Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats, Heterocephalus glaber.

To investigate the endocrine cause of reproductive suppression in nonbreeding 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: less than 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: less than 0.5 ng/mg Cr, 232 samples from 64 females; plasma: less than 1.0 ng/ml, 7 samples from 6 females). Breeding females had higher (P less than 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: less than 0.5 ng/mg Cr, 11 females from 2 colonies; plasma: less than 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.

[1]  D. Coppola,et al.  The Physiology and Ecology of Puberty Modulation by Primer Pheromones , 1986 .

[2]  M. W. Hardisty Ecology and behaviour , 1979 .

[3]  J. Hodges,et al.  Sex steroids and their relationship to binding proteins in the serum of the marmoset monkey (Callithrix jacchus). , 1983, The Journal of endocrinology.

[4]  D. Abbott Behaviourally mediated suppression of reproduction in female primates , 1987 .

[5]  J. Hodges Monitoring changes in reproductive status , 1986 .

[6]  D. Kleiman,et al.  Endocrine correlates of behavioural oestrus in the female giant panda (Ailuropoda melaneleuca) and associated hormonal changes in the male. , 1982, Journal of reproduction and fertility.

[7]  C. G. Faulkes,et al.  Investigation of genetic diversity in wild colonies of naked mole-rats (Heterocephalus glaber) by DNA fingerprinting , 1990 .

[8]  Jon P. Rood,et al.  Mating relationships and breeding suppression in the dwarf mongoose , 1980, Animal Behaviour.

[9]  B. Lasley,et al.  Comparison of urinary oestrogen excretion in South American primates. , 1981, Journal of reproduction and fertility.

[10]  F. Bronson,et al.  A novel postcopulatory block of reproduction in white-footed mice. , 1988, Biology of reproduction.

[11]  I. W. Rowlands,et al.  Functional anatomy of the hystricomorph ovary , 1974 .

[12]  E. Diczfalusy,et al.  An improved in vitro bioassay method for measuring luteinizing hormone (LH) activity using mouse Leydig cell preparations. , 1974, Acta endocrinologica.

[13]  S. Wasser,et al.  Reproductive Suppression Among Female Mammals: Implications for Biomedicine and Sexual Selection Theory , 1983, The Quarterly Review of Biology.

[14]  M. McClintock 5 – Pheromonal Regulation of the Ovarian Cycle: Enhancement, Suppression, and Synchrony , 1983 .

[15]  Ronald R. Keiper Social structure. , 2003, The Veterinary clinics of North America. Equine practice.

[16]  J. Hodges,et al.  Controlled ovulation in the marmoset monkey (Callithrix jacchus) with human chorionic gonadotropin following prostaglandin-induced luteal regression. , 1987, Fertility and sterility.

[17]  W. Breed Effect of environment on ovarian activity of wild hopping mice (Notomys alexis). , 1976, Journal of Reproduction and Fertility.

[18]  S. Manuck,et al.  Adrenal responsiveness and social status in intact and ovariectomized Macaca fascicularis , 1986, American journal of primatology.

[19]  C. Snowdon,et al.  The effect of social environment on estrogen excretion, scent marking, and sociosexual behavior in tamarins (Saguinus oedipus) , 1984, American journal of primatology.

[20]  J. Jarvis,et al.  ENERGETICS OF SURVIVAL IN HETEROCEPHALUS GLABER (RUEPPELL), THE NAKED MOLE-RAT (RODENTIA: BATHYERGIDAE) , 1978 .

[21]  N. Bennett 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 , 1989 .

[22]  J. Hodges,et al.  Social status controls LH secretion and ovulation in female marmoset monkeys (Callithrix jacchus). , 1988, The Journal of endocrinology.