Kin discrimination and female mate choice in the naked mole-rat Heterocephalus glaber

Naked mole-rats are fossorial, eusocial rodents that naturally exhibit high levels of inbreeding. Persistent inbreeding in animals often results in a substantial decline in fitness and, thus, dispersal and avoidance of kin as mates are two common inbreeding avoidance mechanisms. In the naked mole-rat evidence for the former has recently been found. Here we address the latter mechanism by investigating kin recognition and female mate choice using a series of choice tests in which the odour, social and mate preferences of females were determined. Discrimination by females appears to be dependent on their reproductive status. Reproductively active females prefer to associate with unfamiliar males, whereas reproductively inactive females do not discriminate. Females do not discriminate between kin and non-kin suggesting that the criterion for recognition is familiarity, not detection of genetic similarity per se. In the wild, naked mole-rats occupy discrete burrow systems and dispersal and mixing with non-kin is thought to be comparatively rare. Thus, recognition by familiarity may function as a highly efficient kin recognition mechanism in the naked mole-rat. A preference by reproductively active females for unfamiliar males is interpreted as inbreeding avoidance. These findings suggest that, despite an evolutionary history of close inbreeding, naked mole-rats may not be exempt from the effects of inbreeding depression and will attempt to outbreed should the opportunity arise.     

Evidence for Inbreeding Depression and Pre-Copulatory,but Not Post Copulatory Inbreeding Avoidance in the Cabbage Beetle Colaphellus bowringi

Inbreeding is known to have adverse effects on fitness-related traits in a range of insect species. A series of theoretical and experimental studies have suggested that polyandrous insects could avoid the cost of inbreeding via pre-copulatory mate choice and/or post-copulatory mechanisms. We looked for evidence of pre-copulatory inbreeding avoidance using female mate preference trials, in which females were given the choice of mating with either of two males, a sibling and a non-sibling. We also tested for evidence of post-copulatory inbreeding avoidance by conducting double mating experiments, in which four sibling females were mated with two males sequentially, either two siblings, two non-siblings or a sibling and a non-sibling in either order. We identified substantial inbreeding depression: offspring of females mated to full siblings had lower hatching success, slower development time from egg to adult, lower survival of larval and pupal stages, and lower adult body mass than the offspring of females mated to non-sibling males. We also found evidence of pre-copulatory inbreeding avoidance, as females preferred to mate with non-sibling males. However, we did not find any evidence of post-copulatory inbreeding avoidance: egg hatching success of females mating to both sibling and non-sibling males were consistent with sperm being used without bias in relation to mate relatedness. Our results suggest that this cabbage beetle has evolved a pre-copulatory mechanism to avoid matings between close relative, but that polyandry is apparently not an inbreeding avoidance mechanism in C. bowringi.     

How Do Females’ Genetic Characteristics Influence Male Mate Preference in the Terrestrial Isopod Armadillidium vulgare?

Genetic diversity is a key factor that can influence mate choice in many species. We experimentally determined the influence of this factor on mate preference in the crustacean terrestrial isopod Armadillidium vulgare. This biological model is gregarious which could increase the risk of inbreeding by mating with closely related partners. Mechanisms of inbreeding avoidance during mate choice can thus be expected. Moreover, previous studies predict that males would be the choosy sex. We performed Y‐choice tests giving males the choice between two females presenting different levels of heterozygosity and genetic similarity to the male. Our results show potential inbreeding avoidance according to the genetic characteristics of females presented to males. The higher the variation in genetic similarity to the male between females is, the higher the preference of the male towards the most dissimilar female is. Hence, male preferences may only be detectable when the difference between females’ genetic characteristics is large enough. If heterozygosity is associated with fitness in A. vulgare (as in many organisms), the patterns of mate preference we observe may be adaptive.     

