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.     

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.     

Ovarian growth and folliculogenesis in breeding and nonbreeding females of a social rodent,the Zambian common mole-rat,Cryptomys sp.

Zambian common mole-rats are subterranean rodents that live in families with only one female breeding. Her offspring remain in the parental nest and do not reproduce. Behavioral experiments (Burda, '95) demonstrated that their apparent “sterility” is based on incest avoidance and individual recognition of family members. To elucidate whether some kind of morphologically apparent ovarian suppression still takes place in daughters, ovaries of females of known age, weight, and reproductive histories were examined histologically and morphometrically. The body mass of old females (more than 3 years of age) begins to decrease, and the ovaries seem to begin to atrophy at the age of about 3–6 years. Ovaries in neonates exhibited primordial and primary follicles, sometimes clustered in nests. Ovaries of adult nonbreeding females expressed all stages of the follicular development up to tertiary follicles. Many unruptured luteinized follicles were present, but true corpora lutea as a morphological sign of ovulation were missing. Unruptured luteinized follicles also could be found (additionally to true corpora lutea) in ovaries of breeding females. The number of primordial follicles dropped rapidly during the first 2 years of age; the number of primary, secondary, and tertiary follicles was subject to individual variation; and there was no clear correlation with age or reproductive status. While a tendency to form accessory unruptured luteinized follicles may just reflect taxonomic affinities of bathyergids to hystricomorphs, the otherwise complete folliculogenesis in “sterile” daughters and the presence of unruptured luteinized follicles even in breeding females are further evidence that there is no hormonal suppression of the ovarial cycle. We suggest that ovulation in nonbreeding females is not actively suppressed by the breeding female, but instead that it is not released because the triggering mechanisms, most probably repeated copulation, are missing. J. Morphol. 237:33–41, 1998. © 1998 Wiley-Liss, Inc.     

Features of female reproductive senescence in tamarins (Saguinus spp.), a New World primate.

Cyclical changes in concentration of plasma progesterone, urinary oestrone-conjugates and urinary luteinizing hormone (LH) were compared in young and older cotton-top tamarins (Saguinus oedipus) and saddle-backed tamarins (S. fuscicollis). A group of six young adult tamarin females (4-5 years of age) was sampled over eight periods of 6-8 weeks and six older (14-20 years of age) females were sampled over thirteen periods. There was hormonal evidence of ovulation in all of the sampling periods for young females; in five of thirteen periods, older females displayed no evidence of ovulation. Of the six older females, two were anovulatory in one sampling period, while one female displayed no evidence of ovulation in any of three sampling periods. Generally, females over 17 years of age either did not ovulate or displayed abnormally long periods of moderate concentrations of progesterone and oestrone conjugates. Basal concentrations of LH differed in individuals, but were not always higher in older females. In contrast to patterns of reproductive senescence in other primates, older, anovulatory tamarins displayed moderate concentrations of urinary oestrone conjugates (5-50 micrograms/mg creatinine) and plasma progesterone (8-19 ng/ml), both of which are hormones of probable luteal origin in these species. This result suggests continued production of steroids by the luteal cells of the prominent interstitial gland in reproductively senescent tamarins. This suggestion was reinforced by histological examination of the ovaries of four older, anovulatory females; few primary follicles were found. Three females had no normal antral follicles, but all females had large luteal masses. The presence of functional luteal cells in the older ovaries, which do not experience regular follicular development, may distinguish ovarian ageing in New World primates from that of Old World primates.     

Profiles of oestradiol-17 beta and progesterone and follicular development during the reproductive season in mink (Mustela vison).

Plasma concentrations of oestradiol-17 beta and progesterone were studied in yearling mink females. The blood samples were collected from 2 March until 13 April in females not subjected to mating and in females mated on two consecutive days, early or late in the breeding season, or with 8-9 days between matings. Peaks in oestradiol-17 beta were recorded on the day of first mating, in relation to the second wave of growing follicles, and in early April, around the time when implantation should have occurred. Significant rises in progesterone were recorded from 17 to 21 March and were slightly later in females mated late in the season. Histological studies of ovaries from unmated females revealed that the number of 'active' follicles exceeded the number of degenerated or luteinized follicles until 7 April, after which the number of degenerated follicles increased rapidly. Degeneration was followed by luteinization. On 15 April, ovaries were collected from two females having 15 luteinized follicles each. These females had increased plasma concentrations of progesterone. These studies indicate that, in female mink, peaks in oestradiol-17 beta coincide with the first mating as a result of the copulatory act and that unmated females appear to experience a luteal phase in the absence of ovulation.     

