The Naked and Damaraland Mole-Rats: History
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Contributor:
Nigel C. Bennett
,
Christopher G. Faulkes
,
Cornelia Voigt

The naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Fukomys damarensis) possess extreme reproductive skew with a single reproductive female responsible for reproduction.

  • neuroendocrine
  • behavior
  • physiology

1. Introduction

The rodent moles of the family Bathyergidae provide an incredible opportunity to dissect the numerous reproductive strategies which are operative in this diverse family and that possess a broad spectrum of social organization [1]. Reproduction is a costly and lengthy process, requiring the growth and maturation of the gonads, courtship and copulation; followed by pregnancy and ultimately parturition in females, but it also is crucial for passing on copies of genetic material to the next generation. Several species of subterranean rodents are solitary, these animals are usually very territorial and exceptionally aggressive towards any conspecific or heterospecific mole-rats that enter the tunnel system [1]. The only time that pairing occurs is during the breeding season; outside of this period, any individuals entering the burrow system are usually killed [1]. Consequently, the majority of studies investigating the patterns of reproduction in solitary dwelling species of subterranean mammals have come from post-mortem studies in which specimens of both sexes have been collected on a monthly basis to investigate their reproductive condition. This usually involves the weighing and measuring of the dimensions of gonads, looking for the presence or absence of embryos, as well as assessing the numbers and types of follicles in the ovaries and the presence or absence of spermatozoa in the testes (see [2] review).

2. The Scenario in the Naked Mole-Rat

In the naked mole-rat, reproductive suppression occurs in both non-breeding males and females, the members of which remain philopatric to the colony and are physiologically suppressed from reproducing [3][4][5][6]. Socially induced infertility in non-breeding males is unique and has currently not been reported in any other cooperatively breeding mammal [3][6].
The ovaries and uterine horns of non-breeding female naked mole-rats are much smaller than their breeding counterparts, and their ovaries show little follicular activity when compared to the ovaries of the breeding females. Their ovaries are pre-pubescent in appearance, with few, if any, follicles [7]. While the majority of social mole-rat species are induced ovulators, the naked mole-rat is a spontaneous ovulator [5]. Endocrine studies support the findings on ovarian activity, such that the non-breeding females have low, or non-detectable urinary oestrogen and progesterone concentrations, and furthermore, no cyclical peaks in progesterone occur, indicative of anovulation [4][8]. The absence of a follicular cycle and subsequent ovulation appears to be due to very low concentrations of circulating LH arising from the anterior pituitary. Reproductive suppression in non-breeding naked mole-rats is believed to be the consequence of a reduction or disruption of GnRH release or potentially down regulation of GnRH receptors on the pituitary itself [6]. The ovaries of non-breeding female naked mole-rats are prepubescent while these animals remain in the colony with the breeding female. If a female is taken out of the colony and housed or paired with a male ovarian activation arises with the subsequent reinstatement of follicular development and ovulation [4]. Ovarian activity in a non-breeding female can result from a challenge to the breeding female from a high-ranking subordinate female in a colony or following dispersal and outbreeding in the field [9]. In captivity, a new breeding female frequently arises from in the natal colony through succession as a result of social queuing. Non-breeders may be more reproductively primed than other subordinates and challenge the breeding female, or even kill the existing breeding female, even if this involves mating with an adult sibling [10]. Laboratory studies have reported that an outbreeding reproductive strategy is the preferred option in this species [11][12], and this has been confirmed from studies of wild colonies in the field [9].
