Key points An ex vivo preparation was developed to record from single sensory fibres innervating the glabrous skin of the mouse forepaw.The density of mechanoreceptor innervation of the forepaw glabrous skin was found to be three times higher than that of hindpaw glabrous skin.Rapidly adapting mechanoreceptors that innervate Meissner's corpuscles were severalfold more responsive to slowly moving stimuli in the forepaw compared to those innervating hindpaw skin.We found a distinct group of small hairs in the centre of the mouse hindpaw glabrous skin that were exclusively innervated by directionally sensitive D‐hair receptors.The directional sensitivity, but not the end‐organ anatomy, were the opposite to D‐hair receptors in the hairy skin.Glabrous skin hairs in the hindpaw are not ubiquitous in rodents, but occur in African and North American species that diverged more than 65 million years ago. AbstractRodents use their forepaws to actively interact with their tactile environment. Studies on the physiology and anatomy of glabrous skin that makes up the majority of the forepaw are almost non‐existent in the mouse. Here we developed a preparation to record from single sensory fibres of the forepaw and compared anatomical and physiological receptor properties to those of the hindpaw glabrous and hairy skin. We found that the mouse forepaw skin is equipped with a very high density of mechanoreceptors; >3 times more than hindpaw glabrous skin. In addition, rapidly adapting mechanoreceptors that innervate Meissner's corpuscles of the forepaw were severalfold more sensitive to slowly moving mechanical stimuli compared to their counterparts in the hindpaw glabrous skin. All other mechanoreceptor types as well as myelinated nociceptors had physiological properties that were invariant regardless of which skin area they occupied. We discovered a novel D‐hair receptor innervating a small group of hairs in the middle of the hindpaw glabrous skin in mice. These glabrous skin D‐hair receptors were direction sensitive albeit with an orientation sensitivity opposite to that described for hairy skin D‐hair receptors. Glabrous skin hairs do not occur in all rodents, but are present in North American and African rodent species that diverged more than 65 million years ago. The function of these specialized hairs is unknown, but they are nevertheless evolutionarily very ancient. Our study reveals novel physiological specializations of mechanoreceptors in the glabrous skin that likely evolved to facilitate tactile exploration.

Mole-rats are strictly subterranean and hardly, if ever, come into contact with external light. As a result, their classical visual system is severely regressed and the circadian system proportionally expanded. The family Bathyergidae presents a unique opportunity to study the circadian system in the absence of the classical visual system in a range of species. Daily patterns of activity were studied in the laboratory under constant temperature but variable lighting regimes in individually housed animals from 3 species of mole-rat exhibiting markedly different degrees of sociality. All 3 species possessed individuals that exhibited endogenous circadian rhythms under constant darkness that entrained to a light-dark cycle. In the solitary species, Georychus capensis, 9 animals exhibited greater activity during the dark phase of the light cycle, while 2 individuals expressed more activity in the light phase of the light cycle. In the social, Cryptomys hottentotus pretoriae, 5 animals displayed the majority of their activity during the dark phase of the light cycle and the remaining 2 exhibited more activity during the light phase of the light cycle. Finally in the eusocial Cryptomys damarensis, 6 animals displayed more activity during the light phase of the light cycle, and the other 2 animals displayed more activity during the dark phase of the light cycle. Since all three mole-rat species are able to entrain their locomotor activity to an external light source, light must reach the SCN, suggesting a functional circadian clock. In comparison to the solitary species, the 2 social species display a markedly poorer response to light in all aspects. Thus, in parallel with the sociality continuum, there exists a continuum of sensitivity of the circadian clock to light.

Eusociality, which occurs among mammals only in two species of African mole-rat, is characterized by division of labour between morphologically distinct 'castes'. In Damaraland mole-rats (Cryptomys damarensis), colony labour is divided between 'infrequent worker' and 'frequent worker' castes. Frequent workers are active year-round and together perform more than 95% of the total work of the colony, whereas infrequent workers typically perform less than 5% of the total work. Anecdotal evidence suggests that infrequent workers may act as dispersers, with dispersal being limited to comparatively rare periods when the soil is softened by moisture. Here we show that infrequent workers and queens increase their daily energy expenditure after rainfall whereas frequent workers do not. Infrequent workers are also fatter than frequent workers. We suggest that infrequent workers constitute a physiologically distinct dispersing caste, the members of which, instead of contributing to the work of the colony and helping the queen to reproduce, build up their own body reserves in preparation for dispersal and reproduction when environmental conditions are suitable.

African mole-rats provide a unique taxonomic group for investigating the evolution and neurobiology of sociality. The two species investigated here display extreme differences in social organization and reproductive strategy. Naked mole-rats (NMRs) live in colonies, dominated by a queen and her consorts; most members remain nonreproductive throughout life but cooperate in burrowing, foraging, and caring for pups, for which they are not biological parents (alloparenting). In contrast, Cape mole-rats (CMRs) are solitary and intolerant of conspecifics, except during fleeting seasonal copulation or minimal maternal behavior. Research on other mammals suggests that oxytocin receptors at various telencephalic sites regulate social recognition, monogamous pair bonding, and maternal/allomaternal behavior. Current paradigms in this field derive from monogamous and polygamous species of New World voles, which are evolutionarily remote from Old World mole-rats. The present findings indicate that NMRs exhibit a considerably greater level of oxytocin receptor (OTR) binding than CMRs in the: nucleus accumbens; indusium griseum; central, medial, and cortical amygdaloid nuclei; bed nucleus of the stria terminalis; and CA1 hippocampal subfield. In contrast, OTR binding in the piriform cortex is intense in CMRs but undetectable in NMRs. We speculate that the abundance of OTR binding and oxytocin-neurophysin-immunoreactive processes in the nucleus accumbens of NMRs reflects their sociality, alloparenting behavior, and potential for reproductive attachments. In contrast, the paucity of oxytocin and its receptors at this site in CMRs may reflect a paucity of prosocial behaviors. Whether similarities in OTR expression between eusocial mole-rats and monogamous voles are due to gene conservation or convergent evolution remains to be determined.