Sex steroid correlates of female-specific colouration,behaviour and reproductive state in Lake Eyre dragon lizards, <Emphasis Type="Italic">Ctenophorus maculosus</Emphasis>

In some species, females develop bright colouration to signal reproductive status and exhibit behavioural repertoires to incite male courtship and/or reduce male harassment and forced copulation. Sex steroids, including progesterone and testosterone, potentially mediate female reproductive colouration and reproductive behaviour. We measured associations among plasma profiles of testosterone and progesterone with variation in colour expression and reproductive behaviour, including unique courtship rejection behaviours, in female Lake Eyre dragon lizards, (Ctenophorus maculosus). At onset of breeding, progesterone and testosterone increased with vitellogenesis, coincident with colour intensification and sexual receptivity, indicated by acceptance of copulations. As steroid levels peaked around the inferred ovulation time, maximal colour development occurred and sexual receptivity declined. When females were gravid and exhibited maximal mate rejection behaviours, progesterone levels remained consistently high, while testosterone exhibited a discrete second peak. At oviposition, significant declines in plasma steroid levels, fading of colouration and a dramatic decrease in male rejection behaviours co-occurred. Our results indicate a generally concordant association among steroid levels, colouration, behaviour and reproductive events. However, the prolonged elevation in progesterone and a second peak of testosterone was unrelated to reproductive state or further colour change, possibly suggesting selection on females to retain high steroid levels for inducing rejection behaviours.     

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.     

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 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.     

Psychobiology of sexual behavior in a whiptail lizard, Cnemidophorus inornatus

This study investigated the effects of social environment on gonadal recrudescence and sexual behavior in male and female Little Striped Whiptail lizards (Cnemidophorus inornatus). The presence of sexually active males facilitates ovarian recrudescence in conspecific females. Similarly, the presence of reproductively active females facilitates testicular recrudescence in conspecific males. Males housed with females, however, had lower average circulating concentrations of testosterone and dihydrotestosterone, and higher average concentrations of corticosterone compared to intact males housed in isolation. In other studies, the presence of reproductively active females partially restored courtship behavior in castrated males compared to castrated males housed in isolation. Despite the stimulatory effects of females on castrates, exogenous androgens are required for complete restoration of all components of sexual behavior in male C. inornatus. Females are receptive to male courtship and copulatory behavior only during the vitellogenic stages; females in previtellogenic or postovulatory ovarian stages aggressively reject male courtship advances. These findings demonstrate reciprocal effects of sexual behaviors of males and females upon each other's reproductive behavior and physiology.     

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.     

Sexual coloration, plasma concentrations of sex steroid hormones, and responses to courtship in the female keeled earless lizard (Holbrookia propinqua)

The reproductive condition, steroid hormone concentrations in the plasma, and behavior of bright and plain female Holbrookia propinqua were examined. Bright females performed significantly more aggressive rejection of courtship than plain females. Bright females were significantly more likely than plain females to have follicles larger than 5.0 mm or oviductal eggs; females with large follicles or oviductal eggs had significantly higher concentrations of progesterone and androgen than those with small follicles and lacking oviductal eggs. Plasma progesterone, androgen, and estradiol levels in the females studied behaviorally were significantly higher for the bright females than for the plain ones. Females undergoing rapid brightening were significantly more likely to be sexually receptive and copulate than were either plain or fully brightened females. The role of sex steroid hormones in coloration and behavior and the adaptive value of chromatic signalling by females are discussed.     

