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Dominance is a primary determinant of social dynamics and resource access in social animals. Recent studies show that dominance is also reflected in the gene regulatory profiles of peripheral immune cells. However, the strength and direction of this relationship differs across the species and sex combinations investigated, potentially due to variation in the predictors and energetic consequences of dominance status. Here, we investigated the association between social status and gene expression in the blood of wild meerkats (Suricata suricatta; n = 113 individuals), including in response to lipopolysaccharide, Gardiquimod (an agonist of TLR7, which detects single-stranded RNA in vivo) and glucocorticoid stimulation. Meerkats are cooperatively breeding social carnivores in which breeding females physically outcompete other females to suppress reproduction, resulting in high reproductive skew. They therefore present an opportunity to disentangle the effects of social dominance from those of sex per se. We identify a sex-specific signature of dominance, including 1045 differentially expressed genes in females but none in males. Dominant females exhibit elevated activity in innate immune pathways and a larger fold-change response to LPS challenge. Based on these results and a preliminary comparison to other mammals, we speculate that the gene regulatory signature of social status in the immune system depends on the determinants and energetic costs of social dominance, such that it is most pronounced in hierarchies where physical competition is important and reproductive skew is large. Such a pattern has the potential to mediate life history trade-offs between investment in reproduction versus somatic maintenance., (© 2024 The Author(s). Molecular Ecology published by John Wiley & Sons Ltd.)

Across taxa, breeding among close relatives is usually avoided because it incurs fitness costs to offspring. Incest is often averted through the dispersal of either sex from the natal area to breed. In some philopatric species, association among relatives extends into adulthood, and an ability to discriminate kin may be required for individuals to reduce inbreeding risk. Here, we aim to determine the mechanism of kin recognition for incest avoidance in the Damaraland mole-rat Fukomys damarensis , a cooperative breeder characterized by extreme reproductive skew. Pairs of opposite-sex adults were formed in the laboratory and, within pairs, genetic relatedness and degree of familiarity were manipulated through cross-fostering experiments. We found that unfamiliar pairs were more likely to engage in sexual behaviours and bred more successfully than familiar pairs, regardless of their genetic similarity. Females paired with unfamiliar males were also more likely to exhibit reproductive activation, characterized by increased levels of oestradiol and progesterone. This study shows that in Damaraland mole-rats, inbreeding avoidance can be achieved through a discrimination mechanism that relies on association during rearing, and that ovulation is induced by mating. This study advances our understanding of incest avoidance in species with constrained dispersal.

Mating between closely related individuals can result in a reduction in offspring fitness, known as inbreeding depression. Here, we investigate whether breeding with close relatives affects the reproductive output of parents and the development of their offspring in Damaraland mole-rats ( Fukomys damarensis ), a cooperatively breeding species where females avoid mating with familiar individuals. By cross-fostering litters of pups soon after birth, we were able to form breeding pairs from full siblings that were reared apart. We compared the reproductive output of these sibling pairs and the survival and growth of their pups with that of unrelated pairs over a period of 4 years. The litter sizes and interbirth intervals of sibling pairs did not differ from those of unrelated pairs, but the growth and survival of inbred offspring were lower, showing that breeding between close relatives is associated with substantial fitness costs. This study suggests that inbreeding depression is an important driver of the extreme reproductive skew observed in social mole-rats. Studies of the costs of inbred matings are now needed in similar species, such as naked mole-rats ( Heterocephalus glaber ), where captive females more commonly breed with close relatives, to determine whether these costs are lower than in Damaraland mole-rats.