The neuroendocrine mechanisms leading to the onset of reproductive activity in female subordinate naked mole-rats are still not well-understood. In spontaneously ovulating mammals, the positive feedback effect of increased ovarian oestradiol production leads to GnRH secretion from the hypothalamus, which stimulates the preovulatory LH surge from the anterior pituitary. The neuropeptides kisspeptin (encoded by the Kiss1 gene) and RFamide-related peptide-3 (RFRP-3, encoded by the Rfrp gene) constitute important regulators of GnRH release, but with opposing effects. Kisspeptin activates GnRH neurons and is essential for normal reproductive activity and the timing of puberty onset. RFRP-3, on the other hand, is thought to be the mammalian homolog of the gonadotropin-inhibiting hormone (GnIH) in birds, which inhibits GnRH neuronal activity and gonadotropin release for review, see [13]. Kisspeptin neurons reside in two main regions of the hypothalamus: the anteroventral periventricular nucleus (AVPV) and the arcuate nucleus (ARC). In female rodents, oestradiol stimulates kisspeptin neurons in the AVPV while those in the ARC are inhibited. This positive and negative feedback effect of oestradiol is mediated by oestrogen receptor α (ERα), which is co-expressed in both kisspeptin neuron populations [14]. Kisspeptin neurons in the AVPV send projections to GnRH neurons in the rostral preoptic area and constitute the target for oestradiol to induce the preovulatory GnRH/LH surge [15][16]. The characterisation of these neuropeptides opens up a whole new field of research for investigating the control of reproduction in socially suppressed mammals. However, in naked mole-rats, only a few investigations have been undertaken to date. Zhou, et al. [17], have found that non-breeding female naked mole-rats possess significantly fewer kisspeptin immunoreactive cells in the AVPV when compared to breeding females. No such differences occur in the ARC. This suggests as with other female rodents, the AVPV neuron population is involved in the pre-ovulatory LH surge in naked mole-rats. Moreover, it implies that triggering the activation of these kisspeptin neurons is essential for the onset of reproductive activity. However, more recent studies have found evidence that RFRP-3 plays a crucial role in suppressing puberty onset [18].
Reproductively quiescent females show increased RFRP-3 expression in the dorsomedial hypothalamus when compared to reproductively active females. Furthermore, exogenous RFRP-3 prevents puberty onset in subordinate females that are removed from their natal colony and therefore given the opportunity to enter puberty [19]. Using quantitative PCR, Faykoo-Martinez, et al. [18], have identified several candidate genes, including those of the kisspeptin signaling pathway, which show a differential expression pattern in relation to reproductive status. However, more research is needed to identify the exact roles of RFRP-3 and kisspeptin on the activation of the HPG axis in reproductively quiescent females.
The breeding and non-breeding males from both captive and wild colonies of the naked mole-rat show significant differences in both the size and appearance of the reproductive tracts [20]. Breeding males have larger testes relative to their body mass compared to their non-breeding counterparts. While all males show spermatogenesis and mature sperm production, the non-breeders produce significantly fewer sperm compared to breeders. Furthermore, the spermatozoa in non-breeders appears to have larger numbers of sperm that are non-motile or possess morphological defects such as possessing two flagella, being double headed or pin headed [20]. Non-breeders characteristically have low concentrations of urinary testosterone and lower or non-detectable concentrations of basal circulating luteinising hormone (LH). Furthermore, the pituitary gland is less responsive to the administration of exogenous GnRH when compared to plasma levels of the breeding males [5]. These profiles imply that socially induced impairments occur on the hypothalamic-pituitary axis in non-breeding males [5][21]. However, in contrast to females, no reproductive status-related differences in the number of kisspeptin-expressing cells exist in the hypothalamus [17]. Nevertheless, subordinate males have increased RFRP-3 immunoreactivity in the hypothalamus and when given the opportunity, they do not enter puberty when treated with exogenous RFRP-3, which matches the findings in females [19]. This suggests that a similar mechanism of puberty suppression is acting in both sexes. Under natural conditions, reproductive suppression in males is lifted once the social environment is changed. As a consequence, non-breeding males removed from the inhibitory cues of the natal colony and either housed singly or paired with a female rapidly demonstrate elevated levels of plasma LH and urinary testosterone concentrations [21].