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 failure due to the entrapment of oocytes in luteinized follicles of the little bulldog bat (Noctilio albiventris)

The reproductive tracts of 112 female little bulldog bats collected around the onset of a breeding season in the Cauca Valley of Colombia were examined histologically. Of the 88 females with luteinizing/luteinized follicles or new CL, 72 carried tubal ova or uterine blastocysts and 16 were non-pregnant. In 14 of the latter follicle rupture had apparently failed to occur, and the oocyte or a collapsed zona pellucida was found within a luteinizing or luteinized follicle. These structures appeared to be functional because most of the affected bats demonstrated preferential stimulation of the ipsilateral oviduct and/or uterine horn. Two of these animals also had a second, older luteinized follicle which contained the remnants of an oocyte. None of these 14 bats exhibited the uterine modifications thought to be associated with a previous pregnancy or had prominent mammary glands. Such reproductive features were, in contrast, frequently demonstrated by other females in the population. These observations suggest that the luteinization of unruptured follicles may have occurred in prepubertal members of the population and reflect immaturity of the hypothalamo-pituitary -ovarian axis in these individuals.     

Plasma estradiol, testosterone, and progesterone levels during the ovulatory cycle of the skate (Raja erinacea)

Amounts of estradiol, testosterone, and progesterone in plasma were measured during the reproductive cycle of female Raja erinacea. Estradiol titers correlated directly with follicle size in females undergoing ovarian recrudescence, while highest concentrations were found in females with preovulatory follicles. These data indicate that as follicles grow, their steroidogenic capacity increases. In mature, nonspawning females, titers of estradiol and testosterone varied markedly. Progesterone was not detected in peripheral plasma of skates that did not produce eggs during the observation period. In females producing eggs, estradiol and testosterone predominated during the follicular phase of each spawning cycle. While estradiol and testosterone were elevated, progesterone was not detectable in the peripheral circulation. As ovulation and formation of capsules approached, plasma estradiol and testosterone declined to near baseline levels. Circulating progesterone rose sharply two days before encapsulation of ovulated eggs and remained elevated for only two days. On the day of encapsulation, concentrations of plasma progesterone had fallen to nearly baseline levels. Progesterone titers remained low throughout egg retention and oviposition. These measurements demonstrate that progesterone titers are elevated at specific times during the reproductive cycle of the skate and clearly suggest that progesterone is critically involved in events occurring at ovulation, encapsulation, and possibly oviposition.     

Ovarian function in ewes at the onset of the breeding season

Transrectal ultrasonography of ovaries was performed each day, during the expected transition from anoestrus to the breeding season (mid-August to early October), in six Western white-faced cross-bred ewes, to record ovarian antral follicles > or = 3 mm in size and luteal structures. Jugular blood samples were collected daily for radioimmunoassay (RIA) of follicle-stimulating hormone (FSH), oestradiol and progesterone. The first ovulation of the breeding season was followed by the full-length oestrous cycle in all ewes studied. Prior to the ovulation, all ewes exhibited a distinct increase in circulating concentrations of progesterone, yet no corpora lutea (CL) were detected and luteinized unovulated follicles were detected in only three ewes. Secretion of FSH was not affected by the cessation of anoestrus and peaks of episodic FSH fluctuations were associated with the emergence of ovarian follicular waves (follicles growing from 3 to > or = 5 mm). During the 17 days prior to the first ovulation of the breeding season, there were no apparent changes in the pattern of emergence of follicular waves. Mean daily numbers of small antral follicles (not growing beyond 3 mm in diameter) declined (P < 0.05) after the first ovulation. The ovulation rate, maximal total and mean luteal volumes and maximal serum progesterone concentrations, but not mean diameters of ovulatory follicles, were ostensibly lower during the first oestrous cycle of the breeding season compared with the mid-breeding season of Western white-faced ewes. Oestradiol secretion by ovarian follicles appeared to be fully restored, compared with anoestrous ewes, but it was not synchronized with the growth of the largest antral follicles of waves until after the beginning of the first oestrous cycle. An increase in progesterone secretion preceding the first ovulation of the breeding season does not result, as previously suggested, from the ovulation of immature ovarian follicles and short-lived CL, but progesterone may be produced by luteinized unovulated follicles and/or interstitial tissue of unknown origin. This increase in serum concentrations of progesterone does not alter the pattern of follicular wave development, hence it seems to be important mainly for inducing oestrous behaviour, synchronizing it with the preovulatory surge of luteinizing hormone (LH), and preventing premature luteolysis during the ensuing luteal phase. Progesterone may also enhance ovarian follicular responsiveness to circulating gonadotropins through a local mechanism.     

