Social status controls LH secretion and ovulation in female marmoset monkeys (Callithrix jacchus)

Abstract

The suppression of ovulation in subordinate female marmosets was associated with suppressed pituitary LH secretion and reduced pituitary LH response to gonadotrophin-releasing hormone (GnRH). In subordinate females, basal plasma LH concentrations were commonly below 2 IU/l (n = 5) (maximum 10.7 IU/l). Plasma oestrogen concentrations were similarly low (maximum 0.62 nmol/l) and plasma progesterone concentrations of below 30 nmol/l confirmed the anovulatory condition. This infertility condition was rapidly reversed when subordinate females (n = 5) were removed from their social groups and housed singly, when plasma LH (maximum 140.0 IU/l) and oestrogen (maximum 7.84 nmol/l) concentrations increased preceding ovulation. Infertility was rapidly reimposed when these singly housed females were re-introduced to subordinate status in new social groups, when plasma LH concentrations fell to their previous low values within 4 days; no ovulation occurred thereafter. Plasma oestrogen levels also fell, but less dramatically. The luteal phases of three of the subordinate females were shortened following the re-instatement of subordinate status. The maximum LH response of subordinate females to the highest dose of GnRH (200 ng) was only 19.1 +/- 6.7 IU/l (mean +/- S.E.M.; n = 8): this contrasted with that in dominant females in either the follicular phase (40.0 +/- 13.3 IU/l; n = 6) or the luteal phase (126.7 +/- 24.9 IU/l; n = 10) of the ovarian cycle. These results suggest that the social suppression of fertility in subordinate female marmosets is mediated by impaired hypothalamic GnRH secretion. Such an immediate and precise behavioural control of LH secretion and ovulation is without equal in anthropoid primates.

Social suppression of cortisol in female marmosets: Role of luteinizing hormone/chorionic gonadotropin

“…Furthermore, although leuprolide markedly suppressed both basal and GnRH-stimulated CG concentrations in ovariectomized animals, it did not alter either basal or ACTH-stimulated cortisol concentrations in these females. These results are consistent with Wndings by Kendrick and Dixson (1985a,b) that plasma cortisol concentrations of ovariectomized, estrogen-treated marmosets were unchanged at 2 and 24 h after GnRH injection, which stimulates release of CG in these monkeys (Abbott et al, 1988;Hodges, 1979). In female marmosets, therefore, CG appears to increase cortisol secretion only during the periovulatory phase of the ovarian cycle.…”

“…4), as previously reported for this species (Abbott et al, 1988;Lunn et al, 1992;Saltzman et al, 1998). Basal CG concentrations of ovx females were signiWcantly higher than those of intact females in the follicular phase …”

“…The results indicate that CG stimulates cyclical elevations in endogenous cortisol concentrations, but that this eVect is small in magnitude and is dependent upon, and may be mediated by, ovarian hormones. Thus, our results suggest that social suppression of CG may not play a major role in mediating chronic reductions of basal cortisol concentrations in anovulatory, subordinate female marmosets, which exhibit low, acyclic concentrations of estrogen and progesterone (Abbott et al, 1981(Abbott et al, , 1988Saltzman et al, 1998).…”

“…Subordinate females are often anovulatory and hypoestrogenemic as a result of inhibited hypophyseal secretion of CG (Abbott et al, 1981a,b;Saltzman et al, 1998), which has been shown recently to be the major luteinizing gonadotropin secreted by the pituitary in this species and possibly other New World primates (Gromoll et al, 2003;Müller et al, 2004b). Reproductive suppression can persist for months or even years, but is reversed rapidly following separation of the subordinate female from her dominant female groupmate (Abbott and George, 1991;Abbott et al, 1988).…”

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

“…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). This allows females to react rapidly to changes in the social environment, for example when a new breeding position becomes available due to the loss of the dominant female.…”