Hormones associated with various non-human primate reproductive behaviors: What they can teach us about ourselves

Abstract

The endocrinology associated with reproduction is conserved among humans and non-human primate species because of our shared common evolutionary ancestry. Non-human primate species exhibit various reproductive behaviors that are mediated by different types of steroid hormones such as sexual swelling, social dominance by sex, promiscuous mating, and infanticide. Both the presence and the appropriate concentration of steroid hormones are vital to the effectiveness of each reproductive behavior. Some reproductive characteristics are sex specific while others are more complex and are affected by stress levels and social status. By researching the reproductive endocrinology of non-human primates, we can better understand the reproductive capacity of captive populations, with broader implications concerning our own reproductive physiology. Here, I 1) review the relationship between various steroid hormones and associated reproductive characteristics of non-human primates, and 2) emphasize the vast amount of knowledge we can gain from them, which includes understanding how to circumvent issues concerning our own fertility.

Introduction

The survival of a species depends on their ability to transfer their genetic material successfully to many offspring. Species utilize different reproductive characteristics evolved from their ancestors and reflect their life history traits to facilitate this process. Some of these characteristics are sex-specific, permitting animals to increase their fitness and to reproduce successfully. Social status can also dictate successful reproduction for animals in hierarchical societies, with dominant individuals having more advantages than subordinates. Hormones can mediate the expression of these characteristics and associated behaviors. By revealing the function of these hormones in non-human primates, we can illuminate their role in reproductive processes of other organisms that reproduce sexually, as well as their potential usage in drugs for regulating breeding and fertility in both primates and humans. The aim of this review is divided into two segments: First, I review the hormones of reproduction and address the question: is it merely the presence of certain reproductive hormones or the interaction between them that determines reproductive success in non-human primates? Second, I review the costs and benefits of incorporating non-human primates in research studies of reproduction, as well as the limitations, to identify the reasons why studies of non-human primates are useful in assembling information and broadening our understanding about various aspects of human reproduction and physiology.

I. Reproductive Characteristics of Various Primates

To reproduce successfully, non-human primates have evolved various characteristics and behaviors. Males and females tend to differ in the mechanisms they use in order to communicate to the opposite sex to let them know their reproductive status. It appears as though some reproductive behaviors have been conserved between various primate species, as well as the hormones associated with them, but the way in which the hormones function may vary from species to species, or even between individuals within the same species. The reproductive behaviors that have been heavily observed in non-human primates include sexual swelling, social dominance, promiscuous mating, and infanticide. Most of these behaviors are driven by the functioning of certain reproductive hormones that can be studied and used for analytical research for advances in breeding and fertility of non-human primates, as well as establishing correlations of reproductive hormones in primates and humans. Although infanticide involves the killing of offspring, it has been observed in various non-human primate species, mainly amongst males, as a way to curtail the momentary sterile phase of females whose ovulation is hindered from nursing their young (Boer and Sommer, 1992). In other words, females who no longer have to nurse offspring have a tendency to begin their ovulation cycle so that they can conceive again.

Sexual skin

Physical display of one’s reproductive status is one reproductive characteristic that is observed, mostly in female non-human primates. These physical displays range from sexual swelling of the skin or female genitalia to coloration of their perineal region (Nunn et al., 2001). Females who use this characteristic display these sexual signals during their menstrual cycle at a time when they are most likely ovulating (Nunn et al., 2001). Sexual swelling appears to be most prevalent in species in which females tend to live in social groups and have multiple mates. This phenomenon of reddening and swelling is a sexually selected trait that increases female attractiveness to potential mates and heightens male sexual arousal (Deschner et al., 2004). Additionally, females must compete for access to mates just as much as males do (Nunn et al., 2001). This particular form of achieving reproduction has been conserved among certain species mostly because it is a physical feature openly displayed by females that inform males of their reproductive status. Thus, females showing sexual swelling are more likely to attract attention from males and ultimately be enticed into mating with them. Some species that utilize this reproductive characteristic include chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla beringei), and white-handed gibbons (Hylobates lar).

