Genetic diversity of the largest African mole-rat genus, Bathyergus. One, two or four species?

Recent advances in sequencing technology and phylogenetic methods allow us to solve puzzling taxonomic questions using detailed analyses of genetic diversity of populations and gene flow between them. The genus of solitary-living dune mole-rat, Bathyergus, is quite unique among six genera of African mole-rats. The animals are by far the largest and the only scratch digging mole-rat genus possessing a skull less adapted to digging, grooved upper incisors, and more surface locomotor activity. Most authors recognize two species of dune mole-rats, B. suillus and B. janetta, but according to others, the genus is monotypic. In addition, recent molecular studies have revealed cryptic genetic diversity and suggested the existence of up to four species. In our study, we used mitochondrial and genome-wide nuclear data collected throughout the distribution of the genus to investigate the number of species. In agreement with previous studies, we found Bathyergus to be differentiated into several distinct lineages, but we also found evidence for a degree of gene flow between some of them. Furthermore, we confirmed that B. janetta is nested within B. suillus, making the latter paraphyletic and we documented an instance of local mitochondrial introgression between these two nominal species. Phylogeographic structure of the genus was found to be very shallow. Although traditionally dated to the Miocene, we found the first split within the genus to be much younger estimated to 0.82 Ma before present. Genealogical distinctiveness of some lineages was very low, and the coancestry matrix showed extensive sharing of closely related haplotypes throughout the genus. Accordingly, Infomap clustering on the matrix showed all populations to form a single cluster. Overall, our study tends to support the existence of only one species of Bathyergus namely, B. suillus. Environmental niche modelling confirmed its dependence on sandy soils and the preference for soils with relatively high carbon content. Bayesian skyline plots indicate recent population decline in the janetta lineage, probably related to global environmental change.

Functional and morphological divergence in the forelimb musculoskeletal system of scratch-digging subterranean mammals (Rodentia: Bathyergidae).

Whether the forelimb-digging apparatus of tooth-digging subterranean mammals has similar levels of specialization as compared to scratch-diggers is still unknown. We assessed the scapular morphology and forelimb musculature of all four solitary African mole rats (Bathyergidae): two scratch-diggers, Bathyergus suillus and Bathyergus janetta, and two chisel-tooth diggers, Heliophobius argenteocinereus and Georychus capensis. Remarkable differences were detected: Bathyergus have more robust neck, shoulder, and forearm muscles as compared to the other genera. Some muscles in Bathyergus were also fused and often showing wider attachment areas to bones, which correlate well with its more robust and larger scapula, and its wider and medially oriented olecranon. This suggests that shoulder, elbow, and wrist work in synergy in Bathyergus for generating greater out-forces and that the scapula and proximal ulna play fundamental roles as pivots to maximize and accommodate specialized muscles for better (i) glenohumeral and scapular stabilization, (ii) powerful shoulder flexion, (iii) extension of the elbow and (iv) flexion of the manus and digits. Moreover, although all bathyergids showed a similar set of muscles, Heliophobius lacked the m. tensor fasciae antebrachii (aiding with elbow extension and humeral retraction), and Heliophobius and Georychus lacked the m. articularis humeri (aiding with humeral adduction), indicating deeper morphogenetic differences among digging groups and suggesting a relatively less specialized scratch-digging ability. Nevertheless, Heliophobius and Bathyergus shared some similar adaptations allowing scratch-digging. Our results provide new information about the morphological divergence within this family associated with the specialization to distinct functions and digging behaviors, thus contributing to understand the mosaic of adaptations emerging in phylogenetically and ecologically closer subterranean taxa. This and previous anatomical studies on the Bathyergidae will provide researchers with a substantial basis on the form and function of the musculoskeletal system for future kinematic investigations of digging behavior, as well as to define potential indicators of scratch-digging ability.

Non-Invasive Quantification of Faecal and Urine Reproductive Hormone Metabolites in the Naked Mole-Rat (Heterocephalus glaber).

