Cooperatively breeding banded mongooses do not avoid inbreeding through familiarity-based kin recognition

In species that live in family groups, such as cooperative breeders, inbreeding is usually avoided through the recognition of familiar kin. For example, individuals may avoid mating with conspecifics encountered regularly in infancy, as these likely include parents, siblings, and closely related alloparents. Other mechanisms have also been reported, albeit rarely; for example, individuals may compare their own phenotype to that of others, with close matches representing likely relatives (“phenotype matching”). However, determinants of the primary inbreeding avoidance mechanisms used by a given species remain poorly understood. We use 24 years of life history and genetic data to investigate inbreeding avoidance in wild cooperatively breeding banded mongooses (Mungos mungo). We find that inbreeding avoidance occurs within social groups but is far from maximised (mean pedigree relatedness between 351 breeding pairs = 0.144). Unusually for a group-living vertebrate, we find no evidence that females avoid breeding with males with which they are familiar in early life. This is probably explained by communal breeding; females give birth in tight synchrony and pups are cared for communally, thus reducing the reliability of familiarity-based proxies of relatedness. We also found little evidence that inbreeding is avoided by preferentially breeding with males of specific age classes. Instead, females may exploit as-yet unknown proxies of relatedness, for example, through phenotype matching, or may employ postcopulatory inbreeding avoidance mechanisms. Investigation of species with unusual breeding systems helps to identify constraints against inbreeding avoidance and contributes to our understanding of the distribution of inbreeding across species. Significance statement Choosing the right mate is never easy, but it may be particularly difficult for banded mongooses. In most social animals, individuals avoid mating with those that were familiar to them as infants, as these are likely to be relatives. However, we show that this rule does not work in banded mongooses. Here, the offspring of several mothers are raised in large communal litters by their social group, and parents seem unable to identify or direct care towards their own pups. This may make it difficult to recognise relatives based on their level of familiarity and is likely to explain why banded mongooses frequently inbreed. Nevertheless, inbreeding is lower than expected if mates are chosen at random, suggesting that alternative pre- or post-copulatory inbreeding avoidance mechanisms are used.

It’s all relative: population estimates enhance kin recognition in the guppy

Kin recognition plays a fundamental role in social evolution, enabling active inbreeding avoidance, nepotism, and promoting cooperative social organization. Many organisms recognize kin based on phenotypic similarity – a process called phenotype matching – by comparing information associated with their own phenotype against the phenotypes of conspecifics. However, recent theory demonstrates that to accurately judge phenotypic similarity (and hence, relatedness), individuals require estimates of the population’s distribution of phenotypes as a “frame of reference.” Here, I use the Trinidadian guppy (Poecilia reticulata) to provide the first empirical test of this population estimation theory. I varied the phenotypic distributions of the groups in which focal individuals developed and found that, as adults, their patterns of inbreeding avoidance and nepotistic intrasexual competition differed as predicted by population estimation theory. Individuals reared with conspecifics more similar to themselves treated novel conspecifics as less closely related, suggesting a shifted population estimate. Individuals reared with more phenotypically variable conspecifics exhibited less extreme kin discrimination, suggesting a broader population estimate. These results provide experimental evidence that population estimates inform phenotype matching, and are acquired plastically through social experience. By calibrating phenotype matching to the population distribution of phenotypes, population estimation enhances kin recognition, increasing opportunities for the evolution of inbreeding avoidance and nepotism.

Multiple models generate a geographical mosaic of resemblance in a Batesian mimicry complex

Batesian mimics—benign species that receive protection from predation by resembling a dangerous species—often occur with multiple model species. Here, we examine whether geographical variation in the number of local models generates geographical variation in mimic–model resemblance. In areas with multiple models, selection might be relaxed or even favour imprecise mimicry relative to areas with only one model. We test the prediction that model–mimic match should vary with the number of other model species in a broadly distributed snake mimicry complex where a mimic and a model co-occur both with and without other model species. We found that the mimic resembled its model more closely when they were exclusively sympatric than when they were sympatric with other model species. Moreover, in regions with multiple models, mimic–model resemblance was positively correlated with the resemblance between the model and other model species. However, contrary to predictions, free-ranging natural predators did not attack artificial replicas of imprecise mimics more often when only a single model was present. Taken together, our results suggest that multiple models might generate a geographical mosaic in the degree of phenotype matching between Batesian mimics and their models.

Kin discrimination via odour in the cooperatively breeding banded mongoose

Kin discrimination is often beneficial for group-living animals as it aids in inbreeding avoidance and providing nepotistic help. In mammals, the use of olfactory cues in kin discrimination is widespread and may occur through learning the scents of individuals that are likely to be relatives, or by assessing genetic relatedness directly through assessing odour similarity (phenotype matching). We use scent presentations to investigate these possibilities in a wild population of the banded mongoose Mungos mungo , a cooperative breeder in which inbreeding risk is high and females breed communally, disrupting behavioural cues to kinship. We find that adults show heightened behavioural responses to unfamiliar (extra-group) scents than to familiar (within-group) scents. Interestingly, we found that responses to familiar odours, but not unfamiliar odours, varied with relatedness. This suggests that banded mongooses are either able to use an effective behavioural rule to identify likely relatives from within their group, or that phenotype matching is used in the context of within-group kin recognition but not extra-group kin recognition. In other cooperative breeders, familiarity is used within the group and phenotype matching may be used to identify unfamiliar kin. However, for the banded mongoose this pattern may be reversed, most likely due to their unusual breeding system which disrupts within-group behavioural cues to kinship.