Sexual Swelling: Chimpanzees

Researchers wonder why female chimpanzees have developed a visual form of sexual communication. One hypothesis states that exaggerated swelling results in male-male competition, allowing females to identify and mate with the fittest males (Nunn et al., 2001). Another hypothesis states that the exaggerated swelling of females attracts multiple males as mating partners, which most likely leads to paternity confusion and reduces the risk of infanticide, to be discussed later on (Nunn et al., 2001). These hypotheses support the notion that female sexual swelling signals to males’ reproductive receptivity, which typically causes different forms of relationships to occur.

Field studies show that both possessiveness and consortship appear to be the optimal mating relationships for both males and females due to the fact that the former gives males the highest probability of reproductive success, and the latter gives females the opportunity to exercise choice (Tutin, 1979). The formation of relationships could also be due to the fact that for the duration of the short-term relationship, neither partner has to compete with their same-sex counterparts, which increases the male’s chance of successful conception. These relationships that include female choice highlight the importance of sexual selection, which is arguably driven by the physical display of sexual swelling in females. Sexual swelling in female non-human primates is thought to reflect changes in the levels of estrogen and progesterone release, specifically during the menstrual cycle (Deschner et al., 2004). Maximum sexual swelling occurs during ovulation, at which estrogen levels significantly increase while progesterone levels remain at baseline (Deschner et al., 2004). Recently, two hypotheses have been established and debated over the significance of sexual swelling: females compete with one another for access to mates in a multi-male group and so perhaps the size of her swelling is an indication of her fitness (Deschner et al., 2004). Also to consider, swelling size could cause variability in the chances of conception due to the eccentric patterns of ovarian hormones (Deschner et al., 2004).

A field study reported that the timing of swelling detumescence (reduction) is correlated with ovulation, which is the most opportune time for conception (Deschner et al., 2004). However, it is unknown whether ovulation occurs toward the beginning or end of sexual swelling. It can be deduced that the sexual swelling occurs in concert with ovulation, mediated by the reproductive hormones estrogen and progesterone (Deschner et al., 2004). This study analyzed the role of these hormones in sex and conception of wild female chimpanzees. Deschner et al.’s study included free-living, unprovisioned female chimpanzees in three study populations in East Africa. Endocrine sampling included both urine and fecal samples. Urine samples were analyzed for estrogen conjugates and pregnanediol-3-glucuronide, and fecal samples were analyzed for estradiol and progesterone (Deschner et al., 2004). Deschner et al.’s study revealed that although hormone levels can change, a relationship was present between steroid concentrations from same day extractions. Deschner et al.’s results show a variability in timing of steroid secretion and swelling within the female chimpanzees of these three populations. Plasma estrogen peaked at 7–8 days prior to reduced swelling, but remained elevated until drastically declining at detumescence; this result was seen in both nulliparous and parous females as well as for conception and non-conception cycles (Deschner et al., 2004). Nulliparous females have never given birth while parous females have offspring-reared at least once. Variability in timing and magnitude of peak levels was also observed for progesterone. Female chimpanzees had low progesterone levels during estrogen peak of follicular phase, followed by elevation in progesterone within the first 9 days of detumescence (Deschner et al., 2004). Deschner et al’s results supported one of the hypotheses, specifically that the period of maximal swelling should occur mid to late follicular activity since swelling of sexual skin is induced by estrogen, and that most luteal activity should occur after detumescence since progesterone activity reduces swelling in luteal phase (Deschner et al., 2004). These results suggest that the process of sexual swelling is driven by both the presence and the timing of peaks of these two hormones. Researchers also found significantly higher steroid conjugate levels in both the swelling and post-swelling phases of the conception cycles compared to the non-conception cycles (Deschner et al., 2004). Also, both the estrogen levels and the number of copulations with the alpha male significantly increased during the fertile period, throughout the duration of sexual swelling. Copulations peaked at ~7 days before detumescence and remained elevated until the day of detumescence, which correlates to the time that estrogen peaks were elevated (Deschner et al., 2004). From this study, it can be concluded that both estrogen and progesterone are necessary to regulate the sexual swelling in female chimpanzees, but estrogen alone drives the sexual swelling (which attracts potential mates and leads to a higher chance of conception).