The naked mole-rat (Heterocephalus glaber) occurs in colonies with a distinct dominance hierarchy, including one dominant, breeding female (the queen), 1-3 breeding males, and non-reproductive subordinates of both sexes that are reproductively suppressed while in the colony. To non-invasively evaluate reproductive capacity in the species, we first had to examine the suitability of enzyme immunoassays (EIAs) for determining progestogen and androgen metabolite concentrations in the naked mole-rat, using urine and faeces. A saline control and gonadotrophin-releasing hormone (GnRH) were administered to twelve (six males and six females) naked mole-rats which were previously identified as dispersers and housed singly. The results revealed that urine is possibly not an ideal matrix for progestogen and androgen metabolite quantification in naked mole-rats as no signal was detected in the matrix post GnRH administration. A 5α-Progesterone EIA and an Epiandrosterone EIA were identified as suitable for quantifying faecal progesterone metabolites (fPMs) and faecal androgen metabolites (fAMs) in males and females, respectively. The results suggest that there are individual variations in baseline fPM and fAM concentrations, and only two out of six females and no males exhibited an increase in fPM concentrations greater than 100% (-20% SD) post GnRH administration. Conversely, only four out of six females and three out of six males had an increase in fAM concentrations greater than 100% (-20% SD) following GnRH administration. These results imply that some naked mole-rat individuals have a reduced reproductive capacity even when they are separated from the queen.

Validation of Enzyme Immunoassays via an Adrenocorticotrophic Stimulation Test for the Non-Invasive Quantification of Stress-Related Hormone Metabolites in Naked Mole-Rats.

Small size in mammals usually restricts long-term, frequent monitoring of endocrine function using plasma as a matrix. Thus, the non-invasive monitoring of hormone metabolite concentrations in excreta may provide an invaluable approach. The aim of the current study was to examine the suitability of enzyme immunoassays (EIAs) for monitoring responses to stressors in the naked mole-rat (Heterocephalus glaber, NMR) using urine and feces as hormone matrices. A saline control administration, and a high- and low-dose adrenocorticotropic hormone (ACTH) challenge were performed on six male and six female disperser morph NMRs. The results revealed that a 5α-pregnane-3ß,11ß,21-triol-20-one EIA detecting glucocorticoid metabolites (GCMs) with a 5α-3ß-11ß-diol structure is the most suitable assay for measuring concentrations in male urine samples, whereas an 11-oxoaetiocholanolone EIA detecting GCMs with a 5ß-3α-ol-11-one structure appears the most suitable EIA for quantifying GCMs in female urine. An 11-oxoaetiocholanolone EIA detecting 11,17 dioxoandrostanes was the most suitable EIA for quantifying GCMs in the feces of both sexes. There were sex-related differences in response to the high- and low-dose ACTH challenge. We recommend using feces as a more suitable matrix for non-invasive GCM monitoring for NMRs which can be valuable when investigating housing conditions and other welfare aspects.

Together or alone? Huddling energetic savings in three social mole-rat species of genus Fukomys. A dispersal perspective.

African mole-rats (Bathyergidae) are strictly subterranean rodents distributed in sub-Saharan Africa. Although the soil layer provides a temperature buffer, the temperature in their burrows is usually below their thermoneutral zone and thermogenesis is necessary to maintain a stable body temperature. In social bathyergids, an important mechanism for decreasing the thermoregulatory cost is social thermoregulation in the form of huddling. The effect of huddling may be of special importance during forming of a new family as only two adults are present and social species are known for higher heat losses from their bodies compared to solitary mole-rats. In our study, we measured the resting metabolic rate and energetic saving in three social bathyergid species which differ in body size. We compared animals that were housed individually and in pairs at two different ambient temperatures (Ta). At a temperature within their TNZ (Ta = 30 °C), no energetic savings were expected, whereas in Ta = 20 °C we expected energetic savings due to huddling. We found no energetic savings at 30 °C in any of the species, but almost 20% in the two small bodied Fukomys species F. micklemi and F. anselli at 20 °C. In the largest species, F. mechowii, no significant energetic savings were observed. Our results confirm the importance of huddling for the energetic balance of social mole-rats and show that huddling with one partner can bring substantial energetic savings, which can be allocated to other activities such as extension of established burrow systems or reproduction to increase the workforce and fulfill the purpose of dispersal.

Aggression, Boldness, and Exploration Personality Traits in the Subterranean Naked Mole-Rat (Heterocephalus glaber) Disperser Morphs.

