Fossorial adaptations in African mole-rats (Bathyergidae) and the unique appendicular phenotype of naked mole-rats.

Life underground has constrained the evolution of subterranean mammals to maximize digging performance. However, the mechanisms modulating morphological change and development of fossorial adaptations in such taxa are still poorly known. We assessed the morpho-functional diversity and early postnatal development of fossorial adaptations (bone superstructures) in the appendicular system of the African mole-rats (Bathyergidae), a highly specialized subterranean rodent family. Although bathyergids can use claws or incisors for digging, all genera presented highly specialized bone superstructures associated with scratch-digging behavior. Surprisingly, Heterocephalus glaber differed substantially from other bathyergids, and from fossorial mammals by possessing a less specialized humerus, tibia and fibula. Our data suggest strong functional and developmental constraints driving the selection of limb specializations in most bathyergids, but more relaxed pressures acting on the limbs of H. glaber. A combination of historical, developmental and ecological factors in Heterocephalus are hypothesized to have played important roles in shaping its appendicular phenotype.

The naked truth: a comprehensive clarification and classification of current 'myths' in naked mole-rat biology.

The naked mole-rat (Heterocephalus glaber) has fascinated zoologists for at least half a century. It has also generated considerable biomedical interest not only because of its extraordinary longevity, but also because of unusual protective features (e.g. its tolerance of variable oxygen availability), which may be pertinent to several human disease states, including ischemia/reperfusion injury and neurodegeneration. A recent article entitled 'Surprisingly long survival of premature conclusions about naked mole-rat biology' described 28 'myths' which, those authors claimed, are a 'perpetuation of beautiful, but falsified, hypotheses' and impede our understanding of this enigmatic mammal. Here, we re-examine each of these 'myths' based on evidence published in the scientific literature. Following Braude et al., we argue that these 'myths' fall into four main categories: (i) 'myths' that would be better described as oversimplifications, some of which persist solely in the popular press; (ii) 'myths' that are based on incomplete understanding, where more evidence is clearly needed; (iii) 'myths' where the accumulation of evidence over the years has led to a revision in interpretation, but where there is no significant disagreement among scientists currently working in the field; (iv) 'myths' where there is a genuine difference in opinion among active researchers, based on alternative interpretations of the available evidence. The term 'myth' is particularly inappropriate when applied to competing, evidence-based hypotheses, which form part of the normal evolution of scientific knowledge. Here, we provide a comprehensive critical review of naked mole-rat biology and attempt to clarify some of these misconceptions.

Growth affects dispersal success in social mole-rats, but not the duration of philopatry.

In naked mole-rats (Heterocephalus glaber), some non-breeding males show faster growth and are more likely to disperse than others. These differences have been suggested to be the result of a specialized developmental strategy leading to shorter philopatry and independent breeding, as opposed to extended philopatry as non-reproductive helpers. However, it is unclear whether fast-growing males disperse sooner than slow-growing males. An alternative explanation is that variation in quality between individuals causes high-quality individuals to grow quickly and maximize dispersal success without reducing philopatry. Here we show that in Damaraland mole-rats (Fukomys damarensis), males that subsequently disperse successfully grow faster than other non-reproductive males. This pattern is predicted by both hypotheses and does not discriminate between them. However, contrary to the suggestion that faster growth represents a developmental specialization for early dispersal, fast-growing and slow-growing males remained equally long in their natal groups. Our study provides no evidence for adaptive divergence in male development leading either to early dispersal or extended philopatry. Instead of representing specialized dispersers, fast-growing males of this species may be high-quality individuals.

Subterranean Mammals: Reservoirs of Infection or Overlooked Sentinels of Anthropogenic Environmental Soiling?

Global reports of emergent pathogens in humans have intensified efforts to identify wildlife reservoirs. Subterranean mammals, such as bathyergid mole rats, are largely overlooked, despite their high-level exposure to soil-dwelling microbes. Initial assessment of bathyergid reservoir potential was determined using a broad-range 16S rRNA PCR approach, which revealed an 83% PCR-positivity for the 234 bathyergid lung samples evaluated. The presence of the Bacillus cereus complex, a ubiquitous bacterial assemblage, containing pathogenic and zoonotic species, was confirmed through nucleotide sequencing, prior to group- and species-specific PCR sequencing. The latter allowed for enhanced placement and prevalence estimations of Bacillus in four bathyergid species sampled across a range of transformed landscapes in the Western Cape Province, South Africa. Two novel Bacillus strains (1 and 2) identified on the basis of the concatenated 16S rRNA-groEL-yeaC data set (2066 nucleotides in length), clustered with B. mycoides (ATCC 6462) and B. weihenstephanensis (WSBC 10204), within a well-supported monophyletic lineage. The levels of co-infection, evaluated with a groEL strain-specific assay, developed specifically for this purpose, were high (71%). The overall Bacillus presence of 17.95% (ranging from 0% for Georychus capensis to 45.35% for Bathyergus suillus) differed significantly between host species (χ2 = 69.643; df = 3; P < 0.05), being significantly higher in bathyergids sampled near an urban informal settlement (χ2 = 70.245; df = 3; P < 0.05). The results highlight the sentinel potential of soil-dwelling mammals for monitoring anthropogenically introduced, opportunistic pathogens and the threats they pose to vulnerable communities, particularly in the developing world.