The fertility process in chimpanzees, one of our closest living relatives, can illuminate the notion that women evolved earlier fertility termination due to increased health risks in late births, according to Hawkes and Smith (2010). Thompson et al. (2007) contrasted age patterns of fertility in chimpanzees and humans, specifically two well-studied human foraging populations: the !Kung of Botswana and the Ache of Paraguay. They found that chimpanzees experience an earlier onset of fertility (10–14 years old), and reproduce more broadly across their life cycle compared to humans (Thompson et al., 2007). The !Kung population had peak fertility rates similar to chimpanzees, and there was no significant difference found between the age-dependent decline in chimpanzee fertility after age 25 from both human populations (Thompson et al., 2007). They also found that human reproduction ends when mortality is very low, while the fertility in chimpanzees declines at a similar pace to the decline in survival probability (Thompson et al., 2007). The similar patterns of declining birth rates observed between humans and chimpanzees suggest that the physiology of reproductive senescence was likely conserved in human evolution (Thompson et al., 2007).

Sexual Swelling: Gorillas

Another non-human primate species that utilizes sexual swelling of the skin as a reproductive characteristic are gorillas. Behavioral studies show that female mountain gorillas reach sexual maturity at age 6, followed by a 2 year period of sterility (Czekala and Sicotte, 2000). I would argue that sterility allows the body to fully develop and establish a baseline rate of sex hormone release needed for successful reproduction. Previous studies of sexual behavior and female hormones in gorillas reveal two phenomena: mating occurs during a brief mid-cycle period of maximal labial tumescence (swelling), and 17-β estradiol and testosterone reach peak concentrations during the same period (Nadler et al. 1983). These distinct hormonal peaks suggest that different aspects of sexual activity correspond with one or both of the two hormones (Nadler et al., 1983). However, only nulliparous females exhibit signs of estrous such as small labial swelling, but parous females do not (Czekala and Sicotte., 2000). Proceptivity of nulliparous females (pro-conception) is more variable compared to parous females that are proceptive for 1–4 days (Czekala and Sicotte, 2000). Czekala and Sicotte report the hormone pattern data for one individual female as the following: rising levels of estrogen 9 days prior to end of follicular phase, estrogen levels remain low during early to mid-luteal phase, then estrogen levels rise again by day 18. There was no clear pattern observed for progesterone (Czekala and Sicotte, 2000).

Labial swelling appeared to reach its maximum while estrogen levels were low, suggesting that estrogen does not play a prominent role in labial swelling of nulliparous female gorillas as it does in chimpanzees (Czekala and Sicotte, 2000). Though the levels of estrogen in both chimpanzees and gorillas differ drastically, higher levels in former and lower levels in the latter, estrogen is still necessary to facilitate the sexual swelling in gorillas. Comparison between chimpanzees and gorillas can highlight different aspects of the life evolutionary histories of each organism and help decipher what characteristics caused them to diverge from one another.

Sexual Swelling: White-handed gibbons

There appears to be a relationship between sexual swelling and mating systems: the absence of swelling has been observed in monogamous species and exaggerated swellings within polygamous species (Barelli et al., 2007). However, given that white-handed gibbons are monogamous, sexual swellings in gibbons are very perceptible. Gibbon swellings could most likely resemble that of polygamous practicing species (Barelli et al., 2007). Studies on captive white handed gibbons do not clarify the relationship between the sexual swelling cycle and ovulation or fertility phase, which is something that Barelli et al. sought to achieve (Barelli et al., 2007). Researchers measured levels of immunoreactive 5α-reduced 20 oxo pregnanes (5-P-3-OH) and fecal metabolites of progesterone (also known as progestogen) from fecal samples to determine the lengths of both the luteal and follicular phase of the menstrual cycle, as well as the possible day of ovulation and timing of the fertile phase (Barelli et al., 2007). Fecal progestogen was shown to have low levels in follicular phase, followed by elevated levels in the luteal phase (Barelli et al. 2007). Barelli et al. found that maximum swelling was limited to the follicular and early luteal phases, with a gradual decrease 4–5 days after post-ovulatory progestogen. Although maximum swelling duration varied between individuals, overall maximum swelling periods lasted 7–11 days (Barelli et al., 2007). Also, unlike other primate species age plays a role in the duration of the maximum swelling, the point at which swelling of perennial region is swollen to the highest degree, as older females have significantly shorter maximum swelling phases than younger females. Based on these results, younger female gibbons appear to have an advantage over older female gibbons, in that younger females have a longer period to find and attract mates. Even after fertilization, maximum swelling appeared at random intervals throughout pregnancies with average duration of 2.7 days (Barelli et al., 2007). These results suggest that maximum sexual swelling is not solely representative of ovulation and fertilization as it is in chimpanzees since swelling occurs throughout pregnancy in white-handed gibbons.