Natal Dispersal and Philopatry in the Carnivorous Marsupial Phascogale tapoatafa (Dasyuridae)

The proximate and ultimate causes of dispersal in semelparous carnivorous marsupials (Phascogalinae) have previously been hypothesized to be maternal aggression and inbreeding avoidance, respectively. This study tests these hypotheses by exposing 26 litters of Phascogale tapoatafa to a diverse range of social and environmental conditions that potentially affect dispersal (e.g. supplemental feeding, post-weaning desertion by the mother, orphaning, and release of subadults into unoccupied habitat). The mean dispersal age was 162 ± 5.6 d, which is about 3 wk after weaning is complete. Juvenile dispersal was strongly male biased under all conditions, suggesting that extrinsic proximate causes do not adequately account for male emigration. Home range establishment by males was contingent on the presence of females. Half of the monitored daughters were philopatric, and others typically settled adjacent to the natal site, thus possibly enhancing their reproductive potential by occupying an area of known resource quality. Because philopatry increases the risk of incest, females may be selected to preferentially mate with unrelated males (immigrants), when they are available, to avoid inbreeding. If so, the presence of immigrant males would reduce the probability of locally born, related males reproducing at their natal site. Thus inbreeding avoidance by females may create local mate competition among males and select for male dispersal. Emigration also ensured that males avoided inbreeding, but, if they dispersed into unoccupied habitat, male P. tapoatafa often returned to the natal area. This 'boomerang strategy' of returning to mate with related females suggests that, in the absence of conspecifics along the dispersal path of a male, mate competition will be weak at the natal site and female mate choice will not preclude related males. Thus while inbreeding avoidance by either or both sexes is perhaps the most parsimonious explanation of male-biased emigration, dispersal patterns were apparently strongly influenced by additional factors, so that the ultimate causation of the dispersal regime may be more complex.     

No Inbreeding Avoidance by Female Burying Beetles Regardless of Whether They Encounter Males Simultaneously or Sequentially

Inbreeding avoidance reduces the probability that an individual will mate with a related partner, thereby lowering the risk that it produces inbred offspring suffering from inbreeding depression. Inbreeding avoidance can occur through several mechanisms, including active mate choice, polyandry and sex‐biased dispersal. Here, we focus on the role of active mate choice as a mechanism for inbreeding avoidance. Recent evidence suggests that the experimental design used in mate choice experiments (i.e. simultaneous versus sequential choice) can have a strong impact on the strength of the reported mating preferences. In this study, we examine whether similar effects of experimental design also apply in the context of inbreeding avoidance. To this end, we designed two experiments on the burying beetle Nicrophorus vespilloides that matched two different contexts under which females encounter potential mates in the wild; that is, when females encounter males simultaneously and sequentially. We found that females were as likely to mate with related and unrelated males regardless of whether they encountered male partners simultaneously or sequentially. Thus, our study provides no evidence for inbreeding avoidance in this species, and suggests that the number of mates present did not influence the degree of inbreeding avoidance. We discuss potential explanations for the lack of inbreeding avoidance through mate choice, including lack of mechanisms for recognizing close relatives, low costs and/or low risks of inbreeding and the presence of other inbreeding avoidance mechanisms, such as sex‐biased dispersal and polyandry coupled with post‐copulatory mate choice.     

Brother-sister and parent-child marriage outside royal families in ancient egypt and iran: A challenge to the sociobiological view of incest avoidance?

Copious and unequivocal evidence of legally condoned and socially favored brother-sister and parent-child marriage among common people from Roman Egypt (first to third centuries, A.D.) and Zoroastrian Iran (fifth century, B.C. to 11th century, A.D.) can be taken to pose a challenge to the sociobiological case for universal evolved incest avoidance within the nuclear family, triggered by early childhood proximity (the Westermarck effect). Official census documents from Roman Egypt show a high incidence of full sibling unions with relatively small age gaps between the spouses and no indication of reduced marital fertility, sexual aversion, or increased infant and child mortality. Zoroastrian religious tracts actively encourage nuclear family incest and extol its meritorious nature and supernatural benefits. A schematic assessment of the likely extent of inbreeding depression in such families under conditions of very high mortality through other causes makes reproduction at replacement level seem difficult to accomplish. But given the lack of information on the frequency of deleterious recessive genes in these populations, this reconstruction is fraught with uncertainty; pertinent ancient evidence is suggestive of some incidence of inbreeding depression but remains inconclusive. Aversion and revulsion between incestuous spouses proves a similarly elusive issue. Although these cases from antiquity do not clearly contradict the view of incest avoidance as an evolved mechanism that engenders sexual indifference and normally translates into corresponding cultural norms, they demonstrate the need for a more comprehensive consideration of the available historical record in the testing of evolutionary rules.     

