The changes in the dominance hierarchy over time of a complete field-captured colony of Cryptomys hottentotus hottentotus

The common mole-rat, Cryptomys h. hottentotus , is a social subterranean rodent occurring in colonies in which one female and one to three males are involved in reproduction and the remaining colony members are non-reproductive. Within each sex the reproductive animals are usually the largest and most dominant animals.
The dominance hierarchy amongst a field-captured colony was linear ( h = 0.95, calculated from Landau's linearity index) soon after capture. The non-reproductive females were ranked low in the dominance hierarchy; many were subordinate to non-reproductive males. The order of capture of mole-rats was not related to the position in the dominance hierarchy. The hierarchy became non-linear ( h = 0.56) after six months in captivity during which two juvenile animals became adult. The breakdown in the hierarchy may result from the lack of opportunity in captivity for animals to disperse and establish satellite colonies, or from colony members becoming co-dominant in the hierarchy as a result of a rise in rank by young animals.
Dominant mole-rats are involved in a greater proportion of interactive behaviours than subordinates. Popularity studies show that females tend to be more popular animals than males. The largest reproductive male was the least popular animal in the first study, whereas a beta male was the least popular animal in the second study period. The reproductive female was the most popular in both periods.     

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.     

LH responses to single doses of exogenous GnRH by social Mashona mole-rats: a continuum of socially induced infertility in the family Bathyergidae.

The Mashona mole-rat, Cryptomys darlingi, exhibits an extreme reproductive division of labour. Reproduction in the colony is restricted to a single breeding pair. The non-reproductive male and female colony members are restrained from sexual activity by being familiar and related to one another and the reproductive animals. Circulating basal concentrations of luteinizing hormone (LH) as well as LH levels measured in response to a single exogenous gonadotropin releasing hormone (GnRH) challenge are not significantly different between the reproductive and non-reproductive groups of either sex. Socially induced infertility in both non-reproductive males and females does not result from a reduced pituitary secretion of LH or decreased sensitivity to hypothalamic GnRH, but rather appears to result from an inhibition of reproductive behaviour in these obligate outbreeders. The African mole-rats exhibit a continuum of socially induced infertility with differing social species inhabiting regions of varying degrees of aridity. In this continuum a transition from a predominantly behavioural repression in a social mesic-adapted species through to complete physiological suppression lacking incest avoidance in an arid-adapted eusocial species occurs in this endemic African family of rodents.     

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.     

The social structure and reproductive biology of the common mole-rat, Cryptomys h. hottentotus and remarks on the trends in reproduction and sociality in the family Bathyergidae

Cryptomys h. hottentotus occurs in mesic and semi-arid regions of South Africa. It lives in colonies ofup to 14 individuals, in which reproduction is limited to one ofthe largest males and the largest female in the colony.
Reproduction and details of colony size and the number of breeding animals in a colony are described for one complete and two incomplete field-captured colonies. One incomplete colony was kept in captivity for more than 3 years, whereas the complete colony was autopsied.
The social hierarchy of the common mole-rat is almost linear and has a value of 0.7 1 calculated from Landau's linearity index. Subordinate mole-rats weighed less than dominant mole-rats. The reproductive mole-rats are the dominant animals within the colony. The non-reproductive females rank lowest in the hierarchy.
Mating was not confined to a particular season, but occurred more frequently during the summer months. The alpha male initiated pre-copulatory behaviour. The gestation length is 55 to 66 days (n = 2). Two litters each of three pups were born to the colony during captivity. The pups were relatively altricial. They wandered out of the nest 5 days after birth, began to eat solids when 10 days old, and were fully weaned at 4 weeks. When 2 weeks old the pups began to spar with each other and with some of the adult colony members, but levels of aggression were never high. The pups did not disperse but were incorporated into the colony, this suggesting that C. h. hottentotus colonies are largely composed of related individuals.     

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.     

