Neuroendocrinology and sexual differentiation in eusocial mammals

Abstract

Sexual differentiation of the mammalian nervous system has been studied intensively for over 25 years. Most of what we know, however, comes from work on relatively non-social species in which direct reproduction (i.e., production of offspring) is virtually the only route to reproductive success. In social species, an individual's inclusive fitness may include contributions to the gene pool that are achieved by supporting the reproductive efforts of close relatives; this feature is most evident in eusocial organisms. Here, we review what is known about neuroendocrine mechanisms, sexual differentiation, and effects of social status on the brain and spinal cord in two eusocial mammals: the naked mole-rat and Damaraland mole-rat. These small rodents exhibit the most rigidly organized reproductive hierarchy among mammals, with reproduction suppressed in a majority of individuals. Our findings suggest that eusociality may be associated with a relative lack of sex differences and a reduced influence of gonadal hormones on some functions to which these hormones are usually tightly linked. We also identify neural changes accompanying a change in social and reproductive status, and discuss the implications of our findings for understanding the evolution of sex differences and the neuroendocrinology of reproductive suppression.

Telencephalic binding sites for oxytocin and social organization: A comparative study of eusocial naked mole‐rats and solitary cape mole‐rats

“…The similarity of OTR binding in female and male subordinates is consistent with their high degree of neuroanatomical monomorphism (Peroulakis et al, 2002;Holmes et al, 2007Holmes et al, , 2009. We speculate that oxytocin receptors at this site also provide a substrate for the reproductive attachments that are made by the few subordinates that either succeed their queen or her consorts or disperse to form new colonies.…”

Lack of sexual dimorphism in femora of the eusocial and hypogonadic naked mole-rat: A novel animal model for the study of delayed puberty on the skeletal system

“…If this were indeed the case, our data would support neural morphological studies in this species which report that NMR breeders lack many of the sex differences in the brain and spinal cord commonly found in other rodents [27, 49]. Indeed their studies found no evidence of sexual dimorphism; rather breeders, regardless of sex, differed substantially from the subordinates by having more neurons in the ventromedial nucleus of the hypothalamus (VMH), larger overall volumes of specific brain regions and pronounced differences in perineal muscles and motor neurons [49, 50]. …”

Region-specific associations between sex, social status, and oxytocin receptor density in the brains of eusocial rodents

“…While many animals take part in pup care at some level, the breeding female is the only animal that nurses; breeding males also perform more general pup care than subordinates (Lacey and Sherman, 1991). Furthermore, comparisons between breeders and subordinates reveal remarkable neural differences (Holmes et al, 2007(Holmes et al, , 2008(Holmes et al, , 2009(Holmes et al, , 2011Mooney and Holmes, 2013;Zhou et al, 2013). The interesting relationships between brain, behavior, and reproductive status observed in this cooperatively breeding species offer opportunities for investigating whether OTR binding contributes to within-species phenotypes.…”