We previously found no sexual dimorphism in any of the several brain regions examined in naked mole-rats, but breeders, regardless of sex, had larger volumes of the BSTp, PVN, and MeA than did subordinates [Holmes et al., 2007
]. Similarly, the present data indicate that reproductive status influences regional brain volume in Damaraland mole-rats: both the BSTp and PVN were larger in breeders than in subordinates. The effect of status also extended to cell size in some regions; breeders had larger cells in the PVN and MeA than did subordinates. In contrast to what was seen previously for naked mole-rats, however, we also observed sexual dimorphisms in Damaraland mole-rats. Males had larger MeA volumes than did females, regardless of status. A similar pattern was seen in the number of motoneurons in ON (i.e. males had more motoneurons than did females) although in this case the effect was clearly larger among breeders than subordinates. Collectively, these data reveal that both social status and sex influence the morphology of reproductive neural regions in this species and appear to do so in a region-specific manner.
Because breeders were older than subordinates in this study, we cannot rule out the possibility that differences between the subordinate and breeder groups were due to age and not social status. This seems unlikely for several reasons. First, all of the Damaraland mole-rats in the current study were well into adulthood, yet far from senescence, and breeders and subordinates did not differ in body size. We also do not know of any example of progressive increases in nuclear volume with age among adult animals (although there are some examples of shrinking with aging). In regression analyses, while we did see a significant relationship between age and SCN cell size in subordinates (table ), no other relationships between age and neural morphology were detected. Similarly, there were no significant correlations between age and neural morphology in naked mole-rats [Holmes et al., 2011
]. Therefore, it seems more likely that the changes in both species of mole-rat reflect differences in reproductive and social status.
The function of the changes seen in breeders is not known. The neural changes may be required to trigger behavioral and neuroendocrine functioning associated with reproduction or may be a response to changes in the hormonal or social milieu that accompany the transition to breeding status. The PVN is a crucial node at the crossroads of the hypothalamic-pituitary-adrenal and hypothalamic-pituitary-gonadal axes. The BSTp and MeA are involved in the processing of pheromonal input in other rodents and have associated roles in controlling neuroendocrine function and sexual behavior [Simerly, 2002
]. The BSTp has also been implicated in the regulation of stress responses in other rodents via its projections to the PVN [Choi et al., 2008
]. While the relationship between stress and social status in naked mole-rats is not simple [Clarke and Faulkes, 1997
], it seems likely that at least some components of the hypothalamic-pituitary-adrenal axis are affected when an animal becomes a breeder. Furthermore, most sex differences in other species are due to either developmental or adult differences in gonadal hormones [Morris et al., 2004
]. Presumably gonadal hormones affect in some way the structure and/or function of reproductive brain nuclei in the mole-rat brain, although we have yet to demonstrate this.
We did not see an effect of breeding status on MeA volume in Damaraland mole-rats. We previously reported a breeding status effect in naked mole-rats when we compared subordinates to gonadally intact breeders living within their colony [Holmes et al., 2007
]. More recently, however, we saw no effect of status on MeA volume comparing subordinate naked mole-rats to breeders that had produced pups but not raised them (i.e. animals were paired but because no pups were raised they were not in a colony) [Holmes et al., 2011
]. Similarly, the breeding Damaraland mole-rats in the present report were paired animals that had produced at least 1 litter but had not successfully raised any pups to adulthood. Thus, status effects on MeA morphology may require the breeding animals to be housed within a colony (i.e. to actually be socially dominant). This is an intriguing idea that warrants further investigation. Regardless, the effect of sex on MeA morphology that we report distinguishes the Damaraland mole-rat from both of our previous naked mole-rat reports [Holmes et al., 2007
]. We also found a sex difference in ON motoneuron number in Damaraland mole-rats consistent with all other mammalian species studied [e.g. Breedlove and Arnold, 1980
; Forger and Breedlove, 1986
; Ulibarri et al., 1995
; Polak and Freeman, 2010
], with the exception of the naked mole-rat [Peroulakis et al., 2002
; Seney et al., 2006
]. Thus, the current findings demonstrate that sex can
influence neural morphology in a eusocial mammal.
We propose that differences in the degree of sexual dimorphism between naked mole-rats and Damaraland mole-rats are related to species differences in reproductive skew. Damaraland mole-rats live in smaller colonies and have smaller litters; as a result, subordinates have a greater likelihood of becoming reproductive relative to naked mole-rats [Jarvis et al., 1994
; Bennett and Faulkes, 2000
]. Thus, Damaraland mole-rats may be somewhat of an intermediate species in terms of reproductive skew: they show more reproductive skew than laboratory rats or mice but less than naked mole-rats. Indeed, we have recently demonstrated that the morphology of the external genitalia of these animals is related to social structure [Seney et al., 2009
]. Specifically, we compared the genitals and perineal muscles of Damaraland mole-rats, naked mole-rats, and silvery mole-rats (Heliophobius argenteocinereus),
a solitary mole-rat species in which all individuals that reach adulthood may reproduce [Bennett and Faulkes, 2000
]. We found that naked mole-rats lacked sex differences in genitalia and perineal morphology (and, indeed, had status differences), silvery mole-rats exhibited sex differences in these measures, and Damaraland mole-rats were intermediate [Seney et al., 2009
African mole-rats exhibit a vast range of sociality within a phylogenetically similar group, thus providing the opportunity to test hypotheses regarding evolved associations between social structure, reproductive skew and physiology, anatomy, and behavior. The present data demonstrate that social status influences neural morphology in Damaraland mole-rats, as it does in the eusocial naked mole-rat, but also reveals sex differences in the Damaraland mole-rat nervous system. This species appears intermediate between the highly social naked mole-rat and less social traditional laboratory rodents when it comes to the degree of sexual differentiation of the nervous system. We propose that the relative importance of social status and sex in organizing neural morphology is the result of species differences in reproductive skew and, proximately, is likely due to species-specific specializations in neuroendocrine function.