The role of chemical cues in mediating the reproductive suppression of nonbreeding males and females in colonies of naked mole-rats (Heterocephalus glaber) was examined by comparing reproductive activation in isolated nonbreeders with that of isolated nonbreeders maintained in olfactory and gustatory contact with their parent colony. Animals were either removed from their colony and paired directly with a member of the opposite sex from the same colony, or were removed, housed singly for 40 days, and then paired with a member of the opposite sex from the same parent colony that had also been housed singly for 40 days. Approximately half of these separated animals received a daily transfer of soiled bedding and litter from their parent colony. In females, there was no significant difference between the control and bedding transfer group, in the time taken from separation to the first sustained increase of urinary progesterone above 2 ng mg−1 Cr indicative of the luteal phase of an ovarian cycle (7.8 ± 2.6 versus 9.4 ± 2.0 days, respectively). In both control and bedding transfer groups, singly-housed females commenced ovarian cyclicity, revealing that the presence of a male was not required for reproductive activation and ovulation. In males, concentrations of both urinary testosterone and plasma LH increased after separation from their parent colonies in both control and bedding transfer groups, to reach values equivalent to those of breeding males. The mean time between separation and a rise in urinary testosterone to amounts observed in breeding males (24 ng mg−1 Cr) was not significantly different between control and bedding transfer groups (5.0 ± 1.4 versus 4.4 ± 1.7 days, respectively). There was no significant difference in either plasma LH or urinary testosterone concentrations between the control and bedding transfer groups before or after separation from their parent colonies. These results suggest that primer pheromones from urine, or other secretions contained in soiled bedding and litter, do not play a major role in the suppression of reproduction in nonbreeding male or female naked mole-rats.
C. G. Faulkes and D. H. Abbott
Summary. 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 < 0·05). Concentrations 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 < 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. The breeding female may therefore control the reproductive physiology of both breeding and non-breeding males in colonies of naked mole-rats.
Keywords: reproductive suppression; naked mole-rats; hystricomorph rodent; testosterone; luteinizing hormone
D. H. Abbott and J. P. Hearn
Summary. Measurements of growth, plasma progesterone and testosterone levels, and copulatory behaviour were obtained from captive marmosets from birth until 600–800 days of age. Body weight and knee-to-heel length were similar for both sexes. Males exhibited a neonatal testosterone surge from 15–100 days and testosterone levels began to rise again, coincident with the growth of the testis, at about 250 days. The males were copulating by 400–500 days of age. Paired females were apparently ovulating and able to conceive from about 400 days. In peer groups, only the dominant female became pregnant, because subordinate females failed to ovulate.
C. G. Faulkes, D. H. Abbott and J. U. M. Jarvis
Summary. To investigate possible anatomical and endocrine differences between breeding and non-breeding male naked mole-rats, 113 animals from 24 captive and 4 wild colonies were studied.
While breeding males had larger reproductive tract masses compared to non-breeders relative to body mass (P < 0·01), spermatogenesis was active in all of the non-breeding males examined histologically (n = 9) and spermatozoa were present in the epididymides. Compared with non-breeders, breeding males had significantly higher urinary testosterone concentrations (mean ± s.e.m.: 23·8 ± 2·3 vs 5·2 ± 1·4 ng/mg Cr respectively; P < 0·001), and plasma LH (10·7 ± 1·7 vs 5·0 ± 0·8 mi.u./ml respectively; P < 0·01). Single doses of 0·1, 0·5 or 1·0 μg GnRH produced a significant rise in plasma LH concentrations 20 min after s.c. injection in breeding and non-breeding males at all doses (P < 0·001). However, there were differences in the magnitude of the LH response following administration of GnRH between breeding and non-breeding males, with non-breeding males showing a dose–response and having lower plasma LH concentrations 20 min after a single injection of 0·1 or 0·5 μg (P < 0·05), but not 1·0 μg, GnRH. This apparent lack of pituitary sensitivity of non-breeding males to single doses of exogenous GnRH was reversed by 4 consecutive injections of 0·5 μg GnRH at hourly intervals, suggesting that the reduced sensitivity may be the result of insufficient priming of the pituitary by endogenous GnRH.
