Reproductive status affects the expression of prolactin receptor mRNA in the brain of female Damaraland mole-rats

Abstract

The eusocial Damaraland mole-rat (Fukomys damarensis) represents an extreme example of reproductive skew, in that reproduction is completely blocked in female subordinate group members. It is thought that in these animals normal GnRH secretion from the hypothalamus is disrupted. Prolactin, a peptide hormone secreted from the anterior pituitary gland, has been implicated in a wide variety of functions. Well documented in rodents is its role in mediating lactational infertility. Elevated circulating prolactin levels, such as during lactation, are associated with reduced GnRH release into the portal blood and with a reduction in the frequency and amplitude of LH pulses. The present study aimed at investigating whether such a mechanism could act in reproductively suppressed female Damaraland mole-rats. By means of in situ hybridisation we studied the distribution and gene expression of the prolactin receptor (Prlr) in wild-caught female Damaraland mole-rats with different reproductive status. Substantial Prlr expression was found in several brain regions, with highest levels in the choroid plexus and moderate expression in the preoptic and tuberal hypothalamus. While in reproductive and non-reproductive females plasma prolactin levels were very low and not significantly different, quantification of the Prlr hybridisation signal revealed significant differences in relation to reproductive status. Reproductively suppressed females had increased expression of Prlr in the choroid plexus and in the arcuate nucleus (ARC) when compared to reproductive females. This suggests higher local prolactin levels in the brain of suppressed females. Together with previous findings, it could indicate that prolactin inhibits ARC kisspeptin neurons, which then would lead to reduced activation of GnRH neurons in such females.

The best of both worlds: no apparent trade-off between immunity and reproduction in two group-living African mole-rat species

“…Physiologically reproductive suppression in the NBFs presents itself in the form of NBFs exhibiting low circulating basal luteinizing hormone (LH) concentrations and a muchreduced response to an exogenous gonadotropin-releasing hormone (GnRH) challenge in comparison with BFs [70,71]. In addition, the varied expression of potent regulators of gonadotropin release, namely the RFamide peptides kisspeptin (Kiss1) and RFamide-related peptide-3 (RFRP-3), has been implicated in the reduced fertility and exhibiting of sexual behaviours of NBFs compared with BFs [72][73][74][75]. This ensures that if unrelated males enter a stable group (consisting of an established and breeding BF and breeding male pair) when ecological constraints are relaxed (such as good rainfall events), multiple BFs do not arise [76,77].…”

Socially Induced Infertility in Naked and Damaraland Mole-Rats: A Tale of Two Mechanisms of Social Suppression

“…Nevertheless, there are elevated levels of prolactin receptor gene expression in the choroid plexus and in the arcuate nucleus of non-breeding female Damaraland mole-rats when compared to that of breeding females, which suggests higher local prolactin levels in the brain. Such elevated brain prolactin levels could inhibit kisspeptin neuron activity in the arcuate nucleus and thereby contribute to the reduced activation of GnRH neurons and reduced LH release from the pituitary [ 67 , 88 ]. Kisspeptin expression in the arcuate nucleus is known to be suppressed by elevated prolactin levels such as during lactation [ 89 ].…”

Reproductive status-dependent dynorphin and neurokinin B gene expression in female Damaraland mole-rats

“…Brain mass did not differ in relation to social status (t = 1.24, df = 16, P = 0.23). The same brains were used in a previous study investigating the expression of the prolactin receptor (Voigt and Bennett 2018b).…”