Social control of brain morphology in a eusocial mammal

Abstract

Social status impacts reproductive behavior in diverse vertebrate species, but little is known about how it affects brain morphology. We explore this in the naked mole-rat, a species with the most rigidly organized reproductive hierarchy among mammals. Naked mole-rats live in large, subterranean colonies where breeding is restricted to a single female and small number of males. All other members of the colony, known as subordinates, are reproductively suppressed. Subordinates can become breeders if removed from the colony and placed with an opposite sex partner, but in nature most individuals never attain reproductive status. We examined the brains of breeding and subordinate naked mole-rats of both sexes, including several regions linked to reproduction and shown to be sexually dimorphic in other mammals. Stereological analyses revealed that neural morphology depends on status, such that breeders, regardless of sex, had more cells than subordinates in the ventromedial nucleus of the hypothalamus and a larger volume of the bed nucleus of the stria terminalis, paraventricular nucleus, and medial amygdala. Several other brain regions examined were unaffected. Surprisingly, males and females did not differ on any measure. These findings provide evidence that a change in social status triggers considerable neural remodeling and indicate that status, rather than sex, has a predominant role in determining neural structure in this remarkably social mammal.

Fig. 1.

Social status affects reproductive brain nuclei in naked mole-rats. (A) All subjects initially were adult subordinates (light gray) within the natal colony, which also contains breeders (dark gray) and pups of various ages. One-half of the animals were randomly assigned to remain as colony subordinates (Left). The other one-half were removed from the colony and housed with a subordinate of the opposite sex (Right). These paired animals were defined as breeders when they had produced at least one litter. (B Left) Schematic of the sagittal plane of the brain of a subordinate naked mole-rat illustrating the approximate location of the brain regions examined. Hypothalamic and limbic nuclei are indicated by blue circles; rectangles indicate sites of cortical thickness measurements. (Right) The brain of an animal that has transitioned to breeding status. Green circles indicate regions that are either significantly larger (BSTp, PVN, and MeA) or have more cells (black dots, VMH) in breeders. Regions shaded blue did not differ between subordinates and breeders (SCN, ACo, and cortical thickness).

Fig. 2.

(A–C) Mean (± SEM) regional volume of the BSTp, PVN, and MeA and (D) mean cell number in the VMH of subordinate (Sub) and breeder naked mole-rats. Number of animals per group is noted at the base of each bar. An asterisk indicates a significant main effect of social status. No main effects of sex or status-by-sex interactions were detected for any measure.

Fig. 3.

Photomicrographs illustrate the location of nuclei in thionin-stained coronal sections of the naked mole-rat brain. Shown are BSTp (A); the PVN and SCN (B); MeA and ACo (C); and VMH (D). (Scale bar: 500 μm.)