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.     

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)     

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.     

Anovulation in non-reproductive female Damaraland mole-rats (Cryptomys damarensis)

Within colonies of Damaraland mole-rats (Cryptomys damarensis), anovulation in non-reproductive females is thought to play an important role in maintaining reproductive skew. Pituitary sensitivity and ovarian structure were examined in three groups of females that differed with respect to their social environment and breeding status to determine whether anovulation is due to inhibitory social cues or is merely the result of a lack of copulatory stimulation. The contribution of gonadal steroid negative feedback to neuroendocrine differences in the reproductive systems of the respective groups was also investigated. LH secretion after a 0.5 micrograms GnRH challenge in females that had been removed from the presence of the breeding individuals for at least 6 months (removed non-reproductive females) was significantly higher than in non-reproductive females in the colony, but significantly lower than in reproductive females. In both removed non-reproductive females and reproductive females, corpora lutea were observed in ovaries of seven of eight females, indicating that ovulation occurs spontaneously in subordinate females on removal from the breeding pair. Circulating progesterone concentrations in removed non-reproductive females were significantly higher than in non-reproductive females, indicating that circulating progesterone is not responsible for infertility in non-reproductive females. Indeed, after hystero-ovariectomy, reproductive females continued to show significantly greater GnRH-stimulated LH secretion than non-reproductive females. Thus, differential inhibition of gonadotrophin secretion in breeding and non-breeding females occurs independently of gonadal steroids. It is concluded that female Damaraland mole-rats are spontaneous ovulators and that anovulation results from inhibitory social cues within the colony, not a lack of copulatory stimulation. Since non-reproductive females are infertile, inhibition of the hypothalamo-pituitary-gonadal axis has the potential to play a causal role in maintaining reproductive skew in colonies of C. damarensis.     

Stress in an underground empire

The naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Fukomys damarensis) live in large colonies in underground tunnel systems in sub-Saharan Africa. Most members of the colonies are suppressed from reproduction and they are unlikely to reproduce during their lifetime. Only one female and a small number of males reproduce. This extreme cooperative social system has fascinated researchers since the naked mole-rat was first described as eusocial. Despite much research into the mechanisms of social suppression, the exact mechanisms are still unclear. Much evidence points towards high glucocorticoid concentrations caused by agonistic behaviour by the breeding female suppressing reproduction of non-breeders, but laboratory studies have not found any differences in glucocorticoids between breeders and non-breeders. There is, however, considerable evidence from field studies and other social mole-rats that social stress may indeed be an important factor of social suppression in social mole-rats and that those mechanisms are affected by the stability of the colony and environmental conditions. This review aims to provide a summary of the current knowledge of the relationship between environmental conditions, colony stability, glucocorticoids and reproductive suppression in social mole-rat species and suggests some avenues for future research.     

Recrudescence of sexual activity in a reproductively quiescent colony of the Damaraland mole-rat (Cryptomys damarensis), by the introduction of an unfamiliar and genetically unrelated male—a case of incest avoidance in'queenless'colonies

Colonies of the eusocial Damaraland mole-rat, Cryptomys damarensis , are founded from a single reproductive pair of animals genetically unrelated by common descent. All non-reproductive members of the colony are progeny of this reproductive pair. In colonies where the reproductive female has been experimentally removed or has died a natural death, there is a strict incest avoidance and the colony remains reproductively quiescent. Reinstatement of sexual activity in a queenless colony may be brought about in the laboratory by the introduction of an unfamiliar and unrelated adult male.
In the queenless colony under study, there was a marked change in social structure with an increase in Landau's index of linearity from 0.8 to 0.9 on introduction of the new male. The unrelated male became a high ranking dominant reproductive male. The youngest, but most dominant n on-reproductive female became sexually active and subsequently became pregnant and hence acquired the position of reproductive female. The new reproductive female exhibited heightened progesterone (9nmols/mmol creatinine) and oestradiol (3000pmols/mmol creatinine) concentrations in the urine relative to the other non-reproductive females. These hormone concentrations were indicative of a reproductively active female.
Behavioural and hormonal data are presented to show that sexual activity can be re-instated in queenless colonies of laboratory maintained mole-rats by the introduction of unrelated male mole-rats.     

