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

Abstract

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.

LH responses to single doses of exogenous GnRH by social Mashona mole–rats:a continuum of socially induced infertility in the family Bathyergidae

“…Non-reproductive females are anovulatory, whereas non-reproductive males have reduced concentrations of testosterone in their urine and many produce sperm that are few in number and nonmotile (Faulkes et al 1990(Faulkes et al , 1991(Faulkes et al , 1994.…”

“…In these latter species, there are marked differences in basal LH concentrations between reproductive and non-reproductive females, and the response of the pituitary to a GnRH challenge (Faulkes et al 1990(Faulkes et al , 1991Bennett et al 1993).…”

Social status and sex independently influence androgen receptor expression in the eusocial naked mole-rat brain

“…Adult subordinates can become breeders given the appropriate social conditions, i.e., if a breeding member of the colony dies, or if the subordinate is removed from the colony and housed with an opposite sex mate (Brett, 1991;Faulkes et al, 1990;Margulis et al, 1995). This suggests the potential for extensive physiological, behavioral, and neural plasticity in adulthood.…”

Different ovarian responses to potential mates underlie species-specific breeding strategies in common marmoset and Goeldi's monkey

“…Social inhibition of reproductive hormones and direct effects of social subordination appear to contribute to this suppression of cortisol synthesis/secretion Saltzman et al, 1994bSaltzman et al, , 1996Saltzman et al, , 1998. In common marmosets as well as in other cooperatively breeding mammals, the inhibition of ovulation seems to be mediated by a specific neuroendocrine mechanism Damaraland mole-rat: Bennett et al, 1996; naked mole-rat: Faulkes et al, 1990). Due to this specific mechanism, ovulation inhibition occurs rapidly, repeatedly, and reversibly (Abbott et al, 1988;Faulkes and Abbott, 1997;French et al, 1984).…”