Nucleotide sequence variation in the mitochondrial 12S rRNA gene and the phylogeny of African mole-rats (Rodentia: Bathyergidae).

Mitochondrial DNA (mtDNA) sequence variation was examined in eight taxa of the African rodent family Bathyergidae, as well as in two taxa representative of the Old-World hystricognathid rodent families Petromyidae and Thryonomyidae. A total of 812 bp, constituting domains I-III of the 12S ribosomal rRNA gene, were compared for each taxon. The high levels of intrafamilial mtDNA sequence divergence observed (average 16.8, range 3.5-23.2) support an ancient origin for the five genera, 20-38 Mya. These data do not support the current subfamilial groupings of the Bathyergidae. The eastern African naked mole-rat, Heterocephalus glaber, is the most basal representative of the family, with the silvery mole-rat, Heliophobius, being the next most basal. South African forms [dune, common, and cape mole-rats (Bathyergus, Cryptomys, and Georychus, respectively)] group together. The independent origin of the common mole-rat, relative to the naked mole-rat, suggests that complex social systems evolved in parallel along different bathyergid lineages. The 12S rRNA gene is not evolving at a higher rate within the rodent lineages, relative to that seen for artiodactyls and primates. Bathyergid rodents appear to fall at an extreme end of the spectrum of mammalian variation, with respect to both transition/transversion ratios and divergence, showing much lower transition/transversion ratios than those previously reported for intrafamilial comparisons.     

Social Structure Predicts Genital Morphology in African Mole-Rats

Background

African mole-rats (Bathyergidae, Rodentia) exhibit a wide range of social structures, from solitary to eusocial. We previously found a lack of sex differences in the external genitalia and morphology of the perineal muscles associated with the phallus in the eusocial naked mole-rat. This was quite surprising, as the external genitalia and perineal muscles are sexually dimorphic in all other mammals examined. We hypothesized that the lack of sex differences in naked mole-rats might be related to their unusual social structure.

Methodology/Principal Findings

We compared the genitalia and perineal muscles in three African mole-rat species: the naked mole-rat, the solitary silvery mole-rat, and the Damaraland mole-rat, a species considered to be eusocial, but with less reproductive skew than naked mole-rats. Our findings support a relationship between social structure, mating system, and sexual differentiation. Naked mole-rats lack sex differences in genitalia and perineal morphology, silvery mole-rats exhibit sex differences, and Damaraland mole-rats are intermediate.

Conclusions/Significance

The lack of sex differences in naked mole-rats is not an attribute of all African mole-rats, but appears to have evolved in relation to their unusual social structure and reproductive biology.     

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.     

Ecological constraints drive social evolution in the African mole-rats.

The African mole-rats (family Bathyergidae) are subterranean hystricomorph rodents occurring in a variety of habitats and displaying levels of sociality which range from solitary to eusocial, making them a unique mammalian taxonomic group to test ecological influences on sociality. Here, we use an extensive DNA-based phylogeny and comparative analysis to investigate the relationship between ecology, sociality and evolution within the family. Mitochondrial cytochrome-b and 12s rRNA trees reveal that the solitary species are monophyletic when compared to the social species. The naked mole-rat (Heterocephalus glaber) is ancestral and divergent from the Damaraland mole-rat (Cryptomys damarensis), supporting previous findings that have suggested the multiple evolution of eusociality within the family. The Cryptomys genus is species-rich and contains taxa exhibiting different levels of sociality, which can be divided into two distinct clades. A total of seven independent comparisons were generated within the phylogeny, and three ecological variables were significantly correlated with social group size: geophyte density (p < 0.05), mean months per year of rainfall greater than 25 mm (p < 0.001), and the coefficient of rainfall variation (p = 0.001). These results support the food-aridity hypothesis for the evolution of highly social cooperative behaviour in the Bathyergidae, and are consistent with the current theoretical framework for skew theory.     

