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.     

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

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

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.     

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.     

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)     

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.     

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.     

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.     

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.     

Reproductive suppression in female Damaraland mole-rats Cryptomys damarensis: dominant control or self-restraint?

Colonies of Damaraland mole-rats Cryptomys damarensis exhibit a high reproductive skew. Typically one female breeds and the others are anovulatory. Two models, the dominant control model (DCM) and the self-restraint model (SRM), have been proposed to account for this reproductive suppression. The DCM proposes that suppression is under the control of the dominant breeder and is imposed by mechanisms such as aggression, pheromones and interference with copulation, whereas the SRM does not involve aggression directed towards non-breeders and may function in order to minimize inbreeding. We investigated potential proximate mechanisms involved in the suppression of females in a series of experiments. Socially induced stress through aggression did not appear to be responsible for anovulation. Nor did breeders actively interfere with subordinate copulation. Females were physiologically suppressed when housed in intact colonies. However, as predicted by the DCM, they did not become reproductively active when removed from the presence of breeders. We found no evidence that pheromonal cues block ovulation. We suggest that the SRM is the basic model found in the Damaraland mole-rat and that self-restraint functions in order to minimize inbreeding by restricting reproduction until an unrelated male is present. This would explain the rapid onset of reproductive activation in females when paired with an unrelated male, as demonstrated in this study.     

Termite colony ontogeny: a long-term assessment of reproductive lifespan, caste ratios and colony size in Reticulitermes flavipes (Isoptera: Rhinotermitidae)

Thirty Reticulitermes flavipes (Kollar) colonies established by alates collected from two separate field sites were raised in the laboratory for eight years. Twenty-one of the colonies were founded by alates from one field source and nine from another, providing demographic data from two unrelated parental lineages. Colony totals ranged from 3620 to 11641 individuals, with no significant difference in size between lineages. Soldier caste proportion of the colony total and mean wet weights for workers, soldiers and kings were significantly different between the two lineages. This suggests that at least a portion of the variability observed in caste ratios and body size may be heritable. One founding reproductive had died in five of the colonies (17%); none lost both parents. The queenless colonies contained exclusively female replacement reproductives (neotenics); the kingless colony contained a female-skewed mixture of male and female neotenics. All the nests that lost a founding parent contained significantly more pre-alate nymphs than the nests with both a king and a queen. Comparisons with published reports of ontogenetic patterns in other termites and social insects are discussed.     

Nestmate recognition by guards of the Asian hive bee <Emphasis Type="Italic">Apis cerana</Emphasis>

When a honey bee colony becomes queenless and broodless its only reproductive option is for some of its workers to produce sons before the colony perishes. However, for this to be possible the policing of worker-laid eggs must be curtailed and this provides the opportunity for queenless colonies to be reproductively parasitized by workers from other nests. Such reproductive parasitism is known to occur in Apis florea and A. cerana. Microsatellite analyses of worker samples have demonstrated that the proportion of non-natal workers present in an A. cerana colony declines after a colony is made queenless. This observation suggests that queenless A. cerana colonies may be more vigilant in repelling potentially parasitic non-natal workers than queenright colonies. We compared rates of nestmate and non-nestmate acceptance in both queenright and queenless A. cerana colonies using standard assays and showed that there is no statistical difference between the proportion of non-nestmate workers that are rejected in queenless and queenright colonies. We also show that, contrary to earlier reports, A. cerana guards are able to discriminate nestmate workers from non-nestmates, and that they reject significantly more non-nestmate workers than nestmate workers. Received 25 February 2008; revised 21 May 2008; accepted 25 June 2008.     

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.     

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.     

Associations between reproduction and work in workers of the Asian hive bee Apis cerana

If a honey bee (Apis spp.) colony becomes queenless, about 1/3 of young workers activate their ovaries and produce haploid male-producing eggs. In doing so queenless workers maximize their inclusive fitness because the normal option of vicarious production of relatives via their queen’s eggs is no longer available. But if many workers are engaged in reproduction, how does a queenless colony continue to feed its brood and forage? Here we show that in the Asian hive bee Apis cerana hypopharyngeal gland (HPG) size is larger in queenless workers than in queenright workers and that bees undertaking brood-rearing tasks have larger HPG than same-aged bees that are foraging. In queenless colonies, workers with a smaller number of ovarioles are more likely to have activated ovaries. This reinforces the puzzling observation that a large number of ovarioles reduces reproductive success in queenless A. cerana. It further suggests that reproductive workers either avoid foraging or transition to foraging later in life than non-reproductive workers. Finally, our study also showed that ovary activation and larger-than-average numbers of ovarioles had no statistically detectable influence on foraging specialization for pollen or nectar.     

