Kin discrimination and female mate choice in the naked mole-rat Heterocephalus glaber

Naked mole-rats are fossorial, eusocial rodents that naturally exhibit high levels of inbreeding. Persistent inbreeding in animals often results in a substantial decline in fitness and, thus, dispersal and avoidance of kin as mates are two common inbreeding avoidance mechanisms. In the naked mole-rat evidence for the former has recently been found. Here we address the latter mechanism by investigating kin recognition and female mate choice using a series of choice tests in which the odour, social and mate preferences of females were determined. Discrimination by females appears to be dependent on their reproductive status. Reproductively active females prefer to associate with unfamiliar males, whereas reproductively inactive females do not discriminate. Females do not discriminate between kin and non-kin suggesting that the criterion for recognition is familiarity, not detection of genetic similarity per se. In the wild, naked mole-rats occupy discrete burrow systems and dispersal and mixing with non-kin is thought to be comparatively rare. Thus, recognition by familiarity may function as a highly efficient kin recognition mechanism in the naked mole-rat. A preference by reproductively active females for unfamiliar males is interpreted as inbreeding avoidance. These findings suggest that, despite an evolutionary history of close inbreeding, naked mole-rats may not be exempt from the effects of inbreeding depression and will attempt to outbreed should the opportunity arise.     

Social suppression of reproduction in male naked mole-rats, Heterocephalus glaber

To investigate possible anatomical and endocrine differences between breeding and non-breeding male naked mole-rats, 113 animals from 24 captive and 4 wild colonies were studied. While breeding males had larger reproductive tract masses compared to non-breeders relative to body mass (P less than 0.01), spermatogenesis was active in all of the non-breeding males examined histologically (n = 9) and spermatozoa were present in the epididymides. Compared with non-breeders, breeding males had significantly higher urinary testosterone concentrations (mean +/- s.e.m.: 23.8 +/- 2.3 vs 5.2 +/- 1.4 ng/mg Cr respectively; P less than 0.001), and plasma LH (10.7 +/- 1.7 vs 5.0 +/- 0.8 mi.u./ml respectively; P less than 0.01). Single doses of 0.1, 0.5 or 1.0 microgram GnRH produced a significant rise in plasma LH concentrations 20 min after s.c. injection in breeding and non-breeding males at all doses (P less than 0.001). However, there were differences in the magnitude of the LH response following administration of GnRH between breeding and non-breeding males, with non-breeding males showing a dose-response and having lower plasma LH concentrations 20 min after a single injection of 0.1 or 0.5 microgram (P less than 0.05), but not 1.0 microgram, GnRH. This apparent lack of pituitary sensitivity of non-breeding males to single doses of exogenous GnRH was reversed by 4 consecutive injections of 0.5 microgram GnRH at hourly intervals, suggesting that the reduced sensitivity may be the result of insufficient priming of the pituitary by endogenous GnRH. These results indicate that, despite the fact that non-breeding males were apparently producing mature gametes, clear endocrine deficiencies existed in male naked mole-rats.     

Micro- and macrogeographical genetic structure of colonies of naked mole-rats Heterocephalus glaber

Patterns of genetic structure in eusocial naked mole-rat populations were quantified within and among geographically distant populations using multilocus DNA fingerprinting and mitochondrial DNA (mtDNA) sequence analysis. Individuals within colonies were genetically almost monomorphic, sharing the same mtDNA control region haplotype and having coefficients of band sharing estimated from DNA fingerprints ranging from 0.93 to 0.99. Family analysis of a hybrid captive colony of naked mole-rats with increased levels of genetic variability using multilocus DNA fingerprinting gave results consistent with Mendelian inheritance, and has revealed for the first time that multiple paternity can occur. In a survey of wild colonies from Ethiopia, Somalia and locations in northern and southern Kenya, we have examined mtDNA control region sequence variation in 42 individuals from 15 colonies, and together with multilocus DNA fingerprinting and mtDNA cytochrome- b sequence analysis in selected individuals have shown that these populations show considerable genetic divergence. Most of the variance in sequence divergence was found to be between geographical locations (Φ_ct= 0.68) and there was a significant correlation between sequence divergence and geographical separation of haplotypes. Six colonies from Mtito Andei in southern Kenya shared the same control region haplotype, suggesting a recent common maternal ancestor. In contrast, out of four colonies at Lerata in north Kenya, three haplotypes were identified, and phylogenetic analysis suggests that this area may be a zone where two distinct lineages are in close proximity. Genetic distances were maximal between Ethiopian and southern Kenyan populations at 5.8% for cytochrome- b , and are approaching interspecific values seen between other Bathyergids.     