In many vertebrate societies, subordinate females exhibit down-regulated reproductive physiologies relative to those of dominants, a condition commonly termed physiological suppression. Research into the causes of physiological suppression has focused principally on the role of the subordinate's social environment (typically the presence of the dominant female and/or an absence of unrelated males within the group), while few studies have considered the additional role that the physical environment may play. Here we present new evidence from wild Damaraland mole-rats, Fukomys damarensis, revealing that physiological suppression among subordinate females eases markedly during the annual rains (a time when ecological constraints on dispersal are relaxed), despite the continued presence of the dominant female and in groups that contain no new immigrant males. Subordinate females showed substantially higher pituitary sensitivities to GnRH challenge during the wet period than the dry, a contrast that cannot be attributed to between-female differences (as it holds for paired within-female comparisons), associated changes in body mass (as our analyses control for this), or concomitant reductions in physiological stress (as their urinary cortisol concentrations were actually higher in the wet period). We suggest that our findings reflect selection for the maintenance of reproductive readiness among subordinate females during high rainfall periods, given the increased likelihood of encountering dispersal and/or mating opportunities with extra-group males when ecological constraints on dispersal are relaxed.These findings reveal new complexity in the processes that regulate physiological suppression, suggesting a key role in some species for changes in the physical as well as social environment.

African mole-rats (family Bathyergidae) are small to medium sized, long-lived, and strictly subterranean rodents that became valuable animal models as a result of their longevity and diversity in social organization. The formation and integration of new hippocampal neurons in adult mammals (adult hippocampal neurogenesis, AHN) correlates negatively with age and positively with habitat complexity. Here we present quantitative data on AHN in wild-derived mole-rats of 1 year and older, and briefly describe its anatomical context including markers of neuronal function (calbindin and parvalbumin). Solitary Cape mole-rats (Georychus capensis), social highveld mole-rats (Cryptomys hottentotus pretoriae), and eusocial naked mole-rats (Heterocephalus glaber) were assessed. Compared to other rodents, the hippocampal formation in mole-rats is small, but shows a distinct cytoarchitecture in the dentate gyrus and CA1. Distributions of the calcium-binding proteins differ from those seen in rodents; e.g., calbindin in CA3 of naked mole-rats distributes similar to the pattern seen in early primate development, and calbindin staining extends into the stratum lacunosum-moleculare of Cape mole-rats. Proliferating cells and young neurons are found in low numbers in the hippocampus of all three mole-rat species. Resident granule cell numbers are low as well. Proliferating cells expressed as a percentage of resident granule cells are in the range of other rodents, while the percentage of young neurons is lower than that observed in surface dwelling rodents. Between mole-rat species, we observed no difference in the percentage of proliferating cells. The percentages of young neurons are high in social highveld and naked mole-rats, and low in solitary Cape mole-rats. The findings support that proliferation is regulated independently of average life expectancy and habitat. Instead, neuronal differentiation reflects species-specific demands, which appear lower in subterranean rodents.

The doubly labeled water (DLW) technique and indirect calorimetry enable measurement of an animal’s daily energy expenditure (DEE, kJ/day), resting metabolic rate (RMR, kJ/d), sustained metabolic scope (SusMS), body fat content (BF, %) as well as water turnover (WTO, ml/day), and water economy index (ml/kJ). Small mammals have been the primary focus of many of the DLW studies to date. From large multi-species analyses of the energetics and water flux of aboveground small mammals, well-defined trends have been observed. These trends mainly refer to an adaptive advantage for lower RMR, DEE, SusMS, WTO and WEI in more ariddwelling animals to increase water and energy savings under low and unpredictable resource availability. The study of the subterranean rodent family Bathyergidae (African mole-rats) has been of particular interest with regards to field metabolic rate and metabolic studies. Although a great deal of research has been conducted on the Bathyergidae, a complete overview and multi-species analysis of the energetics and water flux of this family is lacking. Consequently, we assessed DEE, RMR, SusMS, BF, WTO and WEI across several different species of bathyergids from various climatic regions, and compared these to the established patterns of energetics and water flux for aboveground rodents. There was notable variation across the Bathyergidae inhabiting areas with different aridities, often contrary to the variations observed in above-ground species. These include increased DEE and WEI in arid-dwelling bathyergid species. While the climate was not a clear factor when predicting the SusMS of a bathyergid species, rather the degree of group living was a strong driver of SusMS, with solitary species possessing the highest SusMS compared to the socially living species. We conclude that the constraints of the underground lifestyle and the consequent spectrum of social behaviors possessed by the family Bathyergidae are most likely to be more crucial to their energetics and water flux than their habitat; however other important unstudied factors may still be at play. More so, this study provides evidence that often unreported parameters, measured through use of the DLW technique (such as BF and WEI) can enable species to be identified that might be at particular risk to climate change.

Lacking fur, living in eusocial colonies and having the longest lifespan of any rodent, makes naked mole-rats (NMRs) rather peculiar mammals. Although they exhibit a high degree of polymorphism, skeletal plasticity and are considered a novel model to assess the effects of delayed puberty on the skeletal system, scarce information on their morphogenesis exists.