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

Abstract

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 statementChoosing 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.