Surprisingly long survival of premature conclusions about naked mole-rat biology

Naked mole-rats express many unusual traits for such a small rodent. Their morphology, social behaviour, physiology, and ageing have been well studied over the past half-century. Many early findings and speculations about this subterranean species persist in the literature, although some have been repeatedly questioned or refuted. While the popularity of this species as a natural-history curiosity, and oversimplified story-telling in science journalism, might have fuelled the perpetuation of such misconceptions, an accurate understanding of their biology is especially important for this new biomedical model organism. We review 28 of these persistent myths about naked mole-rat sensory abilities, ecophysiology, social behaviour, development and ageing, and where possible we explain how these misunderstandings came about.     

Poikilothermic traits and thermoregulation in the Afrotropical social subterranean Mashona mole-rat (Cryptomys hottentotus darlingi) (Rodentia: Bathyergidae)

When acclaimated for two months at 26 C the social Mashona mole-rat Cryptomys hottentotus darlingi (±S.D.) resting metabolic rate (RMR) of 0·98±0.·14cm²O₂g _-1 h_-1 ( n =21), within a thermal neutral zone (TNZ) of 28 31·5 C ambient temperature (Ta). The body temperature (Tb) of the mole-rat is very low. 33·3±0·5 C, and remained stable between 25 31·5 C ( n =28). Above 33 C. Tb increased to a mean of 34·±0· C (n=28) (Ta range 33 39 C). Below Ta 25 C. Tb showed strong poikilothermic tendencies, with Tb dropping to a mean of 26·8±1·16 C. whereas above Ta25 C. Tb varied in a typically endothermic pattern. The conductance is high 0·19±0·03 cm² O_2g¹ C ¹ (n=28) at the lower limit of thermoneutrality. The mean RMR at 18 C (the lowest Ta tested) was 2·63 ± 0·55 cm³ O₂g ¹ h ¹ (n=7) which is 2·6 times that of the resting metabolic rate in the TNZ.     

The social structure and dominance hierarchy of the Mashona mole-rat, Cryptomys darlingi (Rodentia: Bathyergidae) from Zimbabwe

Cryptomys darlingi is a social subterranean rodent mole which inhabits the mesic regions of south-eastern and central Africa. Mashona mole-rats live in small colonies (5-9 animals) in which reproduction is normally restricted to the largest male and female in the colony. The non-reproductive members in a mature colony cannot be placed into clearly defined work-related groups based on body mass.
The dominance hierarchy of a young colony was found to be linear, with a value of 1.00 calculated from Landau's linearity index, while that of a mature colony of nine mole-rats was almost linear (0.77). Dominance was found to be related to gender in the mature colony, with males more dominant than females, and to age in the young colony. The reproductive mole-rats are the dominant animals within their respective genders. Dominance appears to correlate positively with body mass (rs = 0.77 in the mature colony and rs = 0.93 in the young colony).
Popularity studies show that smaller animals and females tend to be more popular than the larger massed individuals or males. In the mature colony which contained predominantly adult animals, the reproductive pair was among the least popular. While in the young colony, composed predominantly of sub-adult and juvenile animals, the reproductive pair was the most popular.
Social organization within Mashona mole-rat colonies is compared with other southern African Cryptomys species.     

Causes and consequences of incest avoidance in the cooperatively breeding mole-rat, Cryptomys darlingi (Bathyergidae)

A number of social mole-rat species maintain a strong reproductive skew (only one breeding pair in the group) solely through incest avoidance. Incest avoidance probably evolved for one of two reasons, namely for actually maintaining a reproductive skew or, alternatively, to avoid high inbreeding depression. In the latter case a strong reproductive skew would result as a fortuitous by-product of the combination of a cloistral family life style of mole-rats and incest avoidance. We undertook breeding experiments in which the fertility of pairs of unrelated individuals were compared with that of pairs of double first cousins. Inbreeding depression was remarkably high and an accompanying model suggests that it may be sufficient to support the idea that strong incest avoidance evolved primarily to eliminate the costs of inbreeding and subsequently facilitated the evolution of reproductive skew.     