Animal personality traits (consistent behavioral differences between individuals in their behavior across time and/or situation) affect individual fitness through facets, such as dispersal. In eusocial naked mole-rat (Heterocephalus glaber) colonies, a disperser morph may arise with distinct morphological, behavioral, and physiological characteristics. This study aimed to quantify the personality traits of a cohort of disperser morphs of naked mole-rat (NMR). Behavioral tests were performed on twelve disperser morphs (six males and six females) in an observation tunnel system that was novel and unfamiliar. Novel stimuli (fresh snakeskin, tissue paper, and conspecific of the same sex) were introduced for fifteen minutes, and the behavioral acts of the individual were recorded. A total of 30 behaviors were noted during the behavioral tests of which eight were used to quantify aggression, boldness, and exploration. The NMR disperser morphs showed consistent individual differences in boldness, and exploration across time and test, indicating a distinct personality. In addition, new naked mole-rat responses including disturbance behaviors; confront, barricade, and stay-away, were recorded. Further investigations into the relationships between animal personality traits and social hierarchy position in entire colonies are needed for more informative results as we further investigate the role of personality in cooperatively breeding societies.

The Somatosensory World of the African Naked Mole-Rat.

The naked mole-rat (Heterocephalus glaber) is famous for its longevity and unusual physiology. This eusocial species that lives in highly ordered and hierarchical colonies with a single breeding queen, also discovered secrets enabling somewhat pain-free living around 20 million years ago. Unlike most mammals, naked mole-rats do not feel the burn of chili pepper's active ingredient, capsaicin, nor the sting of acid. Indeed, by accumulating mutations in genes encoding proteins that are only now being exploited as targets for new pain therapies (the nerve growth factor receptor TrkA and voltage-gated sodium channel, NaV1.7), this species mastered the art of analgesia before humans evolved. Recently, we have identified pain-insensitivity as a trait shared by several closely related African mole-rat species. In this chapter we will show how African mole-rats have evolved pain insensitivity as well as discussing what the proximate factors may have been that led to the evolution of pain-free traits.

Patterns of telomere length with age in African mole-rats: New insights from quantitative fluorescence in situ hybridisation (qFISH).

Naked mole-rats Heterocephalus glaber (NMRs) are the longest-lived rodent and also resist the normal signs of senescence. In a number of species, cellular ageing has been correlated with a reduction in telomere length, yet relatively little is known about telomeres and their age-related dynamics in NMRs and other African mole-rats. Here, we apply fluorescence in situ hybridisation (FISH) to quantify telomeric repeat sequences in the NMR, the Damaraland mole-rat, Fukomys damarensis (DMR) and the Mahali mole-rat, Cryptomys hottentotus mahali (MMR). Both terminal and non-terminal telomeric sequences were identified in chromosomes of the NMR and DMR, whilst the MMR displayed only terminal telomeric repeats. Measurements of tooth wear and eruption patterns in wild caught DMRs and MMRs, and known ages in captive bred NMRs, were used to place individuals into relative age classes and compared with a quantitative measure of telomeric fluorescence (as a proxy for telomere size). While NMRs and MMRs failed to show an age-related decline in telomeric fluorescence, the DMR had a significant decrease in fluorescence with age, suggesting a decrease in telomere size in older animals. Our results suggest that among African mole-rats there is variation between species with respect to the role of telomere shortening in ageing, and the replicative theory of cellular senescence.

Independent evolution of pain insensitivity in African mole-rats: origins and mechanisms.

The naked mole-rat (Heterocephalus glaber) is famous for its longevity and unusual physiology. This eusocial species that lives in highly ordered and hierarchical colonies with a single breeding queen, also discovered secrets enabling somewhat pain-free living around 20 million years ago. Unlike most mammals, naked mole-rats do not feel the burn of chili pepper's active ingredient, capsaicin, nor the sting of acid. Indeed, by accumulating mutations in genes encoding proteins that are only now being exploited as targets for new pain therapies (the nerve growth factor receptor TrkA and voltage-gated sodium channel, NaV1.7), this species mastered the art of analgesia before humans evolved. Recently, we have identified pain insensitivity as a trait shared by several closely related African mole-rat species. One of these African mole-rats, the Highveld mole-rat (Cryptomys hottentotus pretoriae), is uniquely completely impervious and pain free when confronted with electrophilic compounds that activate the TRPA1 ion channel. The Highveld mole-rat has evolved a biophysical mechanism to shut down the activation of sensory neurons that drive pain. In this review, we will show how mole-rats have evolved pain insensitivity as well as discussing what the proximate factors may have been that led to the evolution of pain-free traits.