The colony structure and reproductive biology of the afrotropical Mashona mole-rat, Cryptomys darlingi

Cryptomys darlingi occurs in the mesic Miombo woodland of north-eastem Zimbabwe. It occurs in colonies of up to nine individuals, in which reproduction is limited to one of the largest males and the largest female in the colony.
Reproduction and details of colony size and number of breeding animals in a colony are described for five complete field-captured colonies.
In captivity, mating is not confined to a particular season, and up to three litters of pups are orn per annum. The reproductive female initiates the pre-copulatory behaviour. The gestation lengti is 56–61 days ( n = 2 ). The new-born pups are altricial and litter size is small = 1.7 ± 0.5 ( n = 6). In this case, the pups first left the nest 10 days after birth, began to eat solids when 14 days old, and were fully weaned at five weeks. They began to spar with each other when 36–40 days old, but did not disperse and were incorporated into the colony. This suggests that the Mashona mole-rat colonies are composed of a founding pair and at least three successive litters of pups.     

Colony size and structure, activity patterns and foraging behaviour of a colony of the social mole-rat Cryptomys damarensis (Bathyergidae)

A complete colony of 20 Cryptomys damarensis was trapped in the Kalahari Gemsbok National Park, South Africa. The colony consisted of 15 males and five females and formed three distinct size classes, two of which were presumed to represent worker (smallest mole-rats) and soldier (largest males) castes. Body masses ranged from 86–197 g, with the dominant male being the largest mole-rat. The activity patterns of five animals in the colony were monitored by radiotelemetry. Activity patterns were not influenced by diel fluctuations in burrow temperature and photoperiod. It was suggested that the chance of hyperthemia influenced activity, such that in order to maximize the daily distance burrowed (foraging efficiency), the mole-rats had to engage in frequent (5.58 times. day^-1), but short ( c. 60 min) foraging bouts.     

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.     

Combined Olfactory Contact with the Parent Colony and Direct Contact with Nonbreeding Animals Does Not Maintain Suppression of Ovulation in Female Naked Mole-Rats (Heterocephalus glaber)

The study investigated the role of odor cues from two naked mole-rat colonies, in conjunction with behavioral cues from nonbreeding colony members, in maintaining suppression of ovulation in subordinate female naked mole-rats isolated from the two parent colonies. Four high ranking nonbreeding female naked mole-rats were removed from their respective parent colonies and singly housed in separate burrow systems. For a 64-day period, the removed females were maintained in daily odor contact with their parent colony by daily rotating soiled bedding material between the parent colony and the burrow systems of removed females. In addition, subsets of nonbreeding animals from the respective parent colony were regularly moved into the burrow systems of removed females for 2-day periods during this 64-day period. Removed females were therefore in continual social contact with subsets of parent colony animals except for the breeding pair. All four removed females exhibited raised levels of urinary progesterone (< 2 ng/mg Cr) indicative of the onset of ovarian function within 3 days of being separated from the parent colony. Removed females exhibited a normal ovulatory cycle with levels of progesterone remaining elevated for 25–35 days (mean concentration of progesterone ± SEM; 16.2 ± 2 ng/mg Cr). Initiation of aggression and sexual behavior by removed females increased significantly when they were isolated from the parent colony. The results demonstrated that odor cues from the complete colony in conjunction with behavioral / tactile / vocal cues from the nonbreeding colony members were not the major cues maintaining reproductive suppression in nonbreeding female naked mole-rats. Instead, our results suggest that female reproductive suppression in naked mole-rats is caused by a dominance-related behavioral mechanism requiring direct contact with the breeding female.     

Circulating LH levels and the response to exogenous GnRH in the common mole-rat: implications for reproductive regulation in this social, seasonal breeding species

The effects of breeding season and reproductive status on male and female reproduction were investigated in the common mole-rat, Cryptomys hottentotus hottentotus, a cooperatively breeding rodent which exhibits a unique combination of seasonal breeding and a reproductive division of labor. Pituitary function was examined by measuring the luteinizing hormone (LH) responses to single doses of 2 microg exogenous gonadotrophin-releasing hormone (GnRH) and physiological saline in 69 males and 58 females from 35 wild caught colonies. Neither males nor females exhibited any apparent manifestation of season on basal LH concentrations or on pituitary sensitivity to stimulation by exogenous GnRH. The continuance of reproductive function during the nonbreeding period is essential in common mole-rat males and females, as this period coincides with the period of maximal dispersal opportunity in the winter rainfall area they inhabit. Normal circulating levels of reproductive hormones in dispersing animals may aid intersexual recognition, assist pairbond formation, and thus prime animals for independent reproduction. Circulating basal concentrations of LH as well as LH levels measured in response to a single exogenous GnRH challenge were not significantly different between the reproductive and non-reproductive groups of either sex, suggest the absence of a physiologically well-defined suppression of reproduction in subordinate common mole-rats.     