Selective Inflammatory Pain Insensitivity in the African Naked Mole-Rat (Heterocephalus glaber)

In all mammals, tissue inflammation leads to pain and behavioral sensitization to thermal and mechanical stimuli called hyperalgesia. We studied pain mechanisms in the African naked mole-rat, an unusual rodent species that lacks pain-related neuropeptides (e.g., substance P) in cutaneous sensory fibers. Naked mole-rats show a unique and remarkable lack of pain-related behaviors to two potent algogens, acid and capsaicin. Furthermore, when exposed to inflammatory insults or known mediators, naked mole-rats do not display thermal hyperalgesia. In contrast, naked mole-rats do display nocifensive behaviors in the formalin test and show mechanical hyperalgesia after inflammation. Using electrophysiology, we showed that primary afferent nociceptors in naked mole-rats are insensitive to acid stimuli, consistent with the animal's lack of acid-induced behavior. Acid transduction by sensory neurons is observed in birds, amphibians, and fish, which suggests that this tranduction mechanism has been selectively disabled in the naked mole-rat in the course of its evolution. In contrast, nociceptors do respond vigorously to capsaicin, and we also show that sensory neurons express a transient receptor potential vanilloid channel-1 ion channel that is capsaicin sensitive. Nevertheless, the activation of capsaicin-sensitive sensory neurons in naked mole-rats does not produce pain-related behavior. We show that capsaicin-sensitive nociceptors in the naked mole-rat are functionally connected to superficial dorsal horn neurons as in mice. However, the same nociceptors are also functionally connected to deep dorsal horn neurons, a connectivity that is rare in mice. The pain biology of the naked mole-rat is unique among mammals, thus the study of pain mechanisms in this unusual species can provide major insights into what constitutes “normal” mammalian nociception.     

Altered composition of liver proteasome assemblies contributes to enhanced proteasome activity in the exceptionally long-lived naked mole-rat

The longest-lived rodent, the naked mole-rat (Bathyergidae; Heterocephalus glaber), maintains robust health for at least 75% of its 32 year lifespan, suggesting that the decline in genomic integrity or protein homeostasis routinely observed during aging, is either attenuated or delayed in this extraordinarily long-lived species. The ubiquitin proteasome system (UPS) plays an integral role in protein homeostasis by degrading oxidatively-damaged and misfolded proteins. In this study, we examined proteasome activity in naked mole-rats and mice in whole liver lysates as well as three subcellular fractions to probe the mechanisms behind the apparently enhanced effectiveness of UPS. We found that when compared with mouse samples, naked mole-rats had significantly higher chymotrypsin-like (ChT-L) activity and a two-fold increase in trypsin-like (T-L) in both whole lysates as well as cytosolic fractions. Native gel electrophoresis of the whole tissue lysates showed that the 20S proteasome was more active in the longer-lived species and that 26S proteasome was both more active and more populous. Western blot analyses revealed that both 19S subunits and immunoproteasome catalytic subunits are present in greater amounts in the naked mole-rat suggesting that the observed higher specific activity may be due to the greater proportion of immunoproteasomes in livers of healthy young adults. It thus appears that proteasomes in this species are primed for the efficient removal of stress-damaged proteins. Further characterization of the naked mole-rat proteasome and its regulation could lead to important insights on how the cells in these animals handle increased stress and protein damage to maintain a longer health in their tissues and ultimately a longer life.     

Energetics in a solitary subterranean rodent, the silvery mole-rat, Heliophobius argenteocinereus, and allometry of RMR in African mole-rats (Bathyergidae)

Low resting metabolic rate (RMR) in subterranean rodents used to be considered as a physiological adaptation to cope with stresses of the belowground environment. In African mole-rats (Bathyergidae, Rodentia), RMR was reported to be independent of body mass. This deviation from a general mammalian pattern was considered a precondition for evolution of eusociality, occurring in some bathyergids. We measured metabolic rate and thermoregulation in the silvery mole-rat, Heliophobius argenteocinereus, the only bathyergid genus for which well-supported, comparable data were still missing. Low RMR (154.04 mL O(2) h(-1), which is 82% of the value predicted for a rodent) corresponds to the value expected in a subterranean rodent. Broad range of the thermoneutral zone (25-33 degrees C) and only slightly higher conductance (17.3 mL O(2) h(-1) degrees C(-1), i.e. 112.5% of that predicted for subterranean mammals) indicate that H. argenteocinereus is adapted to lower burrow temperatures rather than to high temperatures. Low RMR in this solitary species, as in other subterranean rodents in general, is probably associated particularly with high energetic cost of foraging. Our results combined with data on other mole-rats show clearly that RMR within the Bathyergidae is mass-dependent.     

Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber)

In all mammals, tissue inflammation leads to pain and behavioral sensitization to thermal and mechanical stimuli called hyperalgesia. We studied pain mechanisms in the African naked mole-rat, an unusual rodent species that lacks pain-related neuropeptides (e.g., substance P) in cutaneous sensory fibers. Naked mole-rats show a unique and remarkable lack of pain-related behaviors to two potent algogens, acid and capsaicin. Furthermore, when exposed to inflammatory insults or known mediators, naked mole-rats do not display thermal hyperalgesia. In contrast, naked mole-rats do display nocifensive behaviors in the formalin test and show mechanical hyperalgesia after inflammation. Using electrophysiology, we showed that primary afferent nociceptors in naked mole-rats are insensitive to acid stimuli, consistent with the animal's lack of acid-induced behavior. Acid transduction by sensory neurons is observed in birds, amphibians, and fish, which suggests that this tranduction mechanism has been selectively disabled in the naked mole-rat in the course of its evolution. In contrast, nociceptors do respond vigorously to capsaicin, and we also show that sensory neurons express a transient receptor potential vanilloid channel-1 ion channel that is capsaicin sensitive. Nevertheless, the activation of capsaicin-sensitive sensory neurons in naked mole-rats does not produce pain-related behavior. We show that capsaicin-sensitive nociceptors in the naked mole-rat are functionally connected to superficial dorsal horn neurons as in mice. However, the same nociceptors are also functionally connected to deep dorsal horn neurons, a connectivity that is rare in mice. The pain biology of the naked mole-rat is unique among mammals, thus the study of pain mechanisms in this unusual species can provide major insights into what constitutes “normal” mammalian nociception.     

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.     

Extended longevity of reproductives appears to be common in Fukomys mole-rats (Rodentia, Bathyergidae)

African mole-rats (Bathyergidae, Rodentia) contain several social, cooperatively breeding species with low extrinsic mortality and unusually high longevity. All social bathyergids live in multigenerational families where reproduction is skewed towards a few breeding individuals. Most of their offspring remain as reproductively inactive "helpers" in their natal families, often for several years. This "reproductive subdivision" of mole-rat societies might be of interest for ageing research, as in at least one social bathyergid (Ansell's mole-rats Fukomys anselli), breeders have been shown to age significantly slower than non-breeders. These animals thus provide excellent conditions for studying the epigenetics of senescence by comparing divergent longevities within the same genotypes without the inescapable short-comings of inter-species comparisons. It has been claimed that many if not all social mole-rat species may have evolved similar ageing patterns, too. However, this remains unclear on account of the scarcity of reliable datasets on the subject. We therefore analyzed a 20-year breeding record of Giant mole-rats Fukomys mechowii, another social bathyergid species. We found that breeders indeed lived significantly longer than helpers (ca. 1.5-2.2fold depending on the sex), irrespective of social rank or other potentially confounding factors. Considering the phylogenetic positions of F. mechowii and F. anselli and unpublished data on a third Fukomys-species (F. damarensis) showing essentially the same pattern, it seems probable that the reversal of the classic trade-off between somatic maintenance and sexual reproduction is characteristic of the whole genus and hence of the vast majority of social mole-rats.     