Relaxation of reproductive suppression in non-breeding female naked mole-rats, Heterocephalus glaber

Ninety-four non-reproductive female naked mole-rats, from seven colonies, were studied in terms of vaginal perforation, vaginal smears and urinary concentrations of oestradiol-17β and progesterone in relation to the time of parturition of the breeding female, the queen. The study concentrated mainly on the period from nine days prepartum to 13 days postpartum of 12 births. Sixty-eight percent ( n = 253) of the non-reproductive females had detectable urinary concentrations of oestradiol-17β and many of these had perforated vaginas throughout the study period. These females showed a significantly increased urinary concentration of oestradiol six days prior to parturition of the queen. In females with undetectable concentrations of oestradiol-17β, the proportion with perforated vaginas increased from six days prepartum (54%) to reach a peak on the day of parturition (92%) of the queen. Urinary progesterone-concentrations were 0.7nmol/mmol creatinine at some stage in the study period in 90% of the females and scattered short peaks or spikes were experienced by all these females, but without synchronization between the females in a colony and without any detectable correlation with the time of parturition of the queen. Maximal concentrations in some females were comparable to the values in cycling breeding females during the luteal phase, but were of a much shorter duration than in breeding females. Vaginal smears did not show clear cyclic patterns.     

Perineal muscles and motoneurons are sexually monomorphic in the naked mole-rat (Heterocephalus glaber)

Naked mole-rats are eusocial mammals that live in colonies with a single breeding female and one to three breeding males. All other members of the colony, known as subordinates, are nonreproductive and exhibit few sex differences in behavior or genital anatomy. This raises questions about the degree of sexual differentiation in subordinate naked mole-rats. The striated perineal muscles associated with the phallus [the bulbocavernosus (BC), ischiocavernosus (IC), and levator ani (LA) muscles], and their innervating motoneurons, are sexually dimorphic in all rodents examined to date. We therefore asked whether perineal muscles and motoneurons were also sexually dimorphic in subordinate naked mole-rats. Muscles similar to the LA and IC of other rodents were found in naked mole-rats of both sexes. No clear BC muscle was identified, although a large striated muscle associated with the urethra in male and female naked mole-rats may be homologous to the BC of other rodents. There were no sex differences in the volumes of the LA, IC, or the urethral muscles. Motoneurons innervating the perineal muscles were identified by retrograde labeling with cholera-toxin-conjugated horseradish peroxidase. All perineal motoneurons were found in a single cluster in the ventrolateral lateral horn, in a position similar to that of Onuf's nucleus of carnivores and primates. There was no sex difference in the size or number of motoneurons in Onuf's nucleus of naked mole-rats. Thus, unlike findings in any other mammal, neither the perineal muscles nor the perineal motoneurons appear to be sexually differentiated in subordinate naked mole-rats.     

Social control of reproduction in breeding and non-breeding male naked mole-rats (Heterocephalus glaber).

Eight male naked mole-rats, from three colonies were studied in captivity. When non-breeding male naked mole-rats were removed from their colonies and paired with a non-breeding female, or removed and housed singly for 6 weeks before pairing with a female, concentrations of urinary testosterone and plasma luteinizing hormone (LH) increased significantly (P less than 0.05). Concentration of these hormones were highest while the males were singly housed: urinary testosterone (mean +/- s.e.m.) increased from 8.2 +/- 1.3 ng/mg urinary creatinine (Cr) in a non-breeder in a colony to 49.1 +/- 5.5 ng/mg Cr when singly housed and 21.8 +/- 2.5 ng/mg Cr when paired with a female. Plasma LH concentrations increased from 4.7 +/- 1.0 miu/ml when a non-breeder in a colony to 19.8 +/- 4.0 miu/ml when singly housed and 9.9 +/- 1.1 miu/ml when paired with a female. After pairing with a female, the pattern of urinary testosterone secretion in the male was synchronized with the ovarian cycle of the female mate, such that urinary testosterone concentrations were significantly higher during the early follicular phase of the female's cycle (P less than 0.05). These results suggest that active suppression of reproductive physiology by social cues occurs in non-breeding male naked mole-rats, and that this is readily reversible if social cues are removed and males are housed singly. When a male was subsequently paired with a female, endocrine suppression was partially reimposed on the reproductively active males, such that urinary testosterone concentrations were suppressed to values similar to those in non-breeding males, except for periods prior to mating.(ABSTRACT TRUNCATED AT 250 WORDS)     

Thermogenic changes with chronic cold exposure in the naked mole-rat (Heterocephalus glaber)