Hind foot drumming: Morphofunctional analysis of the hind limb osteology in three species of African mole-rats (Bathyergidae).

Hind foot drumming is a form of seismic signaling that plays a vital role in the communication of several Bathyergidae species. Hind foot drumming is initiated by the rapid movement of the whole hind limb by flexion and extension of the hip and knee. This study aimed to determine if morphological adaptations of the hind limb osteology were measurable using established morphometric analyses in two drumming (Bathyergus suillus and Georychus capensis) and one non-drumming (Cryptomys hottentotus natalensis) African mole-rat species. Forty-three linear measurements of the hind limb were taken in 48 limbs (n = 16 limbs per species) and 32 indices were calculated. Mixed model analysis of variance was used to compare the three species and sexes within a species. Thirteen indices had significant differences between species. Eleven indices had significant differences between sexes within a species. Significant differences between the drumming (B. suillus and G. capensis) and the non-drumming species were observed in three indices. The femoral greater trochanter was relatively shorter in the drumming species compared to the non-drumming species, which is proposed to allow for increased hip joint mobility, thereby permitting drummers to move their limbs at the rapid speed required to generate seismic signals. Furthermore, the small in-lever (shorter greater trochanter) may increase the velocity of limb motion. The robust tibias in the drumming species, as indicated by the tibial robustness index, are likely to counter the additional biomechanical load caused by the muscles involved in hind foot drumming. The relatively small hind feet seen in the drumming species allows for reduced limb weight needed for the rapid extension and flexion motion required during hind foot drumming. The significant differences reflected in the hind limb osteological indices between B. suillus and G. capensis and the non-drumming species are indicative of adaptations for hind foot drumming.

Surveys and Literature Review of Parasites among African Mole-Rats: Proposing Hypotheses for the Roles of Geography, Ecology, and Host Phylogenetic Relatedness in Parasite Sharing.

Hosts that overlap geographically, are less phylogenetically divergent, and/or share similar ecological conditions (e.g., climate, habitat type) are also likely to share parasites. Here we assessed the ectoparasite communities sustained by 3 solitary species of Bathyergidae (Georychus capensis, Bathyergus suillus, and Bathyergus janetta) as well as the endoparasites exploiting G. capensis and compared them with those reported in the literature for other sympatric and parapatric African mole-rat species. In addition to 1 nematode ( Trichuris sp.) and 1 symbiotic ciliate (Meistoma georychi), we collected mites of the genera Androlaelaps and Bathyergolichus as well as unidentified trombiculids from these hosts. Host specificity was high at either the species, genus, or family level for Androlaelaps spp. and Bathyergolichus spp. irrespective of geographic proximity, host phylogeny, or ecological conditions. Host sharing was more limited for helminths but observed among sympatric host species. Our results suggest that ecological similarity and geographic proximity may be more important determinants of host sharing than phylogeny within Bathyergidae.

Phylogeny and biogeography of the African Bathyergidae: a review of patterns and processes.

BACKGROUND: We review genealogical relationships, biogeographic patterns and broad historical drivers of speciation within the Bathyergidae, a group of endemic African rodents, as well as identify key taxa which need further research. METHODS: We sourced comparable cytochrome b sequence data (comparable data available for all members for the Family) and geographic information for all six genera of the African subterranean rodent. This information was combined into the most comprehensive and geographically representative evolutionary study for the Bathyergidae to date. RESULTS: Species richness within the Bathyergidae appears to be underestimated, with undescribed taxa in five of the six genera. Biogeographic patterns suggest large historical distributions, which were repeatedly fragmented by major landscape changes (especially rifting, uplift and drainage evolution) since the Miocene. Aside from vicariant events, other factors (ecological specialization, population-level responses and climatic change) may have been instrumental in driving divergences in the Bathyergidae. As such, adaptive differences may exist among both populations and species across their discrete ranges, driving independent evolutionary trajectories among taxa. In addition, highly fragmented distributions of divergent (and often relict) lineages indicates the possibility of narrow endemics restricted to diminishing suitable habitats. From this, it is clear that a systematic revision of the Bathyergidae is necessary; such a revision should include comprehensive sampling of all putative taxa, the addition of genomic information to assess adaptive differences, as well as ecological information.