Reproduction elevates the corticosterone stress response in common fruit bats

Changes in reproductive state or the environment may affect the sensitivity of the hypothalamic-pituitary-andrenal (HPA) axis. However, little is known about the dynamics of the resulting corticosteroid stress response, in particular in tropical mammals. In this study, we address the modulation of corticosterone release in response to different reproductive conditions and seasonality in 326 free-living common fruit-eating bats (Artibeus jamaicensis) on Barro Colorado Island in Panama during dry and wet seasons. We present strong evidence that stress sensitivity is primarily modulated by reproductive condition. In reproductively active females, corticosterone increases were more rapid and reached higher levels, but also decreased significantly faster than in inactive females. The corticosterone response was weaker in reproducing males than in females and delayed compared to non-reproductive males. Testes volume in reproductively active males was negatively correlated with corticosterone concentrations. Our findings suggest differentiated dynamics in the corticosterone stress response between sexes, potentially reflecting conflicting ecological demands. In females, a strong acute corticosterone response may represent high stress- and risk-sensitivity that facilitates escape and thus helps to protect reproduction. In males, suppression during reproductive activity could reflect lowered stress sensitivity to avoid chronically elevated corticosterone levels in times of frequent aggressive and therefore costly inter-male encounters.     

Olfactory environment and coitus-induced ovulation and/or luteinization in the cyclic female rat

The role of pheromones in the process of ovulation and/or luteinization induced by coitus was studied in female rats primed with estradiol benzoate (EB) and early mated during 4-day cycles. The effects of coitus were evaluated by using 1) the proportion of females displaying postovulatory corpora lutea (POCL) and/or luteinized unruptured follicles (LUF), and 2) the ovulation coefficient (OC) computed in each female by dividing the number of POCL by the total number of POCL and LUF. A greater proportion of females displayed ovulation and/or luteinization following coitus than those given EB only. This proportion was slightly but significantly increased when females were exposed to bedding soiled with 5 ml of male urine prior to mating, an effect prevented by complete olfactory bulbectomy. However, in the females given EB only, the pheromonal stimulus remained inefficient. Weak ovulatory effects of coitus, as assessed by low OC values, were noted whether the females were exposed or not to male urine. An increase in the frequency of lordosis occurred after olfactory bulbectomy, but no significant changes in OC values were observed in this experimental group. It was concluded that pheromones, act as a primer on the neuroendocrine mechanisms governing ovulation in the cyclic female rat, as in other species of rodents.     

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 pattern of reproduction in female Columbian black-tailed deer, Odocoileus hemionus columbianus.

Ovarian cycles and the pattern of reproduction in female black-tailed deer in British Columbia were ascertained largely through examination of the ovaries from 444 females. Cyclic development and degeneration of single follicles of ovulatory size occurred several weeks before first ovulation. As the breeding season approached, a second or third large follicle developed in each cycle but in 48% of adult females the follicles were at different stages of maturation. Those failing to rupture at first ovulation luteinized 1 to 2 days thereafter. The first ovulation of the season, in November, never resulted in a lasting pregnancy even though some ova were penetrated by spermatozoa and began to cleave. First ovulation was apparently 'silent' in five of seven females for their ova lacked spermatozoa. Of sixty-one pregnant females, fifty-nine conceived at second ovulation; the other two conceived at subsequent ovulations more widely spaced than the 8- to 9-day interval between first and second ovulations. The synchrony of ovulatory cycles among adult females was such that half of them ovulated for the second time in a span of 7 or 8 days. Primary CL that formed after first ovulation grew to an average maximum volume of only about 45 mm3, whereas those originating at second ovulation grew to twice that size within 5 to 8 days. First generation CL shrank from 35 mm3 to 10 mm3 within 2 days. They disappeared within 18 months but corpora albicantia persisted for the life of the female. The possible ecological significance of the reproductive pattern is discussed.