The naked mole-rat (Heterocephalus glaber) lives communally in a thermally buffered underground habitat. Here, it relies primarily on ectothermic (behavioral) mechanisms to maintain body temperature (T(b)). Outside this milieu, it is unable to effectively regulate T(b) and T(b) tracks that of ambient temperature (T(a)). Although naked mole-rats, in their natural habitat have little need for cold-tolerance, we questioned whether or not thermogenic capacity would change with prolonged (>1 year) exposure to cooler conditions. We hypothesized that these rodents would not conform to common mammalian patterns and that non-shivering thermogenic (NST) capacity would be unchanged with chronic cold exposure. The capacity for NST was assessed following noradrenaline administration (0.8 mg/kg, s.c.) to lightly anesthetized (pentobarbital 6% m/v 40 mg/kg) animals and monitoring the concomitant changes in oxygen consumption and T(b). Results concur with the null hypothesis in that prolonged cold exposure did not elicit any increase in NST capacity (1.52+/-0.17 ml O(2)/g/h, cold-acclimated; 1.73+/-0.31 ml O(2)/g/h, control; P>0.05). Rapid heat loss across their uninsulated integument may necessitate continuous maximal stimulation of brown adipose tissue (BAT), and as such, prevent any further increase in thermogenic capacity following cold exposure.     

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.     

Erfahrungsbericht zur Haltung von Nacktmullen (Heterocephalus glaber) im Zoo Dresden

Dresden Zoo has been keeping Naked mole-rats since 1995. But breeding was successful not until 2003. This report describes two different facilities of keeping and managing Naked mole-rats. Mole-rats react extremely sensitive to vibration and they have exceptional climate requirements. Despite their enormous sensitivity to disturbances our experiences indicate that an attractive presentation is possible.     

Morphine induces aggression but not analgesia in the naked mole-rat (Heterocephalus glaber)

1. The antinociceptive effect in the mole-rat of morphine (1, 10, 20 or 30 mg/kg) and nefopam (10 or 20 mg/kg) was studied. 2. In the hotplate test, morphine had no analgesic effect. A reduced response latency after morphine (10 and 20 mg/kg) could possibly be explained by hyperactivity and excited behaviour. 3. After morphine (10, 20 and 30 mg/kg) most of the animals died after fighting when kept in colony cages. Aggressive behaviour and death was prevented by naloxone, or by keeping the animals in single cages. 4. Nefopam (20 mg/kg) significantly increased the latency for the nociceptive response. 5. It was concluded that in the mole-rat, opioid systems in the CNS may not be involved in the regulation of nociception, but in the regulation of agonistic and motor behaviour.     

Genetic diversity of the naked mole‐rat (Heterocephalus glaber)

The naked mole‐rat (Heterocephalus glaber) is used as an animal model in various studies, but not much is known on the genetic diversity of this animal. Here, on the basis of dataset collected from the most part of the distribution range of the naked mole‐rat, we reconstruct phylogenetic relationships between its different lineages using mitochondrial and nuclear markers. We also mapped the distribution of the main genetic lineages, dated the divergence using different Bayesian tree‐calibration techniques, and modeled the distribution of ecological niches for the period of last glacial maximum. Our results show the existence of two deeply divergent clades designated as the eastern clade (East Ethiopia) and the southern clade (South Ethiopia and North Kenya). Additional phylogeographic structure was demonstrated for each of these two clades. Divergence between these two main lineages dated back to the Middle Pleistocene (ca. 1.4–0.8 Mya) and may have been related to climate changes in Africa during the Mid‐Pleistocene Revolution. In light of substantial genetic differences between the eastern and southern lineages of the naked mole‐rat, these two clades can be considered as two deeply divergent subspecies or even as distinct species.     

Dominance and queen succession in captive colonies of the eusocial naked mole-rat,Heterocephalus glaber.

Naked mole-rat colonies exhibit a high reproductive skew, breeding being typically restricted to one female (the ''queen'') and one to three males. Other colony members are reproductively suppressed, although this suppression can be reversed following the removal or death of the queen. We examined dominance and queen succession within captive colonies to investigate the relationship between urinary testosterone and cortisol, dominance rank and reproductive status; and to determine if behavioural and/or physiological parameters can be used as predictors of queen succession. Social structure was characterized by a linear dominance hierarchy before and after queen removal. Prior to queen removal, dominance rank was negatively correlated with body weight and urinary testosterone and cortisol titres in males and females. Queen removal results in social instability and aggression between high ranking individuals. Dominance rank appears to be a good predictor of reproductive status: queens are the highest ranking colony females and are succeeded by the next highest ranking females. The intense dominance-related aggression that accompanies reproductive succession in naked mole-rats provides empirical support for optimal skew theory.     