O2 binding and CO2 sensitivity in haemoglobins of subterranean African mole rats.

Inhabiting deep and sealed subterranean burrows, mole rats exhibit a remarkable suite of specializations, including eusociality (living in colonies with single breeding queens), extraordinary longevity, cancer immunity and poikilothermy, and extreme tolerance of hypoxia and hypercapnia. With little information available on adjustments in haemoglobin (Hb) function that may mitigate the impact of exogenous and endogenous constraints on the uptake and internal transport of O2, we measured haematological characteristics, as well as Hb-O2 binding affinity and sensitivity to pH (Bohr effect), CO2, temperature and 2,3-diphosphoglycerate (DPG, the major allosteric modulator of Hb-O2 affinity in red blood cells) in four social and two solitary species of African mole rats (family Bathyergidae) originating from different biomes and soil types across Central and Southern Africa. We found no consistent patterns in haematocrit (Hct) and blood and red cell DPG and Hb concentrations or in intrinsic Hb-O2 affinity and its sensitivity to pH and DPG that correlate with burrowing, sociality and soil type. However, the results reveal low specific (pH independent) effects of CO2 on Hb-O2 affinity compared with humans that predictably safeguard pulmonary loading under hypoxic and hypercapnic burrow conditions. The O2 binding characteristics are discussed in relation to available information on the primary structure of Hbs from adult and developmental stages of mammals subjected to hypoxia and hypercapnia and the molecular mechanisms underlying functional variation in rodent Hbs.

Workforce Effects and the Evolution of Complex Sociality in Wild Damaraland Mole Rats.

Explaining the evolution of eusocial and cooperatively breeding societies demands that we understand the effects of workforce size on the reproductive success of breeders. This challenge has yet to be addressed in the family that arguably exhibits the most extreme outcomes of vertebrate social evolution, the African mole rats (Bathyergidae), leaving the ultimate causes of their many unusual adaptations open to debate. Here we report-using a 14-year field study of wild Damaraland mole rats, Fukomys damarensis-that workers appear to have strong but unusual effects on offspring. Groups with larger workforces exhibited substantially higher rates of offspring recruitment while maintaining high juvenile survival rates, relationships that may have favored the evolution of the delayed dispersal, cooperation, morphological specialization, and unusual patterns of longevity that characterize such societies. Offspring reared by larger workforces also showed slower growth, however. That reduced offspring growth in larger groups has also been documented under ad lib. food conditions in the laboratory raises the possibility that this reflects socially induced growth restraint rather than simple constraints on resource availability. Our findings shed new light on the evolution of complex sociality in this enigmatic clade and highlight further departures from the norms reported for other cooperative vertebrates.

Neuroanatomical investigation of the gonadotrophin-releasing hormone 1 system in the seasonally breeding Cape dune mole-rat, Bathyergus suillus.

The gonadotrophin-releasing hormone 1 (GnRH1) system has been investigated immunohistochemically in Cape dune mole-rats (Bathyergus suillus), subterranean rodents that normally display severe aggression towards conspecifics. These animals breed seasonally and show a reduced mean plasma level of luteinising hormone during the non-breeding season. GnRH1-immunoreactive (ir) cell bodies and processes are found in the septal/preoptic area and the mediobasal hypothalamus; the cell bodies are found in equal measure in these two regions. Dense aggregations of GnRH1-ir fibres are present in the organum vasculosum of the lamina terminalis and the external zone of the median eminence. The total number of detectable GnRH1-ir cell bodies does not differ between the sexes or within the sexes between breeding and non-breeding seasons. Similarly there is no difference in the distribution of detectable GnRH1-ir cell bodies in male and female mole-rats in and out of the breeding season. Although the average size of GnRH1-ir cell bodies does not differ between the seasons in males, their size in females is significantly smaller in the non-breeding season. Whether this reduced size reflects reduced GnRH1 synthesis remains to be determined.

Social common mole-rats enhance outbreeding via extra-pair mating.