Thermal biology of a strictly subterranean mammalian family, the African mole-rats (Bathyergidae, Rodentia) - a review.

African mole-rats are subterranean rodents, which rarely if ever leave the safety of their burrow systems. The environment of the burrows is humid, with relatively stable temperatures, and may have a hypoxic and hypercapnic atmosphere. One of crucial problems related to the subterranean way of life in mammals is avoidance of overheating, because traditional mammalian cooling mechanisms are not effective under high humidity. In African mole-rats, a variety of adaptations have evolved in response to this and other challenges of the underground ecotope. Traditionally, attention has been devoted mainly to the naked mole-rat Heterocephalus glaber, which became popular as a result of its eusociality and absence of fur, both being unique phenomena in small mammals. Despite more recent research, information on other species is still relatively limited and patchy. I review the results of studies on African mole-rats that are relevant for the understanding of their energetics and thermal biology. Attention is paid to the parameters of the burrow environment, which represent the main selection pressures shaping their physiology. In addition, an overview is given of the morphological, physiological and behavioural adaptations helping mole-rats to face temperature extremes, mechanisms by which they deal with a surplus of metabolic heat and how changes in ambient temperature influence their daily activity. The naked mole-rat is compared to its furred relatives to determine whether this species is really exceptional from the point of thermal biology. An ordination analysis was conducted using published data on mole-rat body temperature, thermoneutral zone, resting metabolic rate and thermal conductance. Most of the variability in these characteristics was found to be explained by body mass, followed by temperature characteristics of climate, but not precipitation, of the species distributional ranges. This analysis shows that the naked mole-rat is comparable to the other mole-rat species in these physiological characteristics.

Evidence for contrasting roles for prolactin in eusocial naked mole-rats, Heterocephalus glaber and Damaraland mole-rats, Fukomys damarensis.

Elevated prolactin (PRL) has been associated with the expression of social and cooperative behaviours in a number of vertebrate species, as well as suppression of reproduction. As social mole-rats exhibit both of these traits, PRL is a prime candidate in mediating their social phenotype. While naked and Damaraland mole-rats (NMRs and DMRs) have evolved eusociality independently within their family, both species exhibit an extreme skew in lifetime reproductive success, with breeding restricted to a single female and one or two males. Non-breeding NMRs of both sexes are physiologically inhibited from reproducing, while in DMRs only the non-breeding females are physiologically suppressed. Newly emerging work has implicated the dopamine system and PRL as a component in socially induced reproductive suppression and eusociality in NMR, but the DMR remains unstudied in this context. To investigate evolutionary convergence in the role of PRL in shaping African mole-rat eusociality, we determined plasma PRL concentrations in breeders and non-breeders of both sexes, comparing DMRs with NMRs. Among samples from non-breeding NMRs 80% had detectable plasma PRL concentrations. As a benchmark, these often (37%) exceeding those considered clinically hyperprolactinaemic (25 ng ml-1) in humans: mean ± s.e.m.: 34.81 ± 5.87 ngml-1; range 0.00-330.30 ng ml-1 Conversely, 85% of non-breeding DMR samples had undetectable values and none had concentrations above 25 ng ml-1: 0.71 ± 0.38 ng ml-1; 0.00-23.87 ngml-1 Breeders in both species had the expected variance in plasma PRL concentrations as part of normal reproductive function, with lactating queens having significantly higher values. These results suggest that while elevated PRL in non-breeders is implicated in NMR eusociality, this may not be the case in DMRs, and suggests a lack of evolutionary convergence in the proximate control of the social phenotype in these mole-rats.

From Mice to Mole-Rats: Species-Specific Modulation of Adult Hippocampal Neurogenesis.

Rodent populations living in their natural environments have very diverse ecological and life history profiles that may differ substantially from that of conventional laboratory rodents. Free-living rodents show species-specific neurogenesis that are dependent on their unique biology and ecology. This perspective aims to illustrate the benefit of studying wild rodent species in conjunction with laboratory rodents. African mole-rats are discussed in terms of habitat complexity, social structures, and longevity. African mole-rats are a group of subterranean rodents, endemic to Africa, that show major differences in both intrinsic and extrinsic traits compared to the classical rodent models. Mole-rats exhibit a spectrum of sociality within a single family, ranging from solitary to eusocial. This continuum of sociality provides a platform for comparative testing of hypotheses. Indeed, species differences are apparent both in learning ability and hippocampal neurogenesis. In addition, social mole-rat species display a reproductive division of labor that also results in differential hippocampal neurogenesis, independent of age, offering further scope for comparison. In conclusion, it is evident that neurogenesis studies on conventional laboratory rodents are not necessarily representative, specifically because of a lack of diversity in life histories, uniform habitats, and low genetic variability. The observed level of adult neurogenesis in the dentate gyrus is the result of an intricate balance between many contributing factors, which appear to be specific to distinct groups of animals. The ultimate understanding of the functional and adaptive role of adult neurogenesis will involve research on both laboratory animals and natural rodent populations.