Female ground tits prefer relatives as extra‐pair partners: driven by kin‐selection?

Socially monogamous female birds routinely mate with males outside the pair bond. Three alternative hypotheses consider genetic benefits as the major driver behind the female strategy. The inbreeding avoidance hypothesis predicts that females paired with closely related males should seek copulations with distantly related extra-pair partners to avoid fitness loss from inbreeding depression; the outbreeding avoidance hypothesis predicts the opposite; the kin-selection hypothesis suggests that regardless of social mate relatedness, females should give related males extra-pair fertilization opportunities to gain inclusive fitness if the costs from inbreeding are minor. We test these hypotheses with a facultative cooperative breeder, the ground tit (Parus humilis). Social pairs of ground tits formed randomly with respect to genetic relatedness. In both bi-parental and cooperative groups, a female's engaging in extra-pair mating was independent of relatedness to her social mate; however, females preferred extra-pair sires to which they were more related than to their social mates. Moreover, females had higher relatedness with either their extra-group extra-pair sires in both bi-parental and cooperative groups, or within-group helper sires in cooperative groups, than expected by chance. When more than one potential extra-pair partner was available around a female's nest, she tended to select a relative. There was no indication of fitness reduction from extra-pair mating, which occurred at an intermediate level of inbreeding. These data support the kin-selection hypothesis, although there might be alternative nongenetic reasons associated with the extra-pair mating preference. Our finding offers a new explanation for why female birds pursue extra-pair mating. It also may broaden our understanding of the role of kin-selection in the evolution of cooperative society.     

Natal dispersal and parental escorting predict relatedness between mates in a passerine bird

Although relatedness between mates is of considerable evolutionary and ecological significance, the way in which the level of relatedness is determined by different behavioural processes remains largely unknown. We investigated the role of behaviour in predicting mate relatedness in great tits using genotypic markers and detailed observations. We studied how mate relatedness is influenced by natal dispersal, inbreeding/outbreeding avoidance after natal dispersal and a behaviour not previously considered that influences membership to social aggregations, namely family escorting behaviour by parents. Among locally born individuals, the level of mate relatedness decreased with natal dispersal distance for females, but not for males. In contrast, mate relatedness was negatively related to the extent of family movements for males, but not for females. However, family movements did not predict dispersal distance for either sex. Local recruits were more related to their mates than immigrants, but this was only significant for females. No evidence was found for inbreeding/outbreeding avoidance after dispersal. Our results suggest that, in highly mobile species, mating options are spatially and/or socially limited, and that parents influence mating options of their offspring before dispersal.     

Premating Avoidance of Inbreeding Absent in Female Guppies (Poecilia reticulata)

The recognition and avoidance of kin during mating can be an important means of reducing the potential for inbreeding depression in offspring. We report here that premating mechanisms to avoid inbreeding, either innate or learnt through juvenile experience, are at best weak in female guppies (Poecilia reticulata). Guppies are small, ovoviviparous, neo‐tropical freshwater fish, with a polygamous mating system where males actively court females and females are selective of their mates. In a series of mate‐choice experiments, naïve, virgin females of the Quare River population in Trinidad were given a choice between a brother and a non‐sib male from the same population. Initially, females were only provided olfactory cues upon which to base their choice and then subsequently both olfactory and visual cues. Despite the females displaying mate choice, we found no evidence of them discriminating between the male types in either experiment. There was thus no indication of inbreeding avoidance, suggesting that experiences after maturation or with mature males (e.g. rare male preference), dispersal and/or post‐mating mechanisms may be evolutionarily more important avoidance mechanisms.     

Incestuous Sisters: Mate Preference for Brothers over Unrelated Males in Drosophila melanogaster

The literature is full of examples of inbreeding avoidance, while recent mathematical models predict that inbreeding tolerance or even inbreeding preference should be expected under several realistic conditions like e.g. polygyny. We investigated male and female mate preferences with respect to relatedness in the fruit fly D. melanogaster. Experiments offered the choice between a first order relative (full-sibling or parent) and an unrelated individual with the same age and mating history. We found that females significantly preferred mating with their brothers, thus supporting inbreeding preference. Moreover, females did not avoid mating with their fathers, and males did not avoid mating with their sisters, thus supporting inbreeding tolerance. Our experiments therefore add empirical evidence for inbreeding preference, which strengthens the prediction that inbreeding tolerance and preference can evolve under specific circumstances through the positive effects on inclusive fitness.     