Ovarian growth and folliculogenesis in breeding and nonbreeding females of a social rodent,the Zambian common mole-rat,Cryptomys sp.

Zambian common mole-rats are subterranean rodents that live in families with only one female breeding. Her offspring remain in the parental nest and do not reproduce. Behavioral experiments (Burda, '95) demonstrated that their apparent “sterility” is based on incest avoidance and individual recognition of family members. To elucidate whether some kind of morphologically apparent ovarian suppression still takes place in daughters, ovaries of females of known age, weight, and reproductive histories were examined histologically and morphometrically. The body mass of old females (more than 3 years of age) begins to decrease, and the ovaries seem to begin to atrophy at the age of about 3–6 years. Ovaries in neonates exhibited primordial and primary follicles, sometimes clustered in nests. Ovaries of adult nonbreeding females expressed all stages of the follicular development up to tertiary follicles. Many unruptured luteinized follicles were present, but true corpora lutea as a morphological sign of ovulation were missing. Unruptured luteinized follicles also could be found (additionally to true corpora lutea) in ovaries of breeding females. The number of primordial follicles dropped rapidly during the first 2 years of age; the number of primary, secondary, and tertiary follicles was subject to individual variation; and there was no clear correlation with age or reproductive status. While a tendency to form accessory unruptured luteinized follicles may just reflect taxonomic affinities of bathyergids to hystricomorphs, the otherwise complete folliculogenesis in “sterile” daughters and the presence of unruptured luteinized follicles even in breeding females are further evidence that there is no hormonal suppression of the ovarial cycle. We suggest that ovulation in nonbreeding females is not actively suppressed by the breeding female, but instead that it is not released because the triggering mechanisms, most probably repeated copulation, are missing. J. Morphol. 237:33–41, 1998. © 1998 Wiley-Liss, Inc.     

Evolution of African mole-rat sociality: burrow architecture, rainfall and foraging in colonies of the cooperatively breeding Fukomys mechowii

African mole rats (Bathyergidae) offer an excellent system with which to test theories relating to the evolution and maintenance of sociality in mammals. The aridity food distribution hypothesis (AFDH) suggests that, within the bathyergids, sociality has evolved in response to patterns of rainfall, its effects on food distribution, and the subsequent costs and risks of foraging and dispersal. Here, in the first detailed study of burrow architecture in a social mole-rat species, with data from 32 burrows, we show that in the giant mole-rat Fukomys mechowii burrow fractal dimension increases with colony size and is higher during the rainy season than during the dry season. The mass of food in the burrow increases with fractal dimension and is higher during the rainy season than during the dry season. These results link for the first time colony size, burrow architecture, rainfall and foraging success and provide support for two assumptions of the AFDH, namely that (1) in arid conditions burrowing may be severely constrained by the high costs of digging; and (2) the potential risks of failing to locate food may be mitigated by increases in colony size.     

Foraging in the subterranean social highveld mole-rat (Cryptomys hottentotus pretoriae): an investigation into mass-dependent geophyte use and foraging patterns

The foraging behaviour of captive colonies of the highveld mole-rat Cryptomys hottentotus pretoriae was investigated in an artificial soil-filled burrow system provided with four trays (patches) that varied in geophyte density and mass. An initial trial involving empty trays (only soil) revealed that there was no preference for any specific tray. There were no statistically significant preferences for excavating in any of the patches of different geophyte density. No preferences were evident for excavation in patches containing geophytes of different mass classes. Empty patches seemed to be preferred over patches containing geophytes when combinations of geophyte density/mass were investigated. The duration of handling and the rate of consumption of geophytes were recorded for 23 individuals of two mass classes. Handling time of geophytes was not related to mole-rat sex, but was strongly linked to mole-rat mass class. Handling time of geophytes was related to geophyte mass class. Small geophytes were less profitable to consume. These findings are considered in light of optimal foraging theory and the situation in the field. It was concluded that the mole-rats generally followed the qualitative predictions of optimal foraging theory, although falling short of being energy maximizers.     