Molecular phylogenetics and taxonomy of the African mole-rats, genus Cryptomys and the new genus Coetomys Gray, 1864

Cryptomys represents the most speciose and widely distributed genus of the Bathyergidae (Mammalia; Rodentia), a family of mole-rats endemic to sub-Saharan Africa. Throughout its range in southern, central, and western Africa, Cryptomys displays diversity in terms of morphology, patterns of behavior, and chromosome number, thus complicating the systematics of the group. A molecular phylogeny was obtained by separate and combined analyses of the mitochondrial 12S rRNA and intron I of the nuclear transthyretin gene for chromosomally and geographically diverse populations of Cryptomys. Our results show that Cryptomys sensu lato is comprised of two distinct and divergent monophyletic clades: hottentotus and mechowi. Based on our analyses, we propose the elevation of the mechowi clade to the genus Coetomys, retaining Cryptomys as the generic epithet of the South African hottentotus clade. This is supported by: (1) reciprocal monophyly of the two lineages based on independent datasets, (2) the level of sequence divergence observed between these lineages relative to other genera (i.e., Bathyergus and Georychus), and (3) different patterns of chromosomal evolution, with Cryptomys sensu stricto being karyotypically conserved (2N=54) and Coetomys exhibiting high karyotypic diversity (2N=40-78).     

The magnetic compass orientation of the burrows of the Damara mole-rat Cryptomys damarensis (Bathyergidae)

In response to reports claiming that part of the ability of mole-rats (Bathyergidae) to orientate with respect to the geomagnetic field involves orientation of their burrow systems in a southward direction, we measured the orientation of burrows of the Damara mole-rat, Cryptomys damarensis , in the Kalahari Desert. It was found that burrow orientation was not significantly different from that expected for a random distribution of compass orientations.     

Different SNP combinations in the GCH1 gene and use of labor analgesia

Recent research has proposed a pathway in which sensory neurons expressing the capsaicin activated ion channel TRPV1 are required for histamine-induced itch and subsequent scratching behavior. We examined histamine-induced itch in the African naked mole-rat (Heterocephalus glaber) and found that although naked mole-rats display innate scratching behavior, histamine was unable to evoke increased scratching as is observed in most mouse strains. Using calcium imaging, we examined the histamine sensitivity of naked mole-rat dorsal root ganglia (DRG) neurons and identified a population of small diameter neurons activated by histamine, the majority of which are also capsaicin-sensitive. This suggested that naked mole-rat sensory neurons are activated by histamine, but that spinal dorsal horn processing of sensory information is not the same as in other rodents. We have previously shown that naked mole-rats naturally lack substance P (SP) in cutaneous C-fibers, but that the neurokinin-1 receptor is expressed in the superficial spinal cord. This led us to investigate if SP deficiency plays a role in the lack of histamine-induced scratching in this species. After intrathecal administration of SP into the spinal cord we observed robust scratching behavior in response to histamine injection. Our data therefore support a model in which TRPV1-expressing sensory neurons are important for histamine-induced itch. In addition, we demonstrate a requirement for active, SP-induced post-synaptic drive to enable histamine sensitive afferents to drive itch-related behavior in the naked mole-rat. These results illustrate that it is altered dorsal horn connectivity of nociceptors that underlies the lack of itch and pain-related behavior in the naked mole-rat.     

Poikilothermic traits in Mashona mole-rat (Fukomys darlingi). Reality or myth?

The African mole-rats (Bathyergidae, Rodentia) is a mammalian family well known for a variety of ecophysiological adaptations for strictly belowground life. The smallest bathyergid, the hairless naked mole-rat from arid areas in Eastern Africa, is even famous as the only truly poikilothermic mammal. Another bathyergid, the Mashona mole-rat (Fukomys darlingi) from Zimbabwe, is supposed to have strong poikilothermic traits, because it is not able to maintain a stable body temperature at ambient temperatures below 20 °C. This is surprising because, compared to the naked mole-rat, this species, together with all congenerics, is larger, haired, and living in more seasonal environment. In addition, other Fukomys mole-rats show typical mammalian pattern in resting metabolic rates. In our study, we measured resting metabolic rate and body temperature of Mashona mole-rats from Malawi across a gradient of ambient temperatures to test its poikilothermic traits. We found that the adult mass specific resting metabolic rate was 0.76±0.20 ml O₂ g⁻¹ h⁻¹ and body temperature 34.8±1.1 °C in the thermoneutral zone (27–34 °C). Body temperature was stable (33.0±0.5 °C) at ambient temperatures from 10 to 25 °C. We thus cannot confirm poikilothermic traits in this species, at least for its Malawian population. Factors potentially explaining the observed discrepancy in Mashona mole-rat energetics are discussed.     