3. The Scenario in the Damaraland Mole-Rat

Incest avoidance appears to be the predominant mechanism of reproductive inhibition in the majority of the social Cryptomys and some members of the genus Fukomys, and is important in maintaining reproductive skew in F. anselli [22], F. darlingi [23][24], F. damarensis [25][26] and F. mechowii [27].
The ovaries of non-breeding female Damaraland mole-rats are more functionally active compared to those of non-breeding naked mole-rats, in that they exhibit a range of follicular development from primordial follicles through to Graafian follicles, with the latter regressing to form luteinised, unruptured follicles [28][29]. Being induced ovulators, corpora lutea of ovulation are absent in non-breeding females and concentrations of urinary progesterone do not reach the concentrations of those in breeding females [30][31]. The disruption of GnRH release or a down regulation of GnRH receptors on the pituitary itself are possible scenarios for the reduced response of the pituitary to an exogenous GnRH challenge [32]. The measurable progesterone found in the non-breeding females is most likely a function of the luteinisation of unruptured tertiary and Graafian follicles [28][32] At the neuroanatomical level no differences are found in the numbers of GnRH immunoreactive neurons, the different proportions of neurons (non-polar, unipolar and bipolar) or the size of the cell soma of the GnRH neurosecretory cells between breeding and non-breeding females [33]. However, the GnRH neurons of non-breeders retain more GnRH in the dendrites as a consequence of the lack of a signal to release into the portal system. The GnRH concentrations in the median eminence and proximal pituitary stalk are significantly higher in non-breeding females when compared to those of breeding females [33]. These findings support the lack of a preovulatory GnRH surge and subsequent ovulation in these females.
In induced ovulators, the mating stimulus activates kisspeptin neurons in the AVPV, which leads to activation of GnRH neurons and consequently, to ovulation. No such activation occurs in the ARC kisspeptin neurons, indicating that this neuron population is not involved in mating-induced ovulation [34]. The release of GnRH is under the control of positive and negative feedback mechanisms of 17β-oestradiol, mediated by the oestrogen receptor α (ERα). Kisspeptin neurons in the AVPV and arcuate nucleus are known to co-express ERα and androgen receptors (AR). Several recent studies in female Damaraland mole-rats have identified differential hypothalamic gene expression patterns of steroid hormone receptors and of neuropeptides involved in the activation of GnRH neurons according to the reproductive status of the female. In breeding females, the mRNA expression of AR is significantly elevated compared to non-breeding females in several hypothalamic and limbic brain regions such as the medial preoptic area, the principal nucleus of the bed nucleus of the stria terminalis, the ventromedial nucleus of the hypothalamus, the ARC and the medial amygdala [35]. These findings could relate not only to the reproductive activity of these females, but also to their dominant position within the colony. Furthermore, breeding females have increased ERα expression in the AVPV, which is in agreement with the stimulatory effect of oestradiol on the kisspeptin neuron population in this region [35]. Interestingly, in Damaraland mole-rats, Kiss1-expressing cells within the preoptic hypothalamus are scarce, with only few cells scattered throughout the AVPV and the periventricular preoptic nucleus [36]. It is likely that in breeding females, these cells only become activated after the mating stimulus has occurred and ovarian oestradiol production has started to increase as has been shown in another induced ovulator, the musk shrew (Suncus murinus, [34][37]). In contrast, in the ARC, Kiss1 gene expression differs according to females’ reproductive status. These kisspeptin neurons coexpress neurokinin B (NKB; encoded by the Tac3 gene) and the endogenous opioid peptide dynorphin (encoded by the Pdyn gene) and are termed the “KNDy” (kisspeptin/neurokinin B/dynorphin) neurons. This neuron population is considered to be the GnRH pulse generator, which is responsible for generating the pulsatile release of GnRH. According to the model, increased NKB expression signals pulse onset. The release of NKB leads through a positive feedback loop to increased neural activity of the KNDy neurons, followed by kisspeptin release and GnRH secretion. The subsequent release of dynorphin terminates the kisspeptin release and the GnRH pulse (for review, see Moore [38]). Female breeding Damaraland mole-rats have significantly more Kiss1-expressing cells, increased neurokinin B and decreased dynorphin gene expression in the ARC compared to non-breeding females [36][39]. These differential gene expression patterns according to reproductive status are in line with the finding that in all mammals, the GnRH pulse generator reactivates at puberty after juvenile quiescence (for review, see [40]). In induced ovulators, such as the musk shrew, virgin mating activates ovarian steroidogenesis, thereby priming the HPG axis and consequently, inducing the onset of puberty [41]. Therefore, the hypothalamic gene expression pattern found in non-breeding female Damaraland mole-rats most likely reflects their pre-pubertal stage. Similar to the findings of [19] in naked mole-rats, female breeding Damaraland mole-rats had significantly fewer RFRP-3-expressing cells within the hypothalamus than non-breeding females [36]. Although the exact mechanisms of puberty onset are still unknown and may differ between the two species, this finding supports the view that RFRP-3 plays an important role in it.
In male Damaraland mole-rats, there are few anatomical differences between the reproductive tracts of breeders and non-breeders, with no differences in the production of spermatozoa or any defects in motility or morphology in non-breeding males [20][42]. However, breeding male Damaraland mole-rats, as with the naked mole-rat, have heavier testes relative to their body mass. Interestingly, larger testes do not result in an enhanced production of spermatozoa, since no significant differences are found in sperm numbers between the two groups [20].
Endocrine studies complement these anatomical findings, in that both the breeding and non-breeding males do not differ in their concentrations of urinary testosterone, brain GnRH concentrations or basal circulating LH concentrations, and they have a similar pituitary response to an exogenous GnRH challenge [30][31][32][33]. Furthermore, there is no difference in the circulating FSH concentrations between the reproductive categories. However, breeding males have been shown to possess six times more FSH receptors in the testicular tissues when compared to those of non-breeding males [43]. Thus, the effect of FSH suppression in this instance must be at the level of the receptor, or the post receptor.
Similar to females, neural gene expression patterns of steroid hormone receptors and neuropeptides involved in activation of GnRH neurons show differences in relation to reproductive status. Breeders have significantly increased androgen receptor and progesterone receptor expression in several hypothalamic brain regions involved in reproduction [44]. Furthermore, while the number of Kiss1-expressing cells in the ARC is similar in breeders and non-breeders, the latter exhibit increased RFRP-3 gene expression in the dorsomedial hypothalamus [45]. This finding matches the recent findings by immunocytochemistry in male and female naked mole-rats [19]. It suggests that not only female, but also male Damaraland mole-rats are subject to physiological suppression.

This entry is adapted from the peer-reviewed paper 10.3390/ani12213039

References

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