Molecular insight into patterns of colony composition and paternity in the common mole-rat Cryptomys hottentotus hottentotus

We report the discovery of intraspecific variation in both colony composition and patterns of paternity in two populations of the social common mole-rat Cryptomys hottentotus hottentotus. These two populations represent the mesic and arid habitat extremes of the species' broad ecological range in South Africa. Until recently colonies of the common mole-rat were thought to consist of familial groups whereby all colony members were the offspring of a monogamous reproductive pair. The remaining colony members were thought to forego reproduction until both social and ecological conditions favoured dispersal and opportunities for independent outbreeding. Results from genetic assignment tests using microsatellite markers indicate that while colony composition is dominated by familial groups, colonies within both populations included both adult and subadult foreign conspecifics. Analysis of parentage reveals that the social organization of C. h. hottentotus is not that of strict monogamy; paternity of offspring was not assigned consistently to the largest, most dominant male within the colony. Moreover, a number of significantly smaller males were found to sire offspring, suggesting a sneak-mating strategy by subordinate within-colony males. Extra-colony extra-pair paternity (ECP) was also found to characterize C. h. hottentotus colonies, occurring with similar frequencies in both habitats. Both dominant established breeding males and subordinate males were identified as siring young in nonsource colonies. Furthermore, established breeding males were found to sire extra-colony young in the same season as siring young within their source colonies. We discuss the significance of these results within the context of the divergent ecological regimes characterizing the two sites and observe that our results revisit the accuracy of using behavioural and morphological characters, which have structured the basis of our understanding of the behavioural ecology of this species, as indicators of breeding status in mark-recapture studies.     

Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole-rat,Heterocephalus glaber.

Naked mole-rat colonies are societies with a high reproductive skew, breeding being restricted to one dominant female (the ''queen'') and 1-3 males. Other colony members of both sexes are reproductively suppressed. Experimental removal of breeding males allowed us to investigate the relationship between urinary testosterone and cortisol, dominance rank, and male reproductive status. Dominance rank was strongly correlated with body weight, age, and urinary testosterone titres in males. No relationship between urinary cortisol levels and male reproductive status or dominance was found. Breeding males were among the highest-ranking, heaviest and oldest males in their respective colonies, and were succeeded by other high-ranking, large, old colony males. In contrast to females, no evidence of competition over breeding status was observed among males. Male-male agonism was low both before and after removal of breeders and mate guarding was not observed. The lower reproductive skew for males compared with female skew or queen control over male reproduction may explain why males compete less strongly than females over breeding status after removal of same-sexed breeders.     

Inbreeding avoidance and reproductive skew in a cooperative mammal

In animal social groups, socially subordinate individuals frequently show low reproductive success or completely fail to breed. This suppression of subordinate reproduction is currently typically attributed to control by dominant individuals. However, subordinates in cooperative groups often lack access to unrelated mates, and an alternative possibility is that their reproduction is limited by inbreeding avoidance. Using the eusocial Damaraland mole-rat Cryptomys damarensis, this paper provides the first experimental evidence, to our knowledge, for this explanation. Subordinate, non-breeding female mole-rats were given access to unrelated mates while remaining in the presence of dominant females, and many became reproductively active soon after unrelated males were introduced. Inbreeding avoidance and the availability of unrelated mates provides a plausible and untested explanation for variation in reproductive skew across animal societies.     

Colony defense in Damaraland mole-rats, Cryptomys damarensis

I examined defense against conspecific intruders in coloniesof the Damaraland mole-rat. I introduced foreign animals tocaptive colonies and examined the effect of the sex and breedingstatus of the intruder on the sex and breeding status of thosethat defended. Intruding mole-rats were almost always attacked.Colony defense against intruders was carried out almost exclusivelyby dominant, reproductive individuals and was directed primarily toward individuals of the same sex. Nonbreeding, subordinatemole-rats participated only rarely. These results contrastsharply with colony defense in the related naked mole-rat andsuggest that investment in defense activities in Damaralandmole-rats primarily reflects repulsion of potential competitorsfor breeding status. Subordinate mole-rats may lack incentiveto participate in potentially costly defense, as they are unlikelyto gain reproductive opportunities within the colony and probablygain fitness primarily through dispersing to breed.     

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

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

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.     

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.     

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.