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.     

Ovarian hormones influence odor cues emitted by female meadow voles, Microtus pennsylvanicus.

During the spring-summer breeding season female meadow voles emit odors that are preferred by males, whereas in the autumn-winter season of reproductive quiescence females emit odors that are not preferred by males, but are attractive to females. The effects of daylength and ovarian hormones on salience of female odors were determined by assaying male responses to odors. Females housed in long and short photoperiods transmitted odors that elicited responses similar to those of spring and autumn female voles, respectively. The odor cues emitted by ovariectomized (OVX) females, irrespective of photoperiodic history, were similar to those generated by females during the nonbreeding season. In the absence of ovarian hormones, long daylengths were not sufficient to induce females to broadcast the spring odors preferred by males. Spring-type odor cues were, however, emitted by OVX voles housed in either photoperiod and treated with estradiol. Ovarian hormones appear necessary and sufficient to generate breeding season odor cues and sufficient to induce production of such cues during the nonbreeding season. We conclude that daylength affects odor cues emitted by females by altering ovarian hormone activity.     

Breeding status affects motoneuron number and muscle size in naked mole-rats: recruitment of perineal motoneurons?

Naked mole-rats live in large colonies and exhibit a strict reproductive hierarchy. Each colony has one breeding female and one to three breeding males; all other individuals are nonreproductive subordinates. Subordinates show a remarkable lack of sex differences in behavior and anatomy, but can become reproductive if removed from the colony. We recently reported that the striated perineal muscles and their innervating motoneurons, which are sexually dimorphic in all other mammals examined to date, are not dimorphic in subordinate naked mole-rats. Here we asked whether sexual differentiation of this neuromuscular system occurs when a subordinate becomes a breeder. The size and number of cells within Onuf's nucleus (homologue of the rat spinal nucleus of the bulbocavernosus) as well as perineal muscle volume were examined in subordinate and breeding naked mole-rats of both sexes. Sex differences in perineal motoneurons were not observed, regardless of social status. To our surprise, however, counts of motoneurons in Onuf's nucleus were increased approximately 30% in breeders of both sexes. This was accompanied by a reciprocal decrease in cells in Onuf's nucleus that were characterized by small soma size, and lacked a clear nucleus or nucleolus. Although not exhibiting typical motoneuron morphology, some of these small cells were positive for the motoneuron marker, SMI-32. The neuronal changes correlate with increased perineal muscle volumes in breeders. We propose that small, relatively undifferentiated cells are recruited to the pool of large Onuf's nucleus motoneurons when subordinate naked mole-rats become breeders.     

Social cues elicit sexual behavior in subordinate Damaraland mole-rats independent of gonadal status

Damaraland mole-rats (Fukomys damarensis) are among a small number of eusocial mammals. Eusociality is a social system where only a few individuals within a colony engage in direct reproduction, while remaining subordinate members are non-breeders and support reproductive efforts of breeding individuals. Inbreeding avoidance precludes mating between subordinate siblings and between offspring and parents. Interestingly, non-breeders readily attempt to mate with unrelated opposite-sex individuals. This is unusual since the non-breeding females do not attain puberty while in their natal colony. Based on this finding, the present study investigated the role of the gonads in the regulation of mating behaviors in this species and identified the mechanism of inbreeding avoidance. Gonadal-intact and gonadectomized non-breeders from different colonies were removed from their colonies and tested for the expression of sexual behavior. Results indicated that gonadal status had only minor effects on the expression of sexual behavior in either males or females. In a second experiment, sexual behaviors were absent between opposite-sex siblings so long as they had frequent contact with each other; however, following 5 weeks of separation, sexual behavior between these siblings was robustly expressed. Thus, Damaraland mole-rats avoid establishing mating relationships with familiar individuals but will readily mate with unfamiliar individuals of the opposite sex, with genetic relatedness apparently playing little role. The initiation of sexual behavior in Damaraland mole-rats does not require the presence of the gonads, but does require that the members of the pair have not been in contact with one another for at least several weeks.     