These results indicate that, despite the fact that non-breeding males were apparently producing mature gametes, clear endocrine deficiencies existed in male naked mole-rats.
Keywords: reproductive suppression; naked mole-rats; hystricomorph rodent; testosterone; LH
J. Barrett, D. H. Abbott and L. M. George
Subordinate female marmoset monkeys remain anovulatory and have low plasma concentrations of luteinizing hormone (LH) when maintained with their dominant females. Olfactory cues from the dominant female have been implicated in maintaining this reproductive suppression. Subordinate females that received either ablation of the vomeronasal organ (an accessory olfactory organ; n = 3), ablation of the main olfactory epithelium (n = 4), or both lesions (n = 5) did not ovulate in the following 7 weeks while housed with their dominant female. Plasma LH concentrations following either or both lesions were similar to pre-lesion concentrations. Olfactory lesions (verified by histological and behavioural trials) did not impair reproductive activity, as olfactory-lesioned dominant females underwent ovarian cycles of similar duration to intact dominant females. Lesioned subordinate females (n = 6), maintained in visual-only contact with their dominant female and group ovulated 29.1 ± 9.3 days (mean ± sem) after physical separation from their dominant females; this first onset of ovulation was significantly delayed (P < 0.05) compared with intact subordinate females completely isolated from their dominant females and group (10.8 ± 1.3 days, n = 8). Behavioural and visual cues together with olfaction all appear to play important roles in maintaining the suppression of ovulation in subordinate female marmoset monkeys.
J. Barrett, D. H. Abbott and L. M. George
Summary. Pheromonal signals from the dominant female marmoset monkey were implicated in maintaining the suppression of LH secretion and ovulation in socially subordinate females. When subordinate, and reproductively suppressed, female marmoset monkeys were removed from their group without scent contact with their dominant females, subordinate females in control group 1 (N = 8) and control group 2 (N = 5), ovulated 10·8 ± 1·4 days and 10·4 ± 0·8 days respectively (mean ± s.e.m.) after separation. Subordinate females (N = 8) removed from their dominant female and group, but maintained in scent contact only with their dominant females, showed a delay in the onset of ovulation (31·0 ± 6·4 days) compared with control groups 1 and 2. Plasma LH concentrations of subordinate females during the scent transfer phase were lower than in controls without scent transfer and comparable to those seen whilst the females were subordinates in groups. Contact of subordinate females with olfactory stimuli from dominant females therefore maintains the suppression of both LH secretion and ovulation in socially subordinate female marmosets. Such pheromonal cues provide evidence of a quantifiable link between dominant female marmosets and the maintenance of physiological suppression of reproduction in their female subordinates.
Keywords: marmoset; reproductive suppression; pheromones; ovulation; progesterone
C. G. Faulkes, D. H. Abbott and J. U. M. Jarvis
Summary. To investigate the endocrine cause of reproductive suppression in non-breeding female naked mole-rats, animals from 35 colonies were studied in captivity. Urinary and plasma progesterone concentrations were elevated in pregnant females (urine: 10·0–148·4 ng/mg Cr, 27 samples from 8 females; plasma: 3·6–30·0 ng/ml, 5 samples from 5 females; Days 21–40 of pregnancy) and cyclic breeding females (urine: 0·5–97·8 ng/mg Cr, 146 samples from 7 females; plasma: < 1·0–35·4 ng/ml, 25 samples from 7 females). The latter group showed cyclic patterns of urinary progesterone, indicating a mean ovarian cycle length of 34·4 ± 1·6 days (mean ± s.e.m.) with a follicular phase of 6·0 ± 0·6 days and a luteal phase of 27·5 ± 1·3 days (19 cycles from 9 breeding females). In non-breeding females urinary and plasma progesterone values were undetectable (urine: < 0·5 ng/mg Cr, 232 samples from 64 females; plasma: < 1·0 ng/ml, 7 samples from 6 females). Breeding females had higher (P < 0·001) plasma LH concentrations (3·0 ± 0·2 mi.u./ml, 73 samples from 24 females) than did non-breeding females (1·6 ± 0·1 mi.u./ml, 57 samples from 44 females). Urinary and plasma progesterone concentrations in non-breeding females from wild colonies situated near Mtito Andei, Kenya, were either below the assay sensitivity limit (urine: < 0·5 ng/mg Cr, 11 females from 2 colonies; plasma: < 1·0 ng/ml, 25 females from 4 colonies), or very low (plasma: 1·6 ± 0·6 ng/ml, 15 females from 4 colonies).