Social Hierarchy

Another reproductive characteristic of non-human primate species is social dominance of individuals by sex. Some species form social hierarchies among the males and/or females mainly because it reduces the amount of aggressive interactions year round as well as stress levels. Once social dominance is established, each individual peacefully complies with his or her societal role. However, one’s social status dictates their access to mates as well as their overall reproductive success, so those individuals with dominant status will benefit greatly. Evidence from various studies supports the hypothesis that higher ranked males experience greater reproductive success than subordinate males (Ellis, 1995). Dominant males obtain their high rank through aggressive behavior, which could be mediated by testosterone. However, the positive relationship between reproductive success and rank among females is not fully understood because some studies indicate the presence of a positive relationship, while others do not (Ellis, 1995). It seems that dominance would be associated with male reproductive success, as dominant males acquire more food and territory, rendering them more attractive than subordinate males to their female counterparts. Females are often attracted to males exhibiting high fitness, causing them to primarily reproduce with dominant males. There is a possibility that dominance may hinder male reproductive success in males due to the fact that dominant males spend so much time fighting to retain their dominant position while subordinate males use that time to reproduce instead. This tactic is referred to as a make-love-not-war effect (Ellis, 1995). Marmosets (Callithrix jacchus) and orangutans (Pongo pygmaeus) exhibit social dominance hierarchies, either male or female oriented, which influence the reproductive success of all individuals.

Social Hierarchy: Marmosets

The common marmosets are small-bodied, cooperatively breeding New World monkeys that live in multi-female social groups (Saltzman et al., 1998). The most dominant female within each group is the sole breeder since social status among females strongly regulates reproduction (Saltzman et al., 1998). Studies show that subordinate females fail to breed in both the wild and in captive groups; instead, they aid the dominant female in providing care for her offspring (Saltzman et al., 1994). Subordinate females are also anovulatory (do not ovulate) due to a decrease in the pituitary release of the luteinizing hormone and the impaired secretion of the gonadotropin-releasing hormone (Saltzman et al., 1994). However, this hormonal suppression can be quickly reversed if a subordinate female is removed from the social group, showing elevated levels of plasma luteinizing hormone and ovulation within 2–3 weeks (Saltzman et al., 1994). Thus, the social status of female marmosets can change based on the social environment they are placed in, and with that change comes the possibility of breeding due to key alterations in hormone levels.