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.     

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.     

The colony structure and dominance hierarchy of the Damaraland mole-rat, Cryptomys damarensis (Rodentia: Bathyergidae), from Namibia

Cryptomys damarensis is one of the few subterranean rodents which is social. This species is found in the semi-arid regions of southwestern and central Africa. The Damaraland mole-rat occurs in coloniesof up to 25 individuals, in which reproduction is limited to one or two of the largest males and the largest female in the colony.
The mean colony size is 18 mole-rats ( n =6 colonies). The mean colony biomass is 2.32 kg and the sex ratio is female biased (0.71–0.78). The number of mole-rats in each colony, the mean body mass and the sex ratio are described for six field-captured colonies, three of which were captured in their entirety.
The dominance hierarchy of two colonies of C. damarensis was found to be linear with a value of between 0.94 and 1.00 calculated from Landau's linearity index. Dominance was found to be related to gender, with the males more dominant than females. The reproductive individuals are the dominant animals within each respective gender. The non-reproductive females rank lowest in the hierarchy.     

Reproductive suppression in eusocial Cryptomys darnavensis colonies: socially-induced infertility in females

Inhibition of reproduction occurs in colonies of the Damaraland mole-rat ( Cryptomys damarensis ), where one female and usually one male are reproductively active. They remain the sole reproductive animals thoughout their stay in the colony, which in the field may exceed five years.
An 18-month study on a captive colony of C. damarensis shows that non-reproductive females remain anovulatory and always have concentrations of urinary progesterone lower than that of the reproductive female 10.7 8.8 nmols/mmol creatinine (n = 85), although their progesterone concentrations are slightly elevated when the reproductive female is early in pregnancy. In contrast the reproductively active female has elevated concentrations of progesterone 63.3 70.1 nmols/mmol creatinine (n= 14).
Standard histological together with immunohistochemical examination of the ovarian structure shows that follicular development in the non-reproductive females is halted at varying stages prior to ovulation and that the unruptured follicles luteinize. These unruptured luteinized follicles stain positive for 3β hydroxysteroid dehydrogenase—the enzyme catalysing the synthesis of progesterone from pregnenolone. It is possible that the low levels of circulating progesterone produced by the luteinized follicles in the non-reproductive females in the colony are sufficient to feedback on the hypothalamo-pituitary axis and prevent the surge of LH necessary for ovulation.
Behavioural studies provide corroborative evidence for sexual suppression. Thus the non-reproductive females in the colony are never involved in courtship or copulatory behaviour. nor do they actively solicit males in the colony. The reproductive female, however, plays an active role in mate selection and is the initiator in courtship behaviour.
The suppression of ovulation in non-reproductivc females is maintained for as long as there is a reproductive female in the colony.     

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.     

Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the system of mating

Early field work on naked mole-rats, Heterocephalus glaber, suggestedthat small colonies are rare and that colonies can only formby fissioning of existing colonies. Many researchers expectedthat this would result in extreme inbreeding and high relatednesswithin colonies and would thus explain the evolution of eusocialityin naked mole-rats. Here I report evidence of dispersers andoutbreeding in colonies of wild naked mole-rats that suggeststhat inbreeding is not the system of mating for this speciesand that outbreeding is probably frequent. Wild dispersers havethe same morphology as was reported for dispersers in laboratorycolonies. Low levels of genetic variation in previous moleculargenetic studies of naked mole-rats probably result from theviscous population structure typical of fossorial rodents.     

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.     