Females in many species engage in matings with males that are not their social mates. These matings are predicted to increase offspring heterozygosity and fitness, and thereby prevent the deleterious effects of inbreeding. We tested this hypothesis in a cooperative breeding mammal, the common mole-rat Cryptomys hottentotus hottentotus. Laboratory-based studies suggested a system of strict social monogamy, while recent molecular studies indicate extensive extra-pair paternity despite colonies being founded by an outbred pair. Our data show that extra-pair and within-colony breeding males differed significantly in relatedness to breeding females, suggesting that females may gain genetic benefits from breeding with non-resident males. Extra-colony male mating success was not based on heterozygosity criteria at microsatellite loci; however, litters sired by extra-colony males exhibited increased heterozygosity. While we do not have the data that refute a relationship between individual levels of inbreeding (Hs) and fitness, we propose that a combination of both male and female factors most likely explain the adaptive significance of extra-pair mating whereby common mole-rats maximize offspring fitness by detecting genetic compatibility with extra-pair mates at other key loci, but it is not known which sex controls these matings.

The pituitary potential for opportunistic breeding in the Cape dune mole-rat, Bathyergus suillus.

In this paper we investigated the effect of sex and season on baseline and post-GnRH challenge luteinising hormone (LH) levels in a solitary, seasonally breeding mole-rat. Circulating basal concentrations of luteinising hormone (LH) were found to differ significantly with season in both sexes. However, no significant difference was found in circulating basal LH concentration between the sexes either within or out of the breeding season. The magnitude of the LH response to an exogenous pharmacological overdose of GnRH both in and out of the breeding season in males and females respectively was not significant. This finding suggests that there is no down regulation of GnRH receptors on the pituitary during the non-breeding season. Cape dune mole-rats thus have the potential for opportunistic breeding outside of the typical breeding period. We argue that this represents an adaptation to limited and brief opportunities for mating in this xenophobic and aggressive species.

Preliminary evidence for the use of microseismic cues for navigation by the Namib golden mole.

Insect prey of the Namib golden mole congregate beneath clumps of grass scattered among the sand dunes of the Namib Desert. In the presence of the light winds that typically blow over the Namib Desert, these grass clumps emit low-amplitude vibrations that are transmitted through the sand. While foraging in the sand-swimming mode (a few centimeters below the surface of the sand), some moles apparently were attracted toward manmade sources emitting vibrations matching those recorded from the grass clumps. This is the first direct evidence that these desert mammals use seismic cues for navigation.

Colony structure and parentage in wild colonies of co-operatively breeding Damaraland mole-rats suggest incest avoidance alone may not maintain reproductive skew.

Colonies of co-operatively breeding African mole-rats have traditionally been thought to be composed of a single breeding female, one or two breeding males, and their offspring. In the naked mole-rat (Heterocephalus glaber), the occurrence of facultative inbreeding means incest avoidance cannot prevent reproduction in subordinate group members, and physiological suppression of reproductive function by the breeding female occurs in both sexes. In contrast, previous studies of captive colonies of the Damaraland mole-rat (Cryptomys damarensis) suggest that breeding within a colony is restricted to a single breeding pair, simply because all other colony members are highly related (first- or second-order relatives) and this species is an obligate outbreeder. Using microsatellite markers, we investigated parentage and colony composition in 18 wild Damaraland mole-rat colonies to determine whether inbreeding avoidance alone can explain the high levels of reproductive skew in this species. Multiple and unidentified paternity was widespread within colonies and immigrants of both sexes were regularly identified. Unrelated, opposite-sex nonbreeders were found coexisting in two colonies. These results suggest that, in the wild, conditions exist where nonreproductive females can come into contact with unrelated males, even when they do not disperse from their natal colony. Inbreeding avoidance alone is therefore insufficient to maintain the high levels of reproductive skew identified in this species suggesting that the breeding female somehow suppresses the reproductive function in nonbreeding females.

Prolonged longevity in naked mole-rats: age-related changes in metabolism, body composition and gastrointestinal function.

Aging is characterized by declines in all physiological processes and concomitant changes in body composition. Age-related changes in metabolism, body composition and gastrointestinal function were investigated in naked mole-rats (Heterocephalus glaber), rodents that exhibit extended longevity. Maximum lifespan of these 40 g rodents (>27 year) is approximately 9 times greater than predicted allometrically. We investigated changes in basal metabolic rate (BMR), body composition and intestinal glucose transport in 1, 5, 10 and 20-year-old male individuals. Body composition was measured using dual X-ray absorptiometry and activity of sodium glucose co-transporters (SGLT1) determined using everted gut sleeves. One-year-olds had lower body mass than other age cohorts, as they had not attained full adult form. Among the 5, 10, and 20-year-olds, no age-related changes in body mass, BMR, percentage body fat, fat-free mass or bone mineral density were found. SGLT1 activity declined moderately (<20%) from 5 to 20 years and was similar at 10-20 years, whereas age-related declines are 40-60% in mice. Although mole-rats have low metabolic rates, their prolonged longevity results in a lifetime energy expenditure more than 4 times that of mice. Since lifetime energy expenditure is an important index of potential exposure to oxidative damage, naked mole-rats may be valuable for studying mechanisms of aging.

