Kin Recognition Research Articles

Do dogs (Canis lupus familiaris) prefer family?

Kin recognition requires the ability to discriminate between one’s own genetic relatives and non-relatives. There are two mechanisms that aid in kin discrimination: phenotype matching and familiarity. Dogs may be a good model for assessing these mechanisms as dogs are a promiscuous social species with a keen sense of smell. Domestic dogs of both sexes were presented with two scents (close kin, distant-kin) and preference was assessed through three measures (latency to approach, number of visits, time spent). Experiment 1 explored the possibility of phenotype matching as subjects had no contact with sires, whose scent was presented alongside a control male's scent. Experiment 2 explored recognition of siblings raised with the subjects and then separated at seven weeks of age. Whereas female dogs in this experiment did not show a statistically significant preference, male dogs showed a preference for distant-kin when presented with sire and female sibling samples.

Chemical fingerprints encode mother–offspring similarity, colony membership, relatedness, and genetic quality in fur seals

Chemical communication underpins virtually all aspects of vertebrate social life, yet remains poorly understood because of its highly complex mechanistic basis. We therefore used chemical fingerprinting of skin swabs and genetic analysis to explore the chemical cues that may underlie mother-offspring recognition in colonially breeding Antarctic fur seals. By sampling mother-offspring pairs from two different colonies, using a variety of statistical approaches and genotyping a large panel of microsatellite loci, we show that colony membership, mother-offspring similarity, heterozygosity, and genetic relatedness are all chemically encoded. Moreover, chemical similarity between mothers and offspring reflects a combination of genetic and environmental influences, the former partly encoded by substances resembling known pheromones. Our findings reveal the diversity of information contained within chemical fingerprints and have implications for understanding mother-offspring communication, kin recognition, and mate choice.

Kin Recognition and Inbreeding Avoidance in a Butterfly

AbstractOwing to the risk of inbreeding depression, the evolution of inbreeding avoidance by means of kin recognition is expected for many biological systems. Nevertheless, an ability to distinguish among relatives and non‐relatives has been only rarely demonstrated, especially so in non‐social organisms. We here show that, in the non‐social tropical butterfly Bicyclus anynana, females discriminate against relatives by preferentially mating with non‐relatives. Inbreeding avoidance was more pronounced in inbred as compared with outbred butterflies, suggesting that it is partly condition dependent. We argue that, in our system, the evolution of inbreeding avoidance is related to carrying a high genetic load and thus to being particularly sensitive to inbreeding depression. We suggest that kin recognition might be more widespread than currently thought and that future studies may possibly benefit from considering condition dependence, especially by paying attention to and/or manipulating population history, genetic load, and the risk of inbreeding depression. We further suggest that kin recognition in B. anynana might be based on cuticular hydrocarbons used for self‐referencing.

Multiple mating predicts intensity but not mechanism of kin recognition

Understanding how animals recognize their kin has been a major challenge in biology. Most animals use one of 2 mechanisms: whereby kin are remembered from interactions early in life, such as in a nest, or phenotype whereby putative kin are compared with a template of what kin should look, smell, or sound like. Cross-species studies suggest that there is a link between which of these 2 mechanisms are used and the degree of female promiscuity (multiple mating). Phenotype matching is more likely to be used by promiscuous species because these species have lower average brood relatedness than monogamous species and familiarity is thus an unreliable cue of relatedness. However, it is unclear if this relationship holds within species, across populations that differ in their degree of promiscuity. Here, we take advantage of variation in brood relatedness across populations of guppies (Poecilia reticulata) to examine the relationship between kin recognition mechanisms and multiple mating within a single species. Contrary to the established hypothesis, we show that variation in recognition mechanism across populations is not governed by multiple mating. Instead, our data show that kin recognition, quantified as association preferences for shoalmates, is strongest when brood relatedness is high, consistent with Hamilton’s rule, but multiple mating does not otherwise influence the specific recognition mechanism used.

Female guppies can recognize kin but only avoid incest when previously mated

Kin recognition plays a key role in inbreeding avoidance for taxa from all major animal groups; however, perplexingly, a number of species, for which the risks and costs of inbreeding are high, do not discriminate against relatives in mate choice experiments. We tested a possible explanation for this paradox: most tests of inbreeding avoidance have used virgin females, but theory predicts that virgin females should first mate indiscriminately to gain reproductive assurance and, only subsequently, become choosy. To test this idea, we used the Trinidadian guppy, which suffers inbreeding depression but for which evidence for kin recognition is equivocal. We manipulated rearing environment to disentangle 2 forms of kin recognition and tested the preferences of both virgin and nonvirgin females. As predicted, virgins were indiscriminate in their mate choice. Nonvirgins, in contrast, expressed strong preferences for unfamiliar and unrelated males. Therefore, female guppies recognize kin in a mate choice context but become selective only once reproductively assured. This dynamic likely increases population fitness in newly colonized or small, at-risk populations by ensuring that virgins mate even when only unfamiliar or unrelated males are available. Our findings suggest that inbreeding avoidance may be more common than previously thought and that the use of virgin females can sometimes prevent the detection of powerful mate preferences.