Investigation of genetic diversity in wild colonies of naked mole-rats (Heterocephalus glaber) by DNA fingerprinting

DNA from 20 individuals from four wild colonies of naked mole-rats, Heterocephalus glaber , were analysed for restriction fragment length polymorphism of class I major histocompatibility complex genes and minisatellite DNA, both of which have been shown to be highly variable between individuals in other species. The minisatellite probe employed in this study revealed limited polymorphism in the DNA of naked mole-rats, both within and between neighbouring colonies. Of the two class I major histocompatibility complex probes, both showed a lack of polymorphism within colonies, while one revealed a single difference in the restriction fragment pattern between one colony and the other three. This probe also revealed a possible variation in copy number of genes in some individuals. The low numbers of bands on the restriction fragment pattern also indicated that the naked mole-rat MHC I, in contrast to that of other mammalian species, may contain relatively few genes homologous to the class I major histocompatibility complex of the mouse. The absence of variability in naked mole-rat DNA in these normally highly polymorphic loci suggests that there may be little or no genetic diversity either within or between closely neighbouring colonies of naked mole-rats in the wild. The lack of polymorphism in the MHC I questions its possible role in individual odour recognition in this species of rodent.     

Influence of gonadal sex hormones on behavioral components of the reproductive hierarchy in naked mole-rats

Naked mole-rats (Heterocephalus glaber) are fossorial, eusocial rodents that live in colonies which typically include 60-80 individuals. Generally, only one of the females and 1-3 of the males in a colony are reproductives. The reproductives engage in mutual genital nuzzling behavior that is rarely exhibited by subordinates (non-reproductives). Thus, genital nuzzling may represent a mechanism of bonding and/or specific recognition between reproductive individuals. We investigated whether gonadal hormones are involved in the maintenance of genital nuzzling behavior and mating behaviors in isolated pairs of mole-rats and also in established breeding pairs of mole-rats within colonies. We also explored whether sex hormone deprivation would alter the strict partner preference for performance of nuzzling within colonies. Our results indicate (a) considerable variation between pairs in the frequency of nuzzling, (b) a reduction in the frequency of nuzzling following castration of the male and restoration of the 'baseline' frequency after replacement of testosterone in castrated males, (c) the failure of either castration or combined castration and ovariectomy to eliminate genital nuzzling in established pairs, and (d) the exhibition of nuzzling behavior by some of the subordinates in all three experimental colonies beginning several weeks after gonadectomy of both of the reproductives. No cases of lordosis behavior were seen during the approximately 109 h of behavioral observations. This is not surprising, since female mole-rats have an approximately 30-day ovulatory cycle, and lordosis only occurs during a peri-ovulatory period of a few hours. A total of 44 cases of mounting behavior were recorded; all these involved breeding males in colonies or males from isolated pairs, and all occurred when males were either gonad-intact or castrated with testosterone replacement. Thus, in contrast to nuzzling behavior, male sex behavior appeared to be eliminated during androgen deprivation.     

LH responses of female naked mole-rats, Heterocephalus glaber, to single and multiple doses of exogenous GnRH

To investigate possible differential pituitary secretion of LH in breeding and non-breeding female naked mole-rats, the LH responses to administration of exogenous GnRH were measured in 55 females from 20 captive colonies. Single doses of 0.1, 0.5 or 1.0 micrograms GnRH produced a significant rise in plasma LH concentrations 20 min after s.c. injection in breeding and non-breeding females at all doses (P less than 0.001). While at the highest dose of 1.0 microgram there was no difference in the LH response between breeding and non-breeding females, as the dose was lowered there was a progressive decline in the LH response in non-breeding females such that, at the 0.1 microgram dose, GnRH produced only a small, but significant, increase in plasma LH (1.3 +/- 0.2 to 2.9 +/- 0.5 mi.u./ml, N = 5) compared with breeding females (3.4 +/- 0.8 to 9.6 +/- 2.0 mi.u./ml, N = 6). The LH responses of the latter were not significantly reduced at the lower doses of GnRH. The apparent lack of sensitivity to low doses of exogenous GnRH in non-breeding females was reversed by 4 consecutive 1-h injections of 0.1 microgram, which produced a rise in LH from 1.2 +/- 0.2 to 9.0 +/- 0.2 mi.u./ml (N = 4), comparable to that of breeding females given a single injection of 0.1 microgram GnRH. These results suggest that the anterior pituitary in non-breeding female naked mole-rats is less sensitive to low doses of exogenous GnRH than in breeding females, possibly due to a lack of priming by endogenous GnRH. Therefore, the socially-induced block to ovulation in non-breeding female naked mole-rats may be due to inhibition of hypothalamic GnRH secretion.