Eusociality in African mole-rats: new insights from patterns of genetic relatedness in the Damaraland mole-rat (Cryptomys damarensis).

After the discovery of eusociality in the naked mole-rat, it was proposed that inbreeding and high colony relatedness in this species were the major underlying factors driving cooperative breeding in African molerats. By contrast, field and laboratory studies of the eusocial Damaraland mole-rat (Cryptomys damarensis) have raised the possibility that this species is an obligate outbreeder, although the build-up of inbreeding over several generations could still occur. Using microsatellite markers, we show that most breeding pairs in wild colonies of the Damaraland mole-rat are indeed unrelated (R = 0.02 +/- 0.04) and that mean colony relatedness (R = 0.46 +/- 0.01), determined across 15 colonies from three separate populations, is little more than half that previously identified in naked mole-rats. This finding demonstrates that normal familial levels of relatedness are sufficient for the occurrence of eusociality in mammals. Variation in the mean colony relatedness among populations provides support both for the central role played by ecological constraints in cooperative breeding and for the suggestion that inbreeding in naked mole-rats is a response to extreme constraints on dispersal. Approaches that determine the relative importance of an array of extrinsic factors in driving social evolution in African mole-rats are now required.

The naked mole rat--a new record for the oldest living rodent.

We report a new record for the world's longest-lived rodent, a male naked mole rat (Heterocephalus glaber). On the basis of his weight at capture, this animal was approximately 1 year old when collected near Mtito Andei, Kenya in July/August 1974. He died in April 2002, indicating that he lived for more than 28 years. As such, his life-span surpassed the previous longevity record for a rodent, which was held by a porcupine (Hystrix brachyura) that lived for 27 years and 4 months.

A comparison of the ecology of two populations of the common mole-rat, Cryptomys hottentotus hottentotus: the effect of aridity on food, foraging and body mass.

The aridity food distribution hypothesis (AFDH) maintains that ecological constraints in arid habitats curtail dispersal and promote the evolution of cooperative foraging social groups within the African mole-rats. To evaluate the validity of the AFDH, we investigated inter-habitat differences in food resource characteristics, foraging behaviour, colony size and individual body mass in two common mole-rat populations, one from a mesic and one from an arid habitat. Although food was clumped at both localities, the geophyte density was lower at the arid site. However, geophytes from the arid site were larger than those from the mesic region, and this is suggested to compensate for the reduced geophyte density, enabling colonies to meet their energy requirements. Differences in food resource characteristics in turn influenced the pattern of foraging, the burrow systems at the arid site being longer and more linear than those from the mesic site. Mean colony size did not differ between the two sites, but animals from the arid site exhibited a reduced individual mass relative to those from the mesic area, probably an adaptation to reduce total colony energy expenditure given the elevated foraging costs in arid environments. The common mole-rat from the arid localities should occur in larger colonies than their mesic counterparts. The results from this investigation do not support this contention.

Food availability and foraging by wild colonies of Damaraland mole-rats (Cryptomys damarensis): implications for sociality.

We investigated some of the ecological determinants of sociality in the Damaraland mole-rat, including the spatial distribution and biomass of resources (geophytes) available to foraging Damaraland mole-rats in partly vegetated sand dunes in the Kalahari and in grasslands near Dordabis, Namibia, and the foraging behaviour and residency characteristics of colonies at Dordabis. In both study areas, the geophytes had a clumped distribution, but the highest coefficients of dispersion and mean biomass occurred in the Kalahari where the principal food was the gemsbok cucumber. However, because the coefficient of digestibility was lower in geophytes from the Kalahari than from Dordabis, and the mole-rats only ate about half of a gemsbok cucumber, there was less energy available to mole-rats in the Kalahari. At Dordabis, large established colonies occur in the areas with the richest resources and remain resident in the same area for many years; within this area they search (blindly) for food during brief periods when the soil, at burrow depth, is moist and easily worked. Initially, long straight burrows are dug and few bulbs are taken; once the soil dries, minor changes are made to the burrow system as the mole-rats exploit the food patches they located immediately after the rain. Our results show that the characteristics of the resources, and the short time interval during which location of new resources is possible, favour group living; however, the constraints imposed by these features affect large and small colonies in different ways. Small colonies are more likely to fail than large ones and some crucial factors in the survival of these newly formed colonies are the richness of the area in which their burrows are located, and the size of the colony work force available to locate the food.