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.     

Are non-reproductive male highveld mole-rats, Cryptomys hottentotus pretoriae physiologically suppressed while in the confines of the natal colony?

The highveld mole-rat, Cryptomys hottentous pretoriae is a social, subterranean, co-operative breeder with a high reproductive skew. The relationship between reproductive status and reproductive physiology in male highveld mole-rats was investigated. Testicular morphometrics, histological parameters, plasma testosterone concentrations and sperm motility parameters were studied in 31 males (14 reproductive and 17 non-reproductive males). Reproductive males were significantly larger than non-reproductive males, with testicular mass and volume corrected for body mass considerably larger for the reproductive males. Circulating plasma testosterone concentrations of reproductive males were not significantly higher than non-reproductive males (reproductive males 10.3±1.8 nmol l⁻¹ vs non-reproductive males 7.3±1.74 nmol l⁻¹). Sperm motility parameters were measured, but no significant differences were found between reproductive and non-reproductive males. All 14 reproductive males had motile sperm, whereas 13 of the 17 (76%) of non-reproductive males possessed motile sperm. A typical ejaculate of a reproductive male contains 48.3% motile sperm characterized by a high percentage of flagellar defects, whereas the non-reproductive male has an ejaculate containing 45.6% motile sperm with a high percentage of head defects. It is apparent that non-reproductive males are not physiologically suppressed from reproducing. Moreover, the non-reproductive males are excluded from incestuous matings as a result of being the offspring of the reproductive female.     

Social behavior and brood decline in reproductive-phase colonies ofBelonogaster petiolata (Degeer) (Hymenoptera: Vespidae)

Colonies ofBelonogaster petiolata in Gauteng (South Africa) produced reproductive offspring (gynes and males) in late January and early February of each nesting season; their appearance was associated with a decline in worker and brood numbers. Brood decline could commence in the presence of a dominant, reproductively active queen, and loss or removal of the queen was not followed directly by cessation of nest growth and brood care. An older worker usually took over the α-position in queenless colonies. Several factors appear to contribute to brood decline and, ultimately, termination of the colony cycle in this species. These include (1) cessation of the supply of solid food to colonies (and particularly their larvae) during the reproductive phase, (2) a decrease in the worker/larva ratio during the latter phase due to the progressive loss of workers, (3) increasing number of gynes and males, and (4) an adult priority over food reception from foragers.     

Reproduction Is Associated with a Tissue-Dependent Reduction of Oxidative Stress in Eusocial Female Damaraland Mole-Rats (Fukomys damarensis)

Oxidative stress has been implicated as both a physiological cost of reproduction and a driving force on an animal''s lifespan. Since increased reproductive effort is generally linked with a reduction in survival, it has been proposed that oxidative stress may influence this relationship. Support for this hypothesis is inconsistent, but this may, in part, be due to the type of tissues that have been analyzed. In Damaraland mole-rats the sole reproducing female in the colony is also the longest lived. Therefore, if oxidative stress does impact the trade-off between reproduction and survival in general, this species may possess some form of enhanced defense. We assessed this relationship by comparing markers of oxidative damage (malondialdehyde, MDA; protein carbonyls, PC) and antioxidants (total antioxidant capacity, TAC; superoxide dismutase, SOD) in various tissues including plasma, erythrocytes, heart, liver, kidney and skeletal muscle between wild-caught reproductive and non-reproductive female Damaraland mole-rats. Reproductive females exhibited significantly lower levels of PC across all tissues, and lower levels of MDA in heart, kidney and liver relative to non-reproductive females. Levels of TAC and SOD did not differ significantly according to reproductive state. The reduction in oxidative damage in breeding females may be attributable to the unusual social structure of this species, as similar relationships have been observed between reproductive and non-reproductive eusocial insects.