Male rhesus macaques use vocalizations to distinguish female maternal, but not paternal, kin from non-kin.

Recognizing close kin and adjusting one’s behavior accordingly (i.e., favor kin in social interactions, but avoid mating with them) would be an important skill that can increase an animals’ inclusive fitness. Previous studies showed that philopatric female rhesus macaques (Macaca mulatta) bias their social behavior toward maternal and paternal kin. Benefits gained from selecting kin should, however, not only apply to the philopatric sex, for which the enduring spatial proximity facilitates kin discrimination. Given that dispersal is costly, the dispersing sex may benefit from migrating together with their kin or into groups containing kin. In male rhesus macaques, natal migrants bias their spatial proximity toward familiar male kin rather than familiar non-kin. Here, we set up playback experiments to test if males use the acoustic modality to discriminate familiar female kin from non-kin in a non-sexual context. Males responded differently to the presentation of “coo” calls of related and unrelated females, with their reaction depending on the interaction between kin-line (maternal vs paternal kin) and degree of relatedness (r = 0.5, 0.25). Specifically, males were more likely to respond to close kin compared to more distant kin or unrelated females, with this effect being significant in the maternal, but not paternal kin-line. The present study adds to our knowledge of kin recognition abilities of the dispersing sex, suggesting that male rhesus macaques are also able to identify kin using the acoustic modality. We discuss that the probability of response might be affected by the potential benefit of the social partner.

Social network analysis of mating patterns in American black bears (Ursus americanus).

Nonrandom mating can structure populations and has important implications for population-level processes. Investigating how and why mating deviates from random is important for understanding evolutionary processes as well as informing conservation and management. Prior to the implementation of parentage analyses, understanding mating patterns in solitary, elusive species like bears was virtually impossible. Here, we capitalize on a long-term genetic data set collected from black bears (Ursus americanus) (N=2422) in the Northern Lower Peninsula (NLP) of Michigan, USA. We identified mated pairs using parentage analysis and applied logistic regression (selection) models that controlled for features of the social network, to quantify the effects of individual characteristics, and spatial and population demographic factors on mating dynamics. Logistic regression models revealed that black bear mating was associated with spatial proximity of mates, male age, the time a pair had coexisted, local population density and relatedness. Mated pairs were more likely to contain older males. On average, bears tended to mate with nearby individuals to whom they were related, which does not support the existence of kin recognition in black bears. Pairwise relatedness was especially high for mated pairs containing young males. Restricted dispersal and high male turnover from intensive harvest mortality of NLP black bears are probably the underlying factors associated with younger male bears mating more often with female relatives. Our findings illustrate how harvest has the potential to disrupt the social structure of game species, which warrants further attention for conservation and management.

Red squirrels use territorial vocalizations for kin discrimination

The ability to discriminate among individuals, or among classes of individuals, can provide animals with important fitness benefits. Although several mechanisms for discrimination are possible, most require animals to show stable phenotypic variation that reflects their identity or their membership in a particular class (e.g. sex, mate, kin). For territorial animals that rarely interact physically, vocalizations could serve as long-distance signals that facilitate discrimination. In this study, we tested whether the territorial rattle vocalizations of North American red squirrels, Tamiasciurus hudsonicus, are repeatable, and whether they could hence provide the basis for multiple types of discrimination. We measured four structural features from two rattles from each of 76 marked squirrels. All four features were repeatable, which is consistent with territorial rattles being individually distinctive. We then conducted a playback experiment to determine whether squirrels use rattles for discrimination. Specifically, we tested whether squirrels discriminate between the rattles of neighbours and non-neighbours, and kin (coefficient of relatedness, r ≥ 0.25) and non-kin (r