Researchers have shown that subordinate female marmosets have drastically lower plasma cortisol concentrations than dominant females, but it remains unclear whether the rank-related differences in plasma cortisol are a result of social status, drive it, or are the result of differences in reproductive function (Saltzman et al, 1998) (Saltzman et al, 1994). The Saltzman et al. (1994) study clarified the effects of social status, reproductive function and group formation on circulating levels of cortisol in adult female marmosets. The study included 32 captive-born adult female common marmosets that were pair-housed with adult males at least 12 days prior to the start of the experiment (Saltzman et al., 1994). The purpose was to determine the baseline cortisol level for each female for comparison in data analysis, and to ensure that all females began the experiment on the same level of cortisol. Females were placed in 1 of 8 different pre-assigned social groups, meaning all of them were exposed to the same “stimuli” per se (Saltzman et al., 1994). Social groups were formed by releasing 4 pre-assigned females and 4 adult males into a new home cage. Dominant status was assigned to females based on who the submissive behaviors were directed towards, and blood samples were collected to determine plasma cortisol levels that would support the researchers’ assumptions (Saltzman et al., 1994). Results showed that 15 females were cyclic (exhibit regular progesterone levels in both luteal and follicular stages), 8 females were oligocyclic (exhibit one or more luteal phase lasting less than 11 days and one or more follicular phase lasting more than 13 days), and 9 females as acyclic (exhibit no sustained elevation of progesterone concentrations above 10 ng/ml) prior to the formation of social groups (Saltzman et al., 1994). Results also showed that differences in cortisol levels did not become apparent until the second day of group formation: dominant females had significantly higher circulating cortisol levels than subordinate females (Saltzman et al., 1994). Researchers attribute this difference to wound formation from aggressive encounters because females who sustained wounds during group formation had significant elevation of cortisol over the basal level than those that refrained from wound aggression (Saltzman et al., 1994). Subordinate females that refrained from wound aggression did engage in high levels of agonism: they received ~11 aggressive acts per hour from other females and performed ~31 submissions per hour to other females (Saltzman et al., 1994). Subordinate females should logically exhibit higher levels of cortisol due to the stressful and aggressive encounters with other females, but the data shows that is not the case. The results from this study show that reproductive status was associated with plasma cortisol levels; though, independent of social status, cortisol levels were substantially elevated in marmosets undergoing ovulatory females. Thus, high levels of cortisol relate to and/or possibly cause ovulation which subordinate females lack. Perhaps, low cortisol causes unsuccessful breeding in subordinates. This study shows how the privileged status of social dominance among female marmosets relate to reproductive advantages, which reveals how essential this reproductive behavior can be regarding reproductive success. This study could also shine light on the role of stress in women pregnancies and how the mother’s stress level can influence development of the fetus (Barbazanges et al, 1996).

Social Hierarchy: Orangutans

Male characteristics of the orangutan society include solitary nature, sexual dimorphism, and most importantly, the extended phase of sub-adulthood (Schurmann et al. 1986). Subadult males are physiologically mature, but lack the distinct features of dominant males like: big body, long hair, gular pouch, cheek callosities, and the inability to form the far-carrying long call (Schurmann et al. 1986). Orangutan groups are small, with the most common observed social unit consisting of a female and her offspring (Schurmann et al., 1986). However, consortship relationships have been observed and can include 2–8 individuals at a time that can remain together for months at a time (Schurmann et al., 1986). The males display one of the two sexually mature morphs: the prime flanged adult male or the unflanged subadult (Knott et al., 2010). Prime flanged males are dominant to unflanged males because they are significantly larger and exhibit the aforementioned secondary features (Knott et al., 2010). Unflanged males tend to use forced copulation more so than flanged males as an alternative mating behavior to resistance by females (Knott et al., 2010). The reproductive functioning of subadult males is not affected in any way because it has been reported that the reproductive system of young subadult orangutan males is successful as early as 8 years old (Schurmann et al., 1986). The breeding behavior of the orangutan male is divided into two parts. First, as a subadult he mates with as many females as possible to increase his chances of paternity for the next generation of offspring. Second, as a prime adult he consolidates and protects his contribution since consorting is fairly difficult due to his enormous size (Schurmann et al., 1986). Although it is unclear why some males develop before others, it is possible that stress can be a strong inhibitor of development, as glucocorticoids prevent the secretion of the growth hormone and the thyroid hormone (Thompson et al., 2012). A study conducted by Thompson et al. (2012) reports that male orangutans who completed their development before age 14 had higher testosterone levels than those that completed development after age 14. They found no significant variance in cortisol levels among the early and late maturing males as well as no correlation between cortisol levels and testosterone levels (Thompson et al., 2012). The authors concluded that early elevated levels of testosterone may play a beneficial role in the early transitional development from young subadult to prime flanged adult, while cortisol may not be associated with any aspect of this reproductive characteristic in male orangutans. A study conducted by Olweus et al. (1988) shows that the amount of circulating testosterone in adolescent human males does not necessarily deter their reproductive development, but does increase aggressive behavior.

