Breeding status affects motoneuron number and muscle size in naked mole‐rats: Recruitment of perineal motoneurons?

Abstract

Naked mole-rats live in large colonies and exhibit a strict reproductive hierarchy. Each colony has one breeding female and one to three breeding males; all other individuals are nonreproductive subordinates. Subordinates show a remarkable lack of sex differences in behavior and anatomy, but can become reproductive if removed from the colony. We recently reported that the striated perineal muscles and their innervating motoneurons, which are sexually dimorphic in all other mammals examined to date, are not dimorphic in subordinate naked mole-rats. Here we asked whether sexual differentiation of this neuromuscular system occurs when a subordinate becomes a breeder. The size and number of cells within Onuf's nucleus (homologue of the rat spinal nucleus of the bulbocavernosus) as well as perineal muscle volume were examined in subordinate and breeding naked mole-rats of both sexes. Sex differences in perineal motoneurons were not observed, regardless of social status. To our surprise, however, counts of motoneurons in Onuf's nucleus were increased approximately 30% in breeders of both sexes. This was accompanied by a reciprocal decrease in cells in Onuf's nucleus that were characterized by small soma size, and lacked a clear nucleus or nucleolus. Although not exhibiting typical motoneuron morphology, some of these small cells were positive for the motoneuron marker, SMI-32. The neuronal changes correlate with increased perineal muscle volumes in breeders. We propose that small, relatively undifferentiated cells are recruited to the pool of large Onuf's nucleus motoneurons when subordinate naked mole-rats become breeders.

Social status and sex independently influence androgen receptor expression in the eusocial naked mole-rat brain

“…The present data are in accord with previous observations that social status influences the nervous system of naked mole-rats (Holmes et al, 2007;Seney et al, 2006). The most consistent finding was a reduced percentage of AR+ nuclei in breeders.…”

“…Among subordinates, there are no sex differences in overall body size, ano-genital distance, or the expression of a large variety of behaviors Pepper et al, 1991;Peroulakis et al, 2002). In addition, we have recently demonstrated that naked mole-rats lack many of the sexual dimorphisms in the brain and spinal cord that are seen in other mammals (Holmes et al, 2007;Peroulakis et al, 2002;Seney et al, 2006). We hypothesize that the reduction in sex differences in naked mole-rats may be related to their unique reproductive strategy.…”

“…Animal history and housing conditions have previously been described (Holmes et al, 2007;Seney et al, 2006). Briefly, age-matched animals were randomly assigned to remain subordinate or become breeders.…”

“…This suggests the potential for extensive physiological, behavioral, and neural plasticity in adulthood. Indeed, when animals were randomly assigned to remain subordinates within their colony, or to become new breeders, we previously found several changes in nervous system morphology associated with social and reproductive status (Holmes et al, 2007;Seney et al, 2006). Gonadally intact breeders, regardless of sex, had more neurons in the ventromedial nucleus of the hypothalamus (VMH), larger overall volumes of the bed nucleus of the stria terminalis (BST), paraventricular nucleus (PVN) and medial amygdala (MeA), and more motoneurons in Onuf's nucleus than subordinates.…”

Social regulation of adult neurogenesis in a eusocial mammal

“…Likewise, colonyhoused subordinates may become breeders if sexual suppression is lifted by a former breeder's death or removal (Margulis et al, 1995;Clarke and Faulkes, 1997). Though pronounced alterations in neural and endocrine functions accompany the change (Faulkes et al, 1990a;Margulis et al, 1995;Clarke and Faulkes, 1997;Seney et al, 2006;Holmes et al, 2008;Holmes et al, 2011;Mooney and Holmes, 2013), many or all subordinates are capable of transitioning to breeding status under the appropriate social conditions. This striking behavioural and physiological plasticity displayed by otherwise mature subordinates makes the naked mole-rat a prime candidate for the study of adult neurogenesis.…”