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. Received: 6 May 1997 / Accepted: 21 August 1997     

Aspects of the feeding habits and reproductive biology of the Ghana mole-rat Cryptomys zechi (Rodentia, Bathyergidae)

The feeding habits and reproductive biology of the Ghana mole‐rat, Cryptomys zechi (Matchie), were studied in a Guinea savanna woodland in Ghana. Both tunnel contents and stomach content analysis indicated that bulbs and tubers constituted the commonest and most preferred food items, although some animal food materials were also consumed. Five plant species, Urgenia altissima, Manihot utilisima, Curuligo sp., Oxalis corniculata and Archis hypogea, were the most popular plant food source. Breeding occurred during the rainy season (March–August) and was at its peak in July. There is evidence that the species is capable of producing two litters in a year. In a colony, reproduction is restricted to one female and one male. Males reached sexual maturity at a lower body weights (105 g) than females (155 g). Estimated mean litter size was 1.5 (range 1–2), the smallest among the bathergids. Available data on birth weights of three other species of social Cryptomys indicate that C. zechi has the highest birth weight, which is comparable to that of solitary bathyergids.     

Molecular evolution of the hyaluronan synthase 2 gene in mammals: implications for adaptations to the subterranean niche and cancer resistance

The naked mole-rat (NMR) Heterocephalus glaber is a unique and fascinating mammal exhibiting many unusual adaptations to a subterranean lifestyle. The recent discovery of their resistance to cancer and exceptional longevity has opened up new and important avenues of research. Part of this resistance to cancer has been attributed to the fact that NMRs produce a modified form of hyaluronan—a key constituent of the extracellular matrix—that is thought to confer increased elasticity of the skin as an adaptation for living in narrow tunnels. This so-called high molecular mass hyaluronan (HMM-HA) stems from two apparently unique substitutions in the hyaluronan synthase 2 enzyme (HAS2). To test whether other subterranean mammals with similar selection pressures also show molecular adaptation in their HAS2 gene, we sequenced the HAS2 gene for 11 subterranean mammals and closely related species, and combined these with data from 57 other mammals. Comparative screening revealed that one of the two putatively important HAS2 substitutions in the NMR predicted to have a significant effect on hyaluronan synthase function was uniquely shared by all African mole-rats. Interestingly, we also identified multiple other amino acid substitutions in key domains of the HAS2 molecule, although the biological consequences of these for hyaluronan synthesis remain to be determined. Despite these results, we found evidence of strong purifying selection acting on the HAS2 gene across all mammals, and the NMR remains unique in its particular HAS2 sequence. Our results indicate that more work is needed to determine whether the apparent cancer resistance seen in NMR is shared by other members of the African mole-rat clade.     

Phylogeographical patterns of genetic divergence and speciation in African mole-rats (Family: Bathyergidae)

African mole-rats are subterranean Hystricomorph rodents, distributed widely throughout sub-Saharan Africa, and displaying a range of social and reproductive strategies from solitary dwelling to the 'insect-like' sociality of the naked mole-rat, Heterocephalus glaber. Both molecular systematic studies of Rodentia and the fossil record of bathyergids indicate an ancient origin for the family. This study uses an extensive molecular phylogeny and mitochondrial cytochrome b and 12s rRNA molecular clocks to examine in detail the divergence times, and patterns of speciation of the five extant genera in the context of rift valley formation in Africa. Based on a value of 40-48 million years ago (Myr) for the basal divergence of the family (Heterocephalus), we estimate divergence times of 32-40 Myr for Heliophobius, 20-26 Myr for Georychus/Bathyergus and 12-17 Myr for Cryptomys, the most speciose genus. While early divergences may have been independent of rifting, patterns of distribution of later lineages may have been influenced directly by physical barriers imposed by the formation of the Kenya and Western Rift, and indirectly by accompanying climatic and vegetative changes. Rates of chromosomal evolution and speciation appear to vary markedly within the family. In particular, the genus Cryptomys appears to have undergone an extensive radiation and shows the widest geographical distribution. Of the two distinct clades within this genus, one exhibits considerable karyotypic variation while the other does not, despite comparatively high levels of sequence divergence between some taxa. These different patterns of speciation observed both within the family and within the genus Cryptomys may have been a result of environmental changes associated with rifting.