PHOTIC INDUCTION OF Fos IN THE SUPRACHIASMATIC NUCLEUS OF AFRICAN MOLE-RATS: RESPONSES TO INCREASING IRRADIANCE

African mole-rats (family Bathyergidae) are strictly subterranean rodent species that are rarely exposed to environmental light. Morphological and physiological adaptations to the underground environment include a severely reduced eye size and regressed visual system. Responses of the circadian system to light, however, appear to be intact, since mole-rats are able to entrain their circadian activity rhythms to the light-dark cycle and light induces Fos expression in the suprachiasmatic nucleus (SCN). Social organization varies from solitary species to highly elaborated eusocial structures, characterized by a distinct division of labor and in which one reproductive female regulates the behavior and reproductive physiology of other individuals in the colony. The authors studied light-induced Fos expression in the SCN to increasing light intensities in four mole-rat species, ranging from strictly solitary to highly social. In the solitary Cape mole-rat, light induces significant Fos expression in the SCN, and the number of Fos-immunopositive cells increases with increasing light intensity. In contrast, Fos induction in the SCN of social species was slightly greater than, but not statistically different from, the dark-control animals as is typical of most rodents. One species showed a trend for an increase in expression with increased light, whereas a second species showed no trend in expression. In the naked mole-rat, Fos expression appeared higher in the dark-controls than in the animals exposed to light, although the differences in Fos expression were not significant. These results suggest a gradient in the sensitivity of the circadian system to light in mole-rats, with a higher percentage of individuals that are unresponsive to light in correlation with the degree of sociality. In highly social species, such as the naked mole-rat that live in a relatively stable subterranean milieu in terms of food availability, temperature, constant darkness, and devoid of 24-h cyclic environmental cues, the temporal coordination of rest-wake activities may be dependent on social interactions and social status rather than on photic regulation of the circadian timing system. (Author correspondence: moosthuizen@zoology.up.ac.za)     

Resource characteristics and foraging adaptations in the silvery mole-rat (<Emphasis Type="Italic">Heliophobius argenteocinereus</Emphasis>), a solitary Afrotropical bathyergid

The African mole rats (Bathyergidae) is a rodent family unique for subterranean life and diverse social systems. Solitary species are thought to be confined to areas with abundant, evenly distributed food resources and easily workable soils, which favors early natal dispersal and independent reproduction. However, there is a paucity of empirical data confirming this assumption. We examined ecological conditions of a typical natural habitat of the solitary silvery mole-rat (Heliophobius argenteocinereus), which is the Miombo woodland, and we identified behavioral and other adaptations which potentially improve its foraging success. We also tested food selectivity of captive mole-rats. In the Miombo, mole-rat food resources were clumped, but relatively ample. This, along with a predictable and relatively short period of year with dry and difficult-to-work soil, creates relatively moderate ecological conditions. Analysis of food stores showed that food storing alone probably does not secure enough food to overcome the advanced dry season in this species. In light of this, several other adaptations, such as food generalism and area-restricted search can assist silvery mole-rats retaining positive energy balance during these times. Food-preference tests showed that silvery mole-rats prefer tubers with high sugar content, followed by those with high water content.     

Light Perception in Two Strictly Subterranean Rodents: Life in the Dark or Blue?

Background

The African mole-rats (Bathyergidae, Rodentia) are strictly subterranean, congenitally microphthalmic rodents that are hardly ever exposed to environmental light. Because of the lack of an overt behavioural reaction to light, they have long been considered to be blind. However, recent anatomical studies have suggested retention of basic visual capabilities. In this study, we employed behavioural tests to find out if two mole-rat species are able to discriminate between light and dark, if they are able to discriminate colours and, finally, if the presence of light in burrows provokes plugging behaviour, which is assumed to have a primarily anti-predatory function.