Rapid and widespread de novo evolution of kin discrimination

Diverse forms of kin discrimination, broadly defined as alteration of social behavior as a function of genetic relatedness among interactants, are common among social organisms from microbes to humans. However, the evolutionary origins and causes of kin-discriminatory behavior remain largely obscure. One form of kin discrimination observed in microbes is the failure of genetically distinct colonies to merge freely upon encounter. Here, we first use natural isolates of the highly social bacterium Myxococcus xanthus to show that colony-merger incompatibilities can be strong barriers to social interaction, particularly by reducing chimerism in multicellular fruiting bodies that develop near colony-territory borders. We then use experimental laboratory populations to test hypotheses regarding the evolutionary origins of kin discrimination. We show that the generic process of adaptation, irrespective of selective environment, is sufficient to repeatedly generate kin-discriminatory behaviors between evolved populations and their common ancestor. Further, we find that kin discrimination pervasively evolves indirectly between allopatric replicate populations that adapt to the same ecological habitat and that this occurs generically in many distinct habitats. Patterns of interpopulation discrimination imply that kin discrimination phenotypes evolved via many diverse genetic mechanisms and mutation-accumulation patterns support this inference. Strong incompatibility phenotypes emerged abruptly in some populations but strengthened gradually in others. The indirect evolution of kin discrimination in an asexual microbe is analogous to the indirect evolution of reproductive incompatibility in sexual eukaryotes and linguistic incompatibility among human cultures, the commonality being indirect, noncoordinated divergence of complex systems evolving in isolation.

Post-birth separation affects the affiliative behaviour of kin in a pitviper with maternal attendance

The relatedness of individuals can have pronounced effects on behavioural interactions, as engaging in mutually beneficial behaviours with kin can increase inclusive fitness. Parental care can be particularly important for kin discrimination in birds and mammals, but similar studies have not been conducted on species exhibiting more rudimentary forms of care. Maternal attendance of young is ubiquitous among viviparous temperate pitvipers, but the adaptive value of this behaviour has received little attention. We sought to determine if being deprived of a maternal attendance period as neonates altered how cottonmouths (Agkistrodon piscivorus Lacépède), a common North American pitviper, responded to kin vs. non-kin. We measured the affiliative behaviour of related and unrelated juvenile–juvenile and mother–juvenile pairs that had been allowed a maternal attendance period or had been separated since birth. We found that maternal attendance was not required for sibling or mother–offspring recognition, but did enhance female affiliative behaviour overall, and particularly that of sisters. In contrast, related juveniles that were separated at birth showed a reversal of the sex-specific affiliative behaviour observed in maternally attended juveniles. Post-birth separation had only a modest effect on mother–juvenile affiliative behaviour, and no effect on the strong affiliation between mothers and daughters. The patterns of affiliative behaviour observed in maternally attended snakes corresponded to patterns that have emerged from previous captive and field studies of pitvipers; however, the behaviour of juveniles separated at birth was atypical. Thus, it is possible that maternal attendance plays some role in the development of adaptive sex-specific and kin-directed affiliative behaviour in pitvipers.

Social shaping of voices does not impair phenotype matching of kinship in mandrills.

Kin selection theory provides a strong theoretical framework to explain the evolution of altruism and cooperative behaviour among genetically related individuals. However, the proximate mechanisms underlying kin discrimination, a necessary process to express kin-related behaviour, remain poorly known. In particular, no study has yet unambiguously disentangled mechanisms based on learned familiarity from true phenotype matching in kin discrimination based on vocal signals. Here we show that in addition to genetic background, social accommodation also shapes individual voices in an Old World monkey (Mandrillus sphinx), even though primate vocalizations were thought to be innate and little flexible. Nonetheless, social shaping of voice parameters does not impair kin discrimination through phenotype-matching of unknown relatives, revealing unexpected discriminatory versatility despite signal complexity. Accurate signal production and perception, therefore, provide a basis for kin identification and kin-biased behaviour in an Old World primate.

Kin discrimination in polyphenic salamander larvae: trade-offs between inclusive fitness and pathogen transmission

Some larval amphibians can develop into two distinct morphological types: a small-headed “normal” morph and a rarer broad-headed morph with specialized adaptations to feed on the normal morph. Cannibalism confers nutritional benefits that accelerate development, essential for survival in transient environments, but incurs potential inclusive fitness costs. Selective cannibalism of non-kin thus should be favored. However, subjects may be more vulnerable to contracting disease from non-siblings to which they lack immunological defenses. We investigated kin discrimination and pathogen transmission among Korean salamander (Hynobius leechii) larvae. We placed broad-headed morph larvae into a circular arena together with two normal morph larvae, one their sibling and the other a non-sibling. To test for kin discrimination, we recorded all behavioral interactions among them. To study pathogen transmission, we fed broad-headed larvae either a sibling or non-sibling normal larva that we previously had infected with the bacterium Aeromonas hydrophila. Two days after ingestion, we determined whether the bacterium had systemically infected cannibals by quantitative PCR (qPCR). Broad-headed larvae discriminated between sibling and non-sibling normal larvae, directing aggressive behaviors mostly toward siblings. Infection loads varied more widely among broad-headed larvae that cannibalized non-siblings than those that cannibalized siblings, but the highest infection loads were recorded after ingestion of non-siblings. Cannibalizing non-siblings thus may increase the risk of contracting disease. Broad-headed larvae discriminate most strongly between siblings and non-siblings late in development, when inclusive fitness costs of cannibalizing relatives diminish and vulnerability to novel pathogens transmitted by non-relatives rises.