Promiscuous Mating

Promiscuous mating has been observed in females of various species as a means of a reproductive behavior. Promiscuous mating is described as females mating with numerous males throughout the duration of their ovulatory cycle. This behavior helps reduce the chances of infanticide by other non-paternity males. Females who mate promiscuously can conceal ovulation from male counterparts. This reduces the likelihood of conception when an undesirable male forces copulation because they know the chance of conception is very low (Knott et al., 2010). This form of mating can be observed in both gorillas and orangutans.

Promiscuous Mating: Gorillas

Studies show that parous fertile female gorillas are proceptive for 1–4 days and the social groups in which they reside in often contain one male. About 40 percent of recorded social groups are multi-male, having more than one sexually active adult male (Stokes et al, 2003; Czekala and Sicote, 2000). Males who are able to mate with fertile females during that 1–4 day proceptivity period will have the best chance of reproductive success. According to Nadler et al (1983), males court females with soliciting, after which females “present”, meaning females willingly position themselves for mating after the male approaches her and pulls her towards him to cover her. Female success entails female solicitation followed by copulation; with female solicitation referring to the female approaching the male followed by female presenting (Nadler et al., 1983).

Studies conducted by Nadler et al and Czekala and Sicotte report the role and function that principal hormones play in the physical display of labial swelling. Czekala and Sicotte’s study presents the first report of daily urinary hormone sampling in wild gorillas which combine mating observations and labial swelling (Nadler et al., 1983). Czekala and Sicotte found that mating and mating attempts occur at or near peak estrogen concentrations. Seven days after estrogen declines, progesterone increases, and both estrogen and progesterone increase at implantation (Czekala and Sicotte, 2000). Nadler et al. found that female solicited copulations occurred mainly outside the periovulatory phase, the period just before ovulation. Figure 1 shows that the hormone pattern during ovulation includes a midcycle preovulatory rise in estrogen, a smaller luteal phase peak, a midcycle peak of testosterone, and a luteal phase increase in testosterone (Nadler et al., 1983). Thirty-three percent of all copulations were initiated or female solicited, with 83 percent of these female solicited copulations occurring in the periovulatory phase (Nadler et al., 1983).

Figure 1: Top displays the days of copulation and hormone concentrations for five female gorillas, normalized to the day of the LH peak. Bottom displays both the perineal labial tumescence and hormone concentrations of a female gorilla during the menstrual cycle, normalized to the day of the LH peak (Nadler et al 1983).

Based on these results, with the data being normalized to the leutenizing hormone peak to determine the day of detumescence, the authors of this study came to the following conclusions concerning female gorillas: increases in copulation at midcycle are associated with midcycle concentrations of 17β-estradiol, the maximum frequency of copulations is associated with peak concentration of testosterone, and the absence of copulations during the mid-to-late luteal phase is associated with heightened levels of progesterone (Nadler et al., 1983). These results also suggest that females strategically mate with desirable males during their conception cycle or while ovulating (at estrogen peaks) which increases their chances of conception and implantation. Males tend to increase their likelihood of paternity through promiscuous mating, allowing their genes to be manifested in more offspring in the future generation due to multiple mating partners. Studies like these enhance our knowledge on what hormones are the principal roles during conception, which can than lead to more effective contraceptive agents for humans by targeting specific hormones and either suppressing or enhancing their secretion or activity.

