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Essay: Reproductive Modulation

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Reproductive modulation has been documented across various animal taxa, including mammals. Species which show the most extreme examples of altered reproduction usually live in highly complex and cooperative social groups. Within mammals, naked mole-rats and marmosets are two examples of highly social species which show pronounced reproductive modulation. In both cases, subordinate males and females show suppressed reproduction. This is primarily controlled by superior conspecifics in the hierarchy, either via behavioural or chemical mechanisms. Behavioural or social cues tend to be characterised by aggression towards the non breeding animals, elevating levels of stress and thus suppressing their reproduction (Brant et al. 1998). Chemical cues are given in the form of pheromones, which elicit physiological or behavioural responses in the recipients. Pheromones have the ability to affect the hypothalamus in the brain of the recipient, which may alter the sex hormones secreted, and thus alter reproduction (Faulkes, 2016). The role that pheromones play in reproduction modulation is better understood in the insects, where specific chemical compounds have been identified. However, the extent to which it alters mammalian reproduction is still openly debated. Many argue that there is no mammal equivalent to the pheromones found in insects and that social and behavioural cues are more important.

Pheromones are received either by the main olfactory epithelium (MOE) or the accessory olfactory epithelium, also known as the vomeronasal organ (VNO). Both of these structures have direct links to the hypothalamus, which regulates reproductive hormones such as gonadotrophin-releasing hormone (GnRH) (Barrett et al. 1993). The suppression of GnRH causes declines in luteinizing hormone (LH) and follicle-stimulating hormone (FSH), eventually leading to a state of hypogonadotrophic hypogonadism, where no sex steroids are produced (Michael, 2016). It has been found that subordinate marmosets exhibit this block in their GnRH pathway (Barrett at al. 1990). Marmosets live in cooperatively breeding groups where the breeding is limited to one female. The role of subordinate individuals in the group is to help raise the offspring of the breeding female. It is therefore in the dominant female’s best interest to maintain a state of anovulation, through her pheromonal cues (Barret et al. 1993). To understand the link between pheromones and reproductive suppression, a study was conducted where subordinate females were separated from the dominant female (Barrett at al. 1990). The individually housed marmosets were exposed daily to the dominant female’s odours, in order to still receive her pheromonal cues. Results found that marmosets kept in odour contact showed delays in reactivation of ovulation, in comparison to the controls with no odour contact. This provides evidence that pheromonal cues play a role in suppressing reproduction. However pheromones alone are not enough to suppress ovulation as all of the singly housed marmosets eventually resumed ovulation, despite the contact with dominant pheromones (Barrett at al. 1990). This suggests that perhaps behavioural cues from the breeding female are needed to maintain reproductive suppression.

Naked mole-rats (Heterocephalus glaber) are good examples of species that show extreme reproductive modulation via behavioural mechanisms. Naked mole-rats are burrowing rodents with colonies consisting of up to 300 individuals (Faulkes & Abbott, 1993). They are known to be the first and perhaps only eusocial mammal species (O’Riain & Faulkes, 2008). Within their colonies there is a strict division of reproduction, restricted to just one female (the ‘queen’) and up to three dominant males (Clarke & Faulkes, 2001). All other members of the group are described as being reproductively ‘quiescent’ but are not permanently sterile (Faulkes & Abbott, 1993). Their role in the colony is to help forage, guard the colony, and assist with raising the pups (Clarke & Faulkes, 2001). Studies of H. glaber have shown that the suppression of subordinate individuals is maintained through behavioural cues from the breeding individuals, not pheromonal cues. Faulks and Abbott (1993) separated non breeding females from their parent colony and housed them individually. The mole-rats were exposed daily to their parent colony’s pheromones from soiled bedding and litter. If pheromonal cues were the cause of the suppressed reproduction, it would be expected that the singly housed mole-rats would still be infertile despite having no physical contact with their parent colony. However, results showed that reproduction in both males and females quickly resumed once separated. An active reproductive system was indicated by a significant increase in testosterone and progesterone respectively, something which was not observed when they were in physical contact with their parent colony. This suggests that pheromonal cues are not the main cause for reproductive suppression (Faulks & Abbott, 1993). Instead it has been proposed that suppression is stress-induced and a result of aggression initiated by the queen (Faulks & Abbott, 1993). There is a positive correlation between the frequency of aggressive behaviours such as shoving and head-butting and the rank of the individual, with the queen being the most aggressive (Clarke & Faulkes, 2001). This added stress affects the GnRH pathway and causes hypogonadotrophic hypogonadism, which ultimately stops ovulation (Michael, 2016). However, although the queen’s pheromones alone do not elicit reproductive suppression, they could help reinforce her status symbol and presence within the group (Faulks & Abbott, 1993). Therefore it cannot be ruled out that pheromones aren’t important in reproductive modulation, although it is generally agreed that they are not the causative agent for reproductive suppression.

Based on the two examples described above, it is evident that the role of pheromones in mammalian reproduction is still unclear. That is not to say that pheromones are not important but perhaps their role in reproduction is a smaller one, such as reinforcing behavioural cues or the social status of dominant individuals. As chemical and behavioural effects are closely intertwined, is it hard to see their importance independent of one another. However, the exclusion experiments with both the marmosets and naked mole-rats provide evidence that pheromonal cues alone are incapable of maintaining suppression in these mammals. I do not believe pheromones have same impact on reproduction as behavioural cues. Therefore, it can be concluded that behavioural cues have greater importance in mammalian reproductive modulation.

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