Inbreeding avoidance in rhesus macaques: Whose choice?

Whether nonhuman primates avoid copulating with close kin living in their social group is controversial. If sexual aversion to relatives occurs, it should be stronger in females than in males because of females' greater investment in each offspring and hence greater costs resulting from less viable offspring. Data presented here show that adult male rhesus macaques breeding in their natal groups at Cayo Santiago experienced high copulatory success, but copulated less with females of their own matrilineages than with females of other matrilineages. Adult females were never observed to copulate with males of their own matrilineage during their fertile periods. Although natal males sometimes courted their relatives, examination of two measures of female mate choice showed that females chose unrelated natal males over male kin. Female aversion to male kin was specific to the sexual context; during the birth season, females did not discriminate against their male relatives in distributing grooming. Evolved inbreeding avoidance mechanisms probably produce different outcomes at Cayo Santiago than in wild rhesus macaque populations. Gender differences in sexual aversion to relatives may be partly responsible for differences between studies in reported frequency of copulations by related pairs. © 1993 Wiley-Liss, Inc.     

Rethinking the Taiwanese minor marriage data: evidence the mind uses multiple kinship cues to regulate inbreeding avoidance

Natural experiments such as the Israeli Kibbutzim and Taiwanese minor marriages provide unique opportunities for testing the effects of childhood association on adult sexual attraction. Within these populations, early childhood association leads to the development of a sexual aversion, an effect first proposed by Edward Westermarck. However, recent analysis of Taiwanese minor marriages indicates that only the age at first association (an inverse index of childhood association) of the younger partner predicts marital fertility rates; the age at first association of the older partner does not. Although considered a puzzle, a recent model of human inbreeding avoidance can explain this pattern. This model suggests that the mind uses at least two kinship cues to regulate the development of sibling sexual aversions: (i) childhood coresidence duration, a default cue used mainly by younger siblings in detecting probable older siblings, and (ii) exposure to one's mother caring for a newborn, a cue only available to older siblings and reliable regardless of coresidence duration and, hence, age at first association. Thus, one reason that the age at first association of only the younger partner in minor marriages predicts fertility is that coresidence duration serves as a cue to siblingship mainly for younger partners; older partners use a different kinship cue not influenced by durations of association. When compared to data from psychological investigations of the effects of coresidence duration on opposition to sibling incest, the minor marriage data reveal an identical pattern providing converging lines of evidence that multiple kinship cues mediate sibling detection and inbreeding avoidance in humans.     

Direct Familiarity Does Not Alter Mating Preference for Sisters in Male Pelvicachromis taeniatus (Cichlidae)

In social species, individuals who grew up together are usually relatives. Therefore, direct familiarity is normally a reliable kin recognition mechanism that is used in many species to discriminate kin from non‐kin. It has been shown in animals and in humans that familiar individuals are rejected as mating partners in order to circumvent potential costs of inbreeding. Here, we tested whether direct familiarity also leads to inbreeding avoidance behaviour in male Pelvicachromis taeniatus, a small socially monogamous cichlid with biparental brood care. In mate choice experiments, reproductively active males were given the choice between familiar sisters and unfamiliar, unrelated females. In a previous study, both sexes of P. taeniatus had preferred unfamiliar full‐sibs over unfamiliar unrelated individuals as mating partners. Here, we show that direct familiarity does not alter the male preference for closely related females. This result is in accordance with theoretical predictions, that inbreeding can be advantageous under certain conditions, and confirms previous findings, that active inbreeding is an adaptive strategy in P. taeniatus.     

