The Genetic Basis of Kin Recognition in a Cooperatively Breeding Mammal

Abstract

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.

Diversity of major urinary proteins (MUPs) in wild house mice

“…We found surprisingly low levels of inter-individual variation in MUP genes and proteins in populations of wild house mice, contrary to suggestions that both are highly polymorphic23456. Through DNA sequencing, we found no individual variation, and every individual carried the same two distinct Mup variants.…”

“…Our findings indicate the electrophoretic methods used for studying MUPs for the past 80 years215 – to infer similarity2, diversity111315 and other variations in MUPs3036, including hormonal regulation3738 and epigenetic control39, need to be re-evaluated. Gel-based methods provided the basis for the barcode hypothesis and claims that MUPs are highly polymorphic24 – and therefore, the hypothesis that MUPs mediate individual odour and genetic kin recognition (inbreeding avoidance)234613 also needs to be re-evaluated. The low individual variation of Mup genes and linked microsatellites suggest that these genes are evolving under purifying selection26, perhaps through a selective sweep in this large region40, and the high homology of different Mup loci may be generated by concerted evolution (gene conversion)4142.…”

“…MUPs are often suggested to be highly polymorphic (high individual variation), and provide distinctive olfactory cues that mediate individual recognition, genetic kin recognition, and inbreeding avoidance (barcode hypothesis)23456. However, almost nothing is known about the variation of MUPs at the genetic or protein level, or how such diversity might be maintained by natural selection.…”

Molecular heterogeneity in major urinary proteins of Mus musculus subspecies: potential candidates involved in speciation

“…Olfactory mating signals present in mouse urine were pointed out as potential candidates for this divergence2225. Hence we targeted a well-known family of semiochemicals (chemicals used for communication between organisms) for which roles in social and sexual communication have been established: the major urinary proteins, known as MUPs2829303132333435363738. Comparison of the two European subspecies of the house mouse from the border of the Bavarian-Czech Republic hybrid zone has revealed quantitative variation in the expression of mRNA for MUPs in the liver and in total urinary MUP concentration39.…”

Preface: Pheromone-Mediation of Female Reproduction and Reproductive Dominance in Social Species

“…Furthermore, the effect can be fully achieved whether using live females or only with their urine (Drickamer 1974;McIntosh and Drickamer 1977), suggesting that the signal is coercive. Male urine constituents are also known to regulate female physiology (Coombes et al 2018), and in turn, females relate to male urine when choosing mate (Green et al 2015). However, the house mouse system is one of the few systems in which our understanding of the reproductive signaling system is comprehensive, and similar investigations, particularly in social insect species, are warranted.…”