Promiscuous Mating: Orangutans

Female orangutans show mating patterns modeling promiscuity as well. Promiscuous mating enables females the chance to allow direct or indirect manipulation of male mating access in accordance with fecundity or social context (Knott et al., 2010). In other words, males think females are not selective with regards to mating, but females tend to mate with their desirable partners while ovulating. Females also mate with non-dominant males to reduce the risk of infanticide by those males, but only during nonovulatory cycles will these matings occur (Knott et al., 2010). Female orangutans are subject to forced copulations by both dominant and subadult males on a regularly, but mostly by subadult males who feel the need to force themselves onto females as a counter strategy for not having dominant status (Barelli et al., 2007). Knott et al. (2009) observed when females resist aggressive behavior by either dominant or subadult males, the copulations do not last as long compared to willing copulations (Barelli et al., 2007). Dominant orangutan males indulged in forced copulations and overly aggressive behavior towards females more than subadult males. This complicates the notion that primary access to females for reproductive purposes is a benefit of garnering dominant status. However, prime males were reported to have obtained preferential mating access with the most fecund females (Knott et al., 2010).

Infanticide

Infanticide is considered to be a reproductive characteristic that is utilized by non-human primate species, chiefly males. For females, infanticide does not fully correspond with obtaining reproductive success since it entails the purposeful death of one’s offspring. Nevertheless, it occurs more so in non-human primate males because it allows the mother to be fertilized again soon afterwards (van Schaik et al, 1997). Animals perform infanticide for many reasons: exploitation, resource competition, parental manipulation and sexual selection (Cameron, 1996). Exploitation involves the death of offspring for the sole purpose of consumption or use of the victim (Cameron, 1996). Another reason why individuals would kill offspring is because the death of the infant would lead to increased access to resources for the killer and his or her descendants (Cameron, 1996). Parental manipulation involves the death of an infant by the parent(s) in order to improve the survival of the mother and existing offspring (Cameron, 1996). When resources are limited or in short supply, parents may be compelled to kill their younger offspring in order to provide for their older offspring who are closer to autonomy. Sexual selection, which entails competition between members of one sex (males) for reproductive investment by the other sex (females), may cause an animal (usually males) to kill another animal’s offspring (Cameron, 1996). For example, the offspring of female gorillas within a social group containing one alpha silverback male are at high risk once that alpha male dies because subadult males will attempt to fill that alpha male position. Once a new alpha male is in place, he will not want to care for another male’s young which leads him to kill the offspring of the females so that he can mate with them. He would then ensure that his legitimate offspring are reared and have access to the best resources. To prevent infanticide, female primates have utilized promiscuous mating because adult males would not know for certain the paternity of the offspring. Thus, it appears that promiscuous mating ensures the survival of one’s offspring by confusing paternity (van Schaik et al, 1997). Thus far, I have found no hormones associated with infanticide, though I would argue that testosterone levels would be higher in infanticidal males because they are trying to obtain a dominant status while securing resources for their future offspring, and dominant males have been found to have higher levels of testosterone (Anestis, 2006).

Costs and benefits of non-human primate usage for research

Strikingly similar attributes exist between humans and non-human primates, ranging from anatomy, physiology, and most importantly, endocrinology (King et al., 1988). These similarities make non-human primates an effective animal models for studies relating to immunology, pathology, reproductive biology, and more. Our common evolutionary ancestry has enabled certain processes to be conserved within humans and other primates, which suggests that processes within humans mirror those of other close related primates. Chimpanzees are one of the closest living relatives of humans (98% DNA match), which explains why they are the most widely used of the great apes (King et al., 1988). The most widely used lab animal nationwide are rodents, calculating ~90% of usage in studies because they are so easy to manage, but incorporating non-human primates into research studies could help broaden our understanding of human biology, specifically reproduction. Currently, ~30 primate species are being used in biomedical and behavioral research, with Old World species from Africa and Asia being among the most commonly used primates based on their ability to adapt to and reproduce well in captivity (King et al., 1988). Although primates are often the first choice of an investigator as an animal model, only ~3.5% of the 20 million laboratory animals studied are primates due to several factors (King et al., 1988). The factors contributing to the restricted use of non-human primates include cost, limited supply, and appropriateness (King et al., 1988). It is relatively expensive to use non-human primates in research because most non-human primates are endangered from habitat loss caused by human activity (Shimizu et al., 2003). Since there is a restriction of non-human primate use, the studies that do request non-human primates must be suitable or deemed necessary because they are not needed for all studies (King et al., 1988). There are also regulations that must be followed to ensure that humane treatments of research animals are being upheld (King et al., 1988). Most primates in research are not allowed to be in terminal experiments, nor are they involved in studies that affect their breeding ability in any way, even though successful breeding programs are put in place to replenish the number of primates that do not survive in terminal experiments or just die from natural causes (King et al., 1988).