Major urinary protein (MUP) profiles show dynamic changes rather than individual 'barcode' signatures.

House mice (Mus musculus) produce a variable number of major urinary proteins (MUPs), and studies suggest that each individual produces a unique MUP profile that provides a distinctive odor signature controlling individual and kin recognition. This 'barcode hypothesis' requires that MUP urinary profiles show high individual variability within populations and also high individual consistency over time, but tests of these assumptions are lacking. We analyzed urinary MUP profiles of 66 wild-caught house mice from eight populations using isoelectric focusing. We found that MUP profiles of wild male house mice are not individually unique, and though they were highly variable, closer inspection revealed that the variation strongly depended on MUP band type. The prominent ('major) bands were surprisingly homogenous (and hence most MUPs are not polymorphic), but we also found inconspicuous ('minor') bands that were highly variable and therefore potential candidates for individual fingerprints. We also examined changes in urinary MUP profiles of 58 males over time (from 6 to 24 weeks of age), and found that individual MUP profiles and MUP concentration were surprisingly dynamic, and showed significant changes after puberty and during adulthood. Contrary to what we expected, however, the minor bands were the most variable over time, thus no good candidates for individual fingerprints. Although MUP profiles do not provide individual fingerprints, we found that MUP profiles were more similar among siblings than non-kin despite considerable fluctuation. Our findings show that MUP profiles are not highly stable over time, they do not show strong individual clustering, and thus challenge the barcode hypothesis. Within-individual dynamics of MUP profiles indicate a different function of MUPs in individual recognition than previously assumed and advocate an alternative hypothesis ('dynamic changes' hypothesis).

Does relatedness influence migratory timing and behaviour in Atlantic salmon smolts?

Aggregating and moving with relatives may enable animals to increase opportunities for kin selection to occur. To gain group-living benefits, animals must coordinate their behaviour. Atlantic salmon, Salmo salar, demonstrate both territoriality and schooling: the two key social behaviours performed by fish. In this investigation we compared the migratory timing and behaviour of six distinct full-sibling groups of tagged S. salar smolts with a large control sample from the same wild population. The results clearly demonstrate that the incidence of schooling and diel migratory timing is not significantly influenced by relatedness, and this adds further support to the hypothesis that S. salar smolt migration is primarily an adaptive response to environmental conditions, rather than a behaviour based solely on genetics or kin-biased behaviour. Used in conjunction with the results of two previous investigations, this is the first study to illustrate that kin discrimination among full-sibling groups of parr does not lead to kin-biased schooling in smolts. Thus, even within the same full-sibling groups, the extent of kin-biased behaviour in fish can both differ within a life history stage under varying ecological conditions and shift from one life history stage to the next.

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.

Genetic studies on the Cayo Santiago rhesus macaques: A review of 40 years of research.

Genetic studies not only contribute substantially to our current understanding of the natural variation in behavior and health in many species, they also provide the basis of numerous in vivo models of human traits. Despite the many challenges posed by the high level of biological and social complexity, a long lifespan and difficult access in the field, genetic studies of primates are particularly rewarding because of the close evolutionary relatedness of these species to humans. The free-ranging rhesus macaque (Macaca mulatta) population on Cayo Santiago (CS), Puerto Rico, provides a unique resource in this respect because several of the abovementioned caveats are of either minor importance there, or lacking altogether, thereby allowing long-term genetic research in a primate population under constant surveillance since 1956. This review summarizes more than 40 years of genetic research carried out on CS, from early blood group typing and the genetic characterization of skeletal material via population-wide paternity testing with DNA fingerprints and short tandem repeats (STRs) to the analysis of the highly polymorphic DQB1 locus within the major histocompatibility complex (MHC). The results of the paternity studies also facilitated subsequent studies of male dominance and other factors influencing male reproductive success, of male reproductive skew, paternal kin bias, and mechanisms of paternal kin recognition. More recently, the CS macaques have been the subjects of functional genetic and gene expression analyses and have played an important role in behavioral and quantitative genetic studies. In addition, the CS colony has been used as a natural model for human adult-onset macular degeneration, glaucoma, and circadian rhythm disorder. Our review finishes off with a discussion of potential future directions of research on CS, including the transition from STRs to single nucleotide polymorphism (SNP) typing and whole genome sequencing.