Antiphonal Vocalization of a Subterranean Rodent, the Naked Mole-Rat (Heterocephalus glaber)

Acoustic signalling is one of the most common communication mediums in a broad range of social animals, and it often encodes attributes of the signaller such as sex, kin relatedness and dominance rank. Particularly, antiphonal vocalization has been regarded to have an important function in animals living in an environment where visual cues are unreliable. Antiphony enables to acknowledge that one's signal was received with certainty. We show the first evidence of such acoustic signals among rodents: the naked mole‐rat. The society of this eusocial subterranean species is organized hierarchically according to body size. Naked mole‐rats are functionally blind, and rely highly on acoustic communication. We focused on one of their vocalizations: the soft chirp (SC). SCs are the most frequent sounds, and are often emitted upon physical contact. We expected the SC to be antiphonal, and if so, SC may function to distinguish colony members from intruders, and/or identify social rank and individuality. To examine our predictions, we placed pairs of individuals of different size together, and recorded their vocal behaviour. The intervals between the SCs of two individuals were shorter than expected intervals which were based on the assumption that animals vocalized without reference of the preceding SC. The acoustic properties of SCs varied among individuals according to body weight and colony of origin. The emission rate was positively related to the relative difference in body weight. Therefore, SCs have an antiphonal nature and may function as expected. These characteristics of SC were highly similar to those of antiphonal sounds in other social species.     

Tissue metabolism and enzyme activities in the rodent Heterocephalus glaber, a poor temperature regulator.

1. Tissue oxygen uptake and enzyme activities were investigated in the naked mole rat, Heterocephalus glaber, a mammal notable for its low body temperature and metabolism and poor temperature regulating ability. 2. Q10 for O2 uptake of Heterocephalus crude liver homogenates ranged from 1.91 for the temperature interval 25-30 degrees C to 1.76 within the range 30-38 degrees C, values similar to those reported for typical homoiotherms. 3. Km pyruvate of lactate dehydrogenase in heart muscle had the same temperature dependence in the mole rat and mouse. 4. O2 uptake and cytochrome oxidase activity of skeletal muscle were higher for mole rat than mouse. The reverse was true for heart muscle. Brain and liver O2 uptake showed similar values for both species, while kidney O2 uptake was highest in the mouse. 5. Pyruvate kinase activity in heart and skeletal muscle was higher in mouse than mole rat, suggesting a greater reliance on glycolysis in the former. 6. Na+, K+ -ATPase activity of liver and kidney was 60% higher in mouse than mole rat, while brain was 30% higher in mouse. 7. The results indicate that the effects of temperature on tissue metabolism in the mole rat conform to those in typical homoiotherms. The low body temperature and O2 uptake in the mole rat find no expression in the tissue respiratory capacity.     

Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats, Heterocephalus glaber

To investigate the endocrine cause of reproductive suppression in nonbreeding female naked mole-rats, animals from 35 colonies were studied in captivity. Urinary and plasma progesterone concentrations were elevated in pregnant females (urine: 10.0-148.4 ng/mg Cr, 27 samples from 8 females; plasma: 3.6-30.0 ng/ml, 5 samples from 5 females; Days 21-40 of pregnancy) and cyclic breeding females (urine: 0.5-97.8 ng/mg Cr, 146 samples from 7 females; plasma: less than 1.0-35.4 ng/ml, 25 samples from 7 females). The latter group showed cyclic patterns of urinary progesterone, indicating a mean ovarian cycle length of 34.4 +/- 1.6 days (mean +/- s.e.m.) with a follicular phase of 6.0 +/- 0.6 days and a luteal phase of 27.5 +/- 1.3 days (19 cycles from 9 breeding females). In non-breeding females urinary and plasma progesterone values were undetectable (urine: less than 0.5 ng/mg Cr, 232 samples from 64 females; plasma: less than 1.0 ng/ml, 7 samples from 6 females). Breeding females had higher (P less than 0.001) plasma LH concentrations (3.0 +/- 0.2 mi.u./ml, 73 samples from 24 females) than did non-breeding females (1.6 +/- 0.1 mi.u./ml, 57 samples from 44 females). Urinary and plasma progesterone concentrations in non-breeding females from wild colonies situated near Mtito Andei, Kenya, were either below the assay sensitivity limit (urine: less than 0.5 ng/mg Cr, 11 females from 2 colonies; plasma: less than 1.0 ng/ml, 25 females from 4 colonies), or very low (plasma: 1.6 +/- 0.6 ng/ml, 15 females from 4 colonies). In captivity, non-breeding females removed from their colonies (i.e. the dominant breeding female) and either paired directly with a non-breeding male (N = 2), or removed and housed singly for 6 weeks before pairing with a non-breeding male (N = 5) may develop a perforate vagina for the first time in as little as 7 days. Urinary progesterone concentrations rose above 2.0 ng/mg Cr (indicative of a luteal phase) for the first time 8.0 +/- 1.9 days after being separated. These results suggest that ovulation is suppressed in subordinate non-breeding female naked mole-rats in captive and wild colonies, and show that plasma LH concentrations are significantly lower in these non-breeding females. This reproductive block in non-breeding females is readily reversible if the social factors suppressing reproduction are removed.