Relic populations of Fukomys mole-rats in Tanzania: description of two new species F. livingstoni sp. nov. and F. hanangensis sp. nov.

Previous studies of African mole-rats of the genera Heliophobius and Fukomys (Bathyergidae) in the regions of East and south central Africa have revealed a diversity of species and vicariant populations, with patterns of distribution having been influenced by the geological process of rifting and changing patterns of drainage of major river systems. This has resulted in most of the extant members of the genus Fukomys being distributed west of the main Rift Valley. However, a small number of isolated populations are known to occur east of the African Rift Valley in Tanzania, where Heliophobius is the most common bathyergid rodent. We conducted morphological, craniometric and phylogenetic analysis of mitochondrial cytochrome b (cyt b) sequences of two allopatric populations of Tanzanian mole-rats (genus Fukomys) at Ujiji and around Mount Hanang, in comparison with both geographically adjacent and more distant populations of Fukomys. Our results reveal two distinct evolutionary lineages, forming clades that constitute previously unnamed species. Here, we formally describe and designate these new species F. livingstoni and F. hanangensis respectively. Molecular clock-based estimates of divergence times, together with maximum likelihood inference of biogeographic range evolution, offers strong support for the hypothesis that vicariance in the Western Rift Valley and the drainage patterns of major river systems has subdivided populations of mole-rats. More recent climatic changes and tectonic activity in the "Mbeya triple junction" and Rungwe volcanic province between Lakes Rukwa and Nyasa have played a role in further isolation of these extra-limital populations of Fukomys in Tanzania.

Temperature preferences of African mole-rats (family Bathyergidae).

Many animals are able to detect small temperature differences and show strong temperature preferences during periods of rest and activity. Mammals inhabiting the subterranean ecotope can adapt their digging and foraging activity in shallow tunnels temporarily to periods with favourable ambient air and soil temperatures. Moreover, subterranean mammals have the unique opportunity to select for their nests in soil depths with certain, daily and seasonally constant temperatures. Our knowledge on nest temperatures in several species of subterranean mammals is based on measurements of temperatures in empty nests. We can expect, however, that the temperature in an occupied nest is higher (due to the "igloo effect"). We performed two experiments regarding the temperature preference in five species of African mole-rats (Bathyergidae, Rodentia: Fukomys anselli, F. mechowii, F. micklemi, Heliophobius argenteocinereus, and Heterocephalus glaber). In a first experiment, the animals were tested pairwise (except for the solitary silvery mole-rats, H. argenteocinereus, that were tested singly) in an apparatus consisting of seven chambers with a temperature gradient ranging between 16 and 37°C (air temperature). While the smaller species (<110g; F. anselli, F. micklemi, H. glaber) chose chambers with average air temperatures around 29°C, the larger mole-rats rested preferably at lower temperatures of approximately 25.6°C (F. mechowii) and 27.7°C (H. argenteocinereus). A strong negative correlation between body mass and preferred air temperature was detected across species. Thus, the results comply with the surface-volume-rule. Contrary to expectations, temperature preference of naked mole-rats (H. glaber) did not deviate from those of furred small mole-rats, but followed the general trend with smaller species preferring higher temperatures. In a second experiment, Ansell's mole-rats (F. anselli) were tested in groups of four, six and nine animals and the preferred temperatures were compared to the values obtained for pairs. The preferred mean air temperatures did not differ among the groups of different sizes. We discuss our findings in the light of ecophysiological adaptations to cope with the ambient conditions proposed by the "thermal stress hypothesis". Furthermore, we suggest that while soil temperature is decisive during digging as the mole-rats warm up or cool due to tight contact between body and soil (conduction), resting animals prevent heat loss through conduction by building a nest.