, females that produced offspring with familiar siblings were significantly more likely to have litters with multiple paternity than females not producing offspring with familiar siblings. However, multiple paternity was not influenced by relatedness of sires. Finally, older individuals were more likely to produce offspring with each other than with younger individuals. Our findings suggest that prior association is a more important mechanism of inbreeding avoidance than phenotype matching for prairie voles mating under ecologically relevant conditions.

Kin selection in den sharing develops under limited availability of tree hollows for a forest marsupial

Animal social behaviour is not static with regard to environmental change. Flexibility in cooperative resource use may be an important response to resource decline, mediating the impacts of resource availability on fitness and demography. In forest ecosystems, hollow trees are key den resources for many species, but are declining worldwide owing to forestry. Altered patterns of den sharing may mediate the effects of the decline of this resource. We studied den-sharing interactions among hollow-dependent Australian mountain brushtail possums to investigate how spatial variation in hollow tree availability affects resource sharing and kin selection. Under reduced den availability, individuals used fewer dens and shared them less often. This suggests increased territoriality in the presence of resource competition. Further, there was a switch from kin avoidance to kin preference with decreasing hollow tree availability. This was driven primarily by a change in den sharing among siblings. The inclusive fitness benefits of den sharing with kin are likely to increase under resource-limiting conditions, but are potentially outweighed by the benefits of associating with non-relatives (avoidance of inbreeding or pathogen transmission) where dens are abundant. We discuss how predictions from social evolutionary theory can contribute to understanding animal responses to landscape change.

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.

Natal dispersal and social organization of the swamp antechinus (Antechinus minimus) in a high-density island population

Radiotelemetry, mark–recapture trapping, and microsatellite analysis of genetic variation among three subpopulations were used to investigate the natal dispersal patterns, genetic structure, and social organization within a high-density island population of an insectivorous marsupial, the swamp antechinus ( Antechinus minimus (É. Geoffroy Saint-Hilaire, 1803)). Both demographic and genetic data indicated a high degree of philopatry for both sexes. Associated with high philopatry is low gene flow, often leading to high population genetic structuring. However, there was only weak evidence to support this; allele frequencies and genotype composition of one population tended to be different from the other two. Interestingly, timing of breeding of this subpopulation was delayed compared with the other two subpopulations. The philopatry of both sexes and the apparent lack of kin avoidance behaviour could lead to inbreeding. However, no apparent inbreeding effects were observed and offspring survival was high compared with mainland populations. The fact that male home-range size increased during the breeding season, overlapping with several females, and single females were found nesting with different males at the time of mating (and vice versa) indicates a promiscuous mating system. Potentially, this may reduce inbreeding to some extent. Alternatively, inbreeding may not be purposefully avoided, potentially leading to purging of detrimental alleles, thereby reducing their damaging effects on inbreeding.

Influence of major histocompatibility complex genotype on mating success in a free-ranging reptile population.

Major histocompatibility complex (MHC) genes are highly polymorphic components of the vertebrate immune system, which play a key role in pathogen resistance. MHC genes may also function as odour-related cues for mate choice, thus ensuring optimal MHC diversity in offspring. MHC-associated mate choice has been demonstrated in some fish, bird and mammal species but it is not known whether this is a general vertebrate phenomenon. We investigated whether MHC-associated mate choice occurs in a wild population of tuatara (Sphenodon punctatus), a territorial and sexually dimorphic reptile. We found weak evidence for MHC-disassortative mating, based on amino acid genotypic distance between pairs, when mated pairs were directly compared with potential pairs in close spatial proximity. No significant association was found between male mating success, number of MHC sequences, microsatellite heterozygosity or MHC lineage. The major determinant of mating success in tuatara was male body size, which was not related to MHC lineage or microsatellite heterozygosity. Our results suggest that male competitive ability is the primary driver of mating success in tuatara. However, MHC-associated preferences also appear to play a role, possibly as a kin avoidance mechanism during territory formation.

Correlates of the occurrence of inbreeding in a wild bird population

Inbreeding occurs when close relatives mate. In most populations, inbreeding is uncommon, with the result that we know little about the characteristics of those individuals that inbreed. However, such information may be invaluable for understanding the causes of inbreeding and inbreeding avoidance and the consequences of inbreeding. We investigated the characteristics of closely inbreeding individuals using 43 years of data from a wild great tit (Parus major) population in order to 1) characterize close inbreeding in terms of the family relationships involved; 2) compare inbreeding with noninbreeding individuals; and 3) determine whether close inbreeding was subsequently avoided by those that experience it. We found an uneven distribution of different types of close inbreeding, with sib mating most frequent and father–daughter matings least frequent. We did not find any evidence for clear predictors of inbreeding. By comparing the reproductive success of individuals that both inbred and outbred in their lifetimes, we demonstrate that inbreeding depression is solely attributable to the mixing of relatives’ genes and is thus independent of any tendency for low-quality parental genotypes or phenotypes to inbreed. Surprisingly, mating with close kin reduced the probability of divorce in the following reproductive season, while brood or fledging failure did not predict for remating. Overall, our results suggest that inbreeding is not a response to lowered prospects and that despite the substantial fitness cost of inbreeding, its avoidance in this population may be based on general mechanisms such as dispersal rather than specific kin avoidance. Key words: divorce, great tit, inbreeding, inbreeding depression, parental quality, Parus major, pedigree, remating, Wytham. [Behav Ecol]

Sex, age, and family differences in the chemical composition of owl monkey (Aotus nancymaae) subcaudal scent secretions

Numerous behavioral studies have shown that animals use olfactory cues as inbreeding avoidance or kin avoidance mechanisms, implying that scent is unique to families. However, few studies have analyzed the chemical profile of a scent and ascertained the messages that are conveyed in scent secretions. Owl monkeys (Aotus nancymaae) are socially monogamous primates that utilize scent when interacting with foreign conspecifics. This suggests there is a difference in the chemical composition of scent marks. We chemically analyzed sub-caudal gland samples from three families of captive owl monkeys (Aotus nancymaae). Samples were analyzed by capillary GC-MS and relative retention time and fragment pattern was compared with known standards. Gland samples were high in large plant-based shikikate metabolites and fatty ketones; alcohols, acids, and acetates were virtually absent. Gender, age, and family could be reliably classified using discriminant analysis (92.9, 100, and 100%, respectively). Female scent profiles were greater in concentration of aromatic plant metabolites, possibly the result of a different diet or physiological differences in female metabolism as compared to male. Offspring of adult age still living in their natal group showed a less complex chemical profile than their parents. Finally, each family had its own unique and complex chemical profile. The presence of family scent may play a role in mediating social interactions.