Social living without kin discrimination: experimental evidence from a communally breeding bird

In many cooperative animal societies, individuals can recognize their relatives and preferentially direct helping behaviors towards them. However, the ability to learn kin recognition cues may be constrained in societies with low relatedness, since group membership alone is not a reliable proxy for kinship. Here, we examine kin discrimination in the greater ani (Crotophaga major), a communally nesting bird in which several unrelated males and females reproduce in a single, shared nest and provide parental care to the mixed clutch of young. Each adult, therefore, is closely related to some nestlings in the clutch and unrelated to others. Food is limited and starvation is a significant cause of nestling mortality, suggesting that adults should increase their fitness by preferentially feeding their own offspring in the mixed clutch. To test this hypothesis, we cross-fostered broods of nestlings between pairs of nests, such that none of the nestlings in the manipulated nests were related to any of the adults feeding them. We found no evidence that adult greater anis discriminate between their own and unrelated nestlings: adults at cross-fostered groups fed nestlings at the same rates as adults at control (sham-manipulated) nests, and rates of nestling starvation were equal at cross-fostered and control nests. These results suggest that adult greater anis do not recognize their own nestlings, and they are consistent with the hypothesis that genetically encoded markers for kin recognition are rare in birds.

Temporal regulation of kin recognition maintains recognition-cue diversity and suppresses cheating.

Kin recognition, the ability to distinguish kin from non-kin, can facilitate cooperation between relatives. Evolutionary theory predicts that polymorphism in recognition cues, which is essential for effective recognition, would be unstable. Individuals carrying rare recognition cues would benefit less from social interactions than individuals with common cues, leading to loss of the genetic-cue diversity. We test this evolutionary hypothesis in Dictyostelium discoideum, which forms multicellular fruiting bodies by aggregation and utilizes two polymorphic membrane proteins to facilitate preferential cooperation. Surprisingly, we find that rare recognition variants are tolerated and maintain their frequencies among incompatible majority during development. Although the rare variants are initially excluded from the aggregates, they subsequently rejoin the aggregate and produce spores. Social cheating is also refrained in late development, thus limiting the cost of chimerism. Our results suggest a potential mechanism to sustain the evolutionary stability of kin-recognition genes and to suppress cheating.

Female major histocompatibility complex type affects male testosterone levels and sperm number in the horse (Equus caballus).

Odours of vertebrates often contain information about the major histocompatibility complex (MHC), and are used in kin recognition, mate choice or female investment in pregnancy. It is, however, still unclear whether MHC-linked signals can also affect male reproductive strategies. We used horses (Equus caballus) to study this question under experimental conditions. Twelve stallions were individually exposed either to an unfamiliar MHC-similar mare and then to an unfamiliar MHC-dissimilar mare, or vice versa. Each exposure lasted over a period of four weeks. Peripheral blood testosterone levels were determined weekly. Three ejaculates each were collected in the week after exposure to both mares (i.e. in the ninth week) to determine mean sperm number and sperm velocity. We found high testosterone levels when stallions were kept close to MHC-dissimilar mares and significantly lower ones when kept close to MHC-similar mares. Mean sperm number per ejaculate (but not sperm velocity) was positively correlated to mean testosterone levels and also affected by the order of presentation of mares: sperm numbers were higher if MHC-dissimilar mares were presented last than if MHC-similar mares were presented last. We conclude that MHC-linked signals influence testosterone secretion and semen characteristics, two indicators of male reproductive strategies.

Social evolution in the shadow of asymmetrical relatedness.

The persistence of altruism and spite remains an enduring problem of social evolution. It is well known that selection for these actions depends on the structure of the population-that is, on actors' genetic relationships to recipients and to the 'neighbourhood' upon which the effects of their actions redound. Less appreciated, however, is that population structure can cause genetic asymmetries between partners whereby the relatedness (defined relative to the neighbourhood) of an individual i to a partner j will differ from the relatedness of j to i. Here, we introduce a widespread mechanism of kin recognition to a model of dispersal in subdivided populations. In so doing, we uncover three remarkable consequences of asymmetrical relatedness. First, altruism directed at phenotypically similar partners evolves more easily among migrant than native actors. Second, spite directed at dissimilar partners evolves more easily among native than migrant actors. Third, unlike migrants, natives can evolve to pay costs that far outstrip those they spitefully impose on others. We find that the frequency of natives relative to migrants amplifies the asymmetries between them. Taken together, our results reveal differentiated patterns of 'phenocentrism' that readily arise from asymmetries of relatedness.