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

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

Reproductive tracts and spermatozoa from reproductively active and reproductively suppressed non-breeding males from two species of eusocial African mole-rats Cryptomys damarensis and Heterocephalus glaber were examined. In two captive colonies of Heterocephalus glaber, reproductive tracts from seven non-breeding males removed from their colonies, and housed singly for 5–6 weeks to cause reproductive activation, were compared with reproductive tracts from seven non-breeding males. The body weight of the separated, reproductively active males increased significantly (P < 0.01), and the mean testis weights relative to body weight of the reproductively active males were significantly larger (P < 0.05) than those of non-breeding males. The number of spermatozoa, in one half of the reproductive tract, was higher in active males than in non-breeding males (mean ± sem: 8.59 × 10⁶ ± 2.69 × 10⁶ versus 1.78 × 10⁶ ± 1.43 × 10⁶, respectively; P < 0.05). In addition, six of the seven reproductively active males, but only two of seven non-breeding males, had motile spermatozoa. A total of 28 wild Cryptomys damarensis from two colonies were examined in the field. The testis weights relative to body weight of breeding males (n = 7) were higher than those of non-breeding males (n = 19; P < 0.01), but the number of spermatozoa did not differ significantly between the two groups (0.13 × 10⁶ ± 0.06 × 10⁶, n=7 versus 0.29 × 10⁶ ± 0.14 × 10⁶, n = 21, respectively). Breeding and non-breeding males produced similar numbers of motile spermatozoa. These results suggest that socially induced reproductive suppression of males differs in these two species of African mole-rats.

Summary. To investigate possible differential pituitary secretion of LH in breeding and non-breeding female naked mole-rats, the LH responses to administration of exogenous GnRH were measured in 55 females from 20 captive colonies. Single doses of 0·1, 0·5 or 1·0 μg GnRH produced a significant rise in plasma LH concentrations 20 min after s.c. injection in breeding and non-breeding females at all doses (P < 0·001).

While at the highest dose of 1·0 μg there was no difference in the LH response between breeding and non-breeding females, as the dose was lowered there was a progressive decline in the LH response in non-breeding females such that, at the 0·1 μg dose, GnRH produced only a small, but significant, increase in plasma LH (1·3 ± 0·2 to 2·9 ± 0·5 mi.u./ml, N = 5) compared with breeding females (3·4 ± 0·8 to 9·6 ± 2·0 mi.u./ml, N = 6). The LH responses of the latter were not significantly reduced at the lower doses of GnRH.

The apparent lack of sensitivity to low doses of exogenous GnRH in non-breeding females was reversed by 4 consecutive 1-h injections of 0·1 μg, which produced a rise in LH from 1·2 ± 0·2 to 9·0 ± 0·2 mi.u./ml (N = 4), comparable to that of breeding females given a single injection of 0·1 μg GnRH.

These results suggest that the anterior pituitary in non-breeding female naked mole-rats is less sensitive to low doses of exogenous GnRH than in breeding females, possibly due to a lack of priming by endogenous GnRH. Therefore, the socially-induced block to ovulation in non-breeding female naked mole-rats may be due to inhibition of hypothalamic GnRH secretion.

Keywords: naked mole-rat; reproductive suppression; LH; pituitary; GnRH

Pituitary function in reproductive and nonreproductive colony members of Damaraland mole-rats, Cryptomys damarensis, was investigated by measuring the LH responses to single doses of 2 μg exogenous GnRH and physiological saline in 29 females and 37 males (31 of these animals from two entire colonies). In females, basal LH concentrations were significantly greater in reproductive (n = 9) than in nonreproductive animals (n = 11): 7.6 ± 1.0 versus 4.3 ± 0.6 miu ml⁻¹, respectively (P < 0.001). Reproductive females had a significantly greater LH response to 2.0 μg GnRH (7.6 ± 1.0 to 37.7 ± 6.2 miu ml⁻¹; n = 9) than did nonreproductive females (4.3 ± 0.6 to 11.8 ± 1.0 miu ml⁻¹; n = 11, P < 0.001). In contrast, there was no significant difference in basal LH concentrations between reproductive (n = 8) and nonreproductive males (n = 20): 5.3 ± 4.3 versus 3.2 ± 1.2 miu ml⁻¹, respectively. There was also no difference in LH response to the administration of 2.0 μg GnRH between reproductive and nonreproductive males (5.3 ± 4.3 to 21.8 ± 8.6 miu ml⁻¹; n = 8; versus 3.2 ± 1.2 to 21.1 ± 8.5 miu ml⁻¹; n = 21; P = 0.5). When the results from the two entire colonies were analysed separately, LH responses to GnRH in the 11 nonreproductive females were less than in the two reproductive females. In contrast, the response of two reproductive males in the colonies did not differ from that of 16 nonreproductive males, although these latter comparisons could not be validated statistically. The following conclusions were made. First, the anterior pituitary of nonreproductive female mole-rats is less sensitive to GnRH than is that of reproductive females, possibly resulting from a lack of priming by endogenous GnRH. Second, the hypothalamic–pituitary axis is more active in reproductive females, giving rise to higher concentrations of LH in plasma. Thus suppression in nonreproductive females is due to inhibition of GnRH rendering them temporarily infertile. Third, the lack of differentiation in response to GnRH in males suggests that nonreproductive males are behaviourally inhibited from breeding.