Methodology/Principal Finding

We used a binary choice test to show that the silvery mole-rat Heliophobius argenteocinereus and the giant mole-rat Fukomys mechowii exhibit a clear photoavoidance response to full-spectrum (“white”), blue and green-yellow light, but no significant reaction to ultraviolet or red light during nest building. The mole-rats thus retain dark/light discrimination capabilities and a capacity to perceive short to medium-wavelength light in the photopic range of intensities. These findings further suggest that the mole-rat S opsin has its absorption maximum in the violet/blue part of the spectrum. The assay did not yield conclusive evidence regarding colour discrimination. To test the putative role of vision in bathyergid anti-predatory behaviour, we examined the reaction of mole-rats to the incidence of light in an artificial burrow system. The presence of light in the burrow effectively induced plugging of the illuminated tunnel.

Conclusion/Significance

Our findings suggest that the photopic vision is conserved and that low acuity residual vision plays an important role in predator avoidance and tunnel maintenance in the African mole-rats.     

Thermoregulatory differences in African mole-rat species from disparate habitats: Responses and limitations

Individuals and populations possess physiological adaptations to survive local environmental conditions. To occur in different regions where ambient temperature varies, animals must adopt appropriate thermoregulatory mechanisms. Failure to adjust to environmental challenges may result in species distributional range shifts or decreased viability. African mole-rats (Bathyergidae) occupy various habitats in sub-Saharan Africa from deserts to montane regions to mesic coastal areas. We examined thermoregulatory characteristics of three African mole-rat species originating from disparate (montane, savannah, and arid/semi-arid) habitats. Animals were exposed to various ambient temperatures, whilst core body temperature and the surface temperature of different body parts were measured. Oxygen consumption was determined as a measure of heat production. Core body temperatures of Natal (montane) mole-rats (Cryptomys hottentotus natalensis) increased significantly at ambient temperatures >24.5 °C, while those of the highveld (Cryptomys hottentotus pretoriae) (savannah) and Damaraland (Fukomys damarensis) (arid/semi-arid) mole-rats remained within narrower ranges. In terms of surface temperature variation, while pedal surfaces were important in regulating heat loss in Natal and Damaraland mole-rats at high ambient temperatures, the ventral surface was important for heat dissipation in Damaraland and highveld mole-rats. This study provides evidence of the variation and limitations of thermo-physiological mechanisms for three mole-rat species relative to their habitats. Information on physiological adaptations to particular habitats may inform predictive modelling of species movements, declines, and extinctions in response to a changing environment, such as climate change.     

Developmental Plasticity in the Ossification of the Proximal Femur of Heterocephalus glaber (Bathyergidae,Rodentia)

The proximal femoral morphology in rodents of different body sizes, locomotor modes, and from the three main rodent lineages (Sciuromorpha, Myomorpha, and Hystricomorpha) exhibit a separated condition of the femoral head and greater trochanter. We assessed the femoral ossification of eight species of all six genera of a subterranean lineage of mammals, the African mole-rats (Bathyergidae), including the naked mole-rat (Heterocephalus glaber). Here we report a surprising level of intraspecific variation in the ossification of the proximal femur of H. glaber, which presents both separated and coalesced conditions, regardless of sex and reproductive status. The other bathyergids, including chisel-tooth and scratch-diggers exhibit a separated condition, similar to the typical rodent condition. Because the coalesced condition is uncommon among rodents, our data suggests that the presence of two femoral morphologies in H. glaber represent developmental plasticity in this species. Such a dual condition may result from a constricted femoral head and greater trochanter morphology and slow skeletal growth rates, which could be also influenced by differential loading histories, such as magnitude and orientation of forces acting on the limb during ontogeny. This is the best documented case of intraspecific variation for this trait amongst non-human vertebrates, and its investigation is important to understanding the mechanisms of skeletal development and phenotypic plasticity in mammals.