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

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

Population genetic models of male and mutual mate choice

Examples of male mate choice are becoming increasingly common, even in polygynous species. We create a series of population genetic models to examine the evolutionary equilibria and dynamics resulting from male mate choice during polygyny, alone and in the context of mutual mate choice by both sexes. We find that unless males with a preference are able to increase their overall courtship output, male preference will be lost. This loss can be counteracted if males choose females not based on arbitrary traits, but based on a trait that indicates high fertility or viability. We also conclude that if male and female preferences and traits are all controlled by different loci, the male and female mate choice systems are decoupled; the presence of a male preference then has no influence on the equilibria or dynamics of female mate choice. If male and female traits are coupled by pleiotropy, it becomes possible for a male preference to be maintained, regardless of whether preferences between the sexes are pleiotropic or controlled by separate loci.     

Males Benefit from Mating with Outbred Females in Drosophila littoralis: Male Choice for Female Genetic Quality?

The evolution and expression of mate choice behaviour in either sex depends on the sex‐specific combination of mating costs, benefits of choice and constraints on choice. If the benefits of choice are larger for one sex, we would expect that sex to be choosier, assuming that the mating costs and constraints on choice are equal between sexes. Because deliberate inbreeding is a powerful genetic method for experimental manipulation of the quality of study organisms, we tested the effects of both male and female inbreeding on egg and offspring production in Drosophila littoralis. Female inbreeding significantly reduced offspring production (mostly due to lower egg‐to‐adult viability), whereas male inbreeding did not affect offspring production (despite a slight effect of paternal inbreeding on egg‐to‐adult viability). As inbreeding depressed female quality more than male quality, the benefits of mate choice were larger for males than for females. In mate choice experiments, inbreeding did not affect male mating success (measured as a probability to be accepted as a mate in a large group), suggesting that females did not discriminate among inbred and outbred males. In contrast, female mating success was affected by inbreeding, with outbred females having higher mating success than inbred females. This result was not explained by lower activity of inbred females. Our results show that D. littoralis males benefit from mating with outbred females of high genetic quality and suggest adaptive male mate choice for female genetic quality in this species. Thus, patterns of mating success in mate choice trials mirrored the benefits of choice: the sex that benefited more from choice (i.e. males) was more choosy.     

Inbreeding Avoidance in Male Primates: A Response to Female Mate Choice?

Inbreeding often has negative fitness consequences for primates, which have led to the evolution of inbreeding avoidance strategies in a number of species. In polygynous primates, females may suffer a higher fitness cost from inbreeding than males and are thus expected to exhibit a lower tolerance for inbreeding. Nevertheless, it is apparent that inbreeding avoidance behaviours are common in both female and male polygynous primates. In this perspectives article, I review the evidence that female mate choice can lead to male inbreeding avoidance behaviours in polygynous primates. I conclude that male inbreeding avoidance may be strongly driven by female mate choice at both proximate and ultimate levels. To better understand the extent to which this pattern applies across the primate order, studies are needed on the separate effects of participating in inbred matings and producing inbred offspring on male and female lifetime reproductive success . It would also be useful to examine how inbreeding avoidance strategies vary across primate mating systems. Finally, measuring the covariance between female choice and male inbreeding avoidance behaviour, and between male inbreeding avoidance behaviour and male fitness, would help to clarify the role of female mate choice in the evolution of male inbreeding avoidance.     

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

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

Mutual mate choice: when it pays both sexes to avoid inbreeding

Theoretical models of sexual selection predict that both males and females of many species should benefit by selecting their mating partners. However, empirical evidence testing and validating this prediction is scarce. In particular, whereas inbreeding avoidance is expected to induce sexual conflicts, in some cases both partners could benefit by acting in concert and exerting mutual mate choice for non-assortative pairings. We tested this prediction with the gregarious cockroach Blattella germanica (L.). We demonstrated that males and females base their mate choice on different criteria and that choice occurs at different steps during the mating sequence. Males assess their relatedness to females through antennal contacts before deciding to court preferentially non-siblings. Conversely, females biased their choice towards the most vigorously courting males that happened to be non-siblings. This study is the first to demonstrate mutual mate choice leading to close inbreeding avoidance. The fact that outbred pairs were more fertile than inbred pairs strongly supports the adaptive value of this mating system, which includes no "best phenotype" as the quality of two mating partners is primarily linked to their relatedness. We discuss the implications of our results in the light of inbreeding conflict models.     

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.