The Genetic Basis of Kin Recognition in a Cooperatively Breeding Mammal

• Published in: Current biology Vol. 25; no. 20; pp. 2631 - 2641
• Main Authors: Green, Jonathan P., Holmes, Andrew M., Davidson, Amanda J., Paterson, Steve, Stockley, Paula, Beynon, Robert J., Hurst, Jane L.
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 19-10-2015
• Subjects: Animals; Female; Genetic Markers - genetics; Genotype; Major Histocompatibility Complex; Mice - genetics; Mice - physiology; Phenotype; Proteins - genetics; Proteins - metabolism; Recognition (Psychology); Reproduction
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2015.08.045

Cooperation between relatives yields important fitness benefits, but genetic loci that allow recognition of unfamiliar kin have proven elusive. Sharing of kinship markers must correlate strongly with genome-wide similarity, creating a special challenge to identify specific loci used independently of other shared loci. Two highly polymorphic gene complexes, detected through scent, have been implicated in vertebrates: the major histocompatibility complex (MHC), which could be vertebrate wide, and the major urinary protein (MUP) cluster, which is species specific. Here we use a new approach to independently manipulate sharing of putative genetic kin recognition markers, with the animal itself or known family members, while genome-wide relatedness is controlled. This was applied to wild-stock outbred female house mice, which nest socially and often rear offspring cooperatively with preferred nest partners. Females preferred to nest with sisters, regardless of prior familiarity, confirming the use of phenotype matching. Among unfamiliar relatives, females strongly preferred nest partners that shared their own MUP genotype, though not those with only a partial (single-haplotype) MUP match to themselves or known family. In the absence of MUP sharing, females preferred related partners that shared multiple loci across the genome to unrelated females. However, MHC sharing was not used, even when MHC type completely matched their own or that of known relatives. Our study provides empirical evidence that highly polymorphic species-specific kinship markers can evolve where reliable recognition of close relatives is an advantage. This highlights the potential for identifying other genetic kinship markers in cooperative species and calls for better evidence that MHC can play this role.
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•Female house mice use genetic markers to choose closely related nesting partners•They strongly prefer partners sharing their own major urinary protein (MUP) genotype•Without MUP sharing, partners sharing multiple loci across the genome are preferred•MHC sharing is not used; instead, MUP provides a species-specific kinship marker
Female house mice can breed cooperatively and usually select related nest partners, but the genetic markers they use to recognize kin are unknown. Green et al. show that mice prefer partners that match their own major urinary protein (MUP) genotype, a species-specific kinship marker. Contrary to widespread assumption, MHC sharing is not involved.