In captivity, non-breeding females removed from their colonies (i.e. the dominant breeding female) and either paired directly with a non-breeding male (N = 2), or removed and housed singly for 6 weeks before pairing with a non-breeding male (N = 5) may develop a perforate vagina for the first time in as little as 7 days. Urinary progesterone concentrations rose above 2·0 ng/mg Cr (indicative of a luteal phase) for the first time 8·0 ± 1·9 days after being separated.
These results suggest that ovulation is suppressed in subordinate non-breeding female naked mole-rats in captive and wild colonies, and show that plasma LH concentrations are significantly lower in these non-breeding females. This reproductive block in non-breeding females is readily reversible if the social factors suppressing reproduction are removed.
Keywords: reproductive suppression; naked mole-rats; ovarian cycles; hystricomorph rodent
J. B. Carroll, D. H. Abbott, L. M. George, J. E. Hindle and R. D. Martin
Summary. A non-invasive study of urinary hormones in 6 captive female Goeldi's monkeys provided accurate information on reproductive function. Conjugated oestrone accounted for 80–85% of the urinary oestrone and oestradiol measured. Radioimmunoassay measurements of conjugated oestrone provided a reliable indicator of cyclic ovarian function (mean cycle length: 24·1 ± 0·9 days; n = 9) and pregnancy (gestation: 145, 155 days; n = 2). Measurements of urinary progesterone and pregnanediol glucuronide were only reliable as indicators of ovarian cyclicity. Elevations in urinary conjugated oestrone coincided with luteal-phase elevations of urinary progesterone and pregnanediol glucuronide. Urinary LH concentrations provided no indication of pituitary activity. However, the frequencies of female sexual solicitations of males were maximal when oestrone conjugate concentrations rose, suggesting a peri-ovulatory period. Ovulation was suppressed in 1 of 3 subordinate females housed in male–female–female trios.
Keywords: monkey; oestrogen; progesterone; pregnanediol glucuronide, LH; ovarian cycle; pregnancy; urinary hormones
Clare A Everett, Catherine A Auchincloss, Matthew H Kaufman, Catherine M Abbott and John D West
A high proportion of LT/Sv strain oocytes arrest in meiotic metaphase I (MI) and are ovulated as diploid primary oocytes rather than haploid secondary oocytes. (Mus musculus castaneus × LT/SvKau)F1 × LT/SvKau backcross females were analysed for the proportion of oocytes that arrested in MI and typed by PCR for a panel of microsatellite DNA sequences (simple sequence repeat polymorphisms) that differed between strain LT/SvKau and M. m. castaneus. This provided a whole genome scan of 86 genetic markers distributed over all 19 autosomes and the X chromosome, and revealed genetic linkage of the MI arrest phenotype to markers on chromosomes 1 and 9. Identification of these two chromosomal regions should facilitate the identification of genes involved in mammalian oocyte maturation and the control of meiosis.
A. S. McNeilly, D. H. Abbott, S. F. Lunn, P. C. Chambers and J. P. Hearn
Summary. A heterologous double-antibody radioimmunoassay was used to measure plasma prolactin concentrations in 27 marmosets. The assay was valid for the marmoset because plasma levels of prolactin were increased in response to TRH and metoclopramide and suppressed in response to bromocriptine treatment.
During the cycle there were no consistent changes in plasma prolactin concentrations. During lactation mothers suckling single or twin infants had higher prolactin levels than did non-suckling females and levels were highest with twins. No statistically significant delay in the resumption of ovulation post partum was observed for the suckling and non-suckling females; conception occurred in all but one marmoset by 70 days post partum.
These results show that neither the suckling stimulus nor high levels of prolactin post partum delay the return of ovulation and fertility in the common marmoset, a result in contrast to that for all other primate species so far investigated.