Despite the various similarities between humans and non-human primates which fuels the need to incorporate non-human primates in more research studies, we must be careful not to exploit and take advantage of these helpless animals. Though we as humans are dominant over non-human primates and other animals, we must not exacerbate the declining rates of endangered primates solely for further knowledge of our physiology. Thus, I argue that the incorporation of non-human primates into research studies should benefit in some way both parties: humans and non-human primates.

What We Can Learn About Ourselves?

Despite these restrictions on non-human primate use in research, there are numerous benefits that can be acquired from studies that used non-human primates. In some cases, the use of non-human primates are in dire need, like testing the efficacy and safety of treatments and vaccines that have been developed in studies using other animals as the animal model (King et al., 1988). Drugs that have been developed using rodents must be tested on closely related human relatives, like monkeys or chimpanzees, to get an idea of how efficient the drug will be if it is administered to humans. In other cases, non-human primates are the only viable option for the animal model when other species are not affected by or vulnerable to the disease under investigation (King et al., 1988). Ideally, an appropriate model organism is necessary to discover drugs that can combat human life-threatening diseases, like aids or cancer.

Studies on fertility control agents and the hormonal patterns involved in reproduction have gained valuable information on reproduction in both men and women due to the incorporation of non-human primates. Shetty et al. (1997) conducted a study to analyze the effects of estrogen deprivation in reproductive functioning of male and female primates using aromatase inhibitors. There are many estrogen dependent processes in female primates that occur throughout ovulation and non-ovulation cycles such as: the preparation of fallopian tubes for gamete interaction, early embryonic development, and preparation of the uterus for implantation (Shetty et al. 1997). Estrogen is therefore necessary in order to carry out the various processes that occur in female primate reproduction. Thus, the absence of such a vital component alters the functionality of these processes. The bonnet monkey was chosen as the primate model because past studies have shown its usefulness as a surrogate model for the human (Shetty et al. 1997). Shetty et al. (1997) found that estrogen deprivation led to the absence of preovulatory estrogen surge that normally occurs between days 8 and 11 in the female bonnet monkey. Estrogen deprivation affected the reproductive state of males as well, resulting in the enhanced secretion of the luteinizing hormone and testosterone which impairs reproduction (Shetty et al. 1997). This study was the first to use monkeys to test the efficacy of aromatase inhibitors as fertility regulator agents for men and women (Shetty et al. 1997). The conclusions they gathered could aid in developing aromatase inhibitors to induce super follicular maturation in women, as well as devising short term treatments to help increase testicular testosterone to boost spermatogenesis as a means of male fertility control (Shetty et al. 1997).

The use of non-human primate animal models will broaden our understanding of human biology and biological systems that cannot always be tested in humans. When it comes to reproduction, non-human primates are considered to be the closest model in relation to humans, which alludes to the reason why they are often sought after by many scientists. The endocrine mechanism of macaques has been investigated to analyze the role of prenatal hormone exposure in the determination of sexual phenotype (Shetty et al. 1997). Also, investigating the role of hormones in non-human primates like luteinizing hormone, testosterone, and follicle stimulating hormone that can be detected early in life, have shown that reversible elimination of elevated levels by treatment of GnRH agonists show that perinatal elevations of steroid hormones could alter normal sexual development in males particularly (Shetty et al. 1997).

What We Can Learn About Reproductive Systems in Primates

The involvement of non-human primates in research is and should not be one-sided, as in solely beneficial to humans; advances in the reproductive capacity and fertility control can be made as well with the usage of non-human primates as animal models. For example, data has already been gathered on the influence of the CBC pill (combination birth control) on sexual behavior in women, but no data has been reported regarding its effects on gorilla estrous behavior. Safarty et al. (2012) examined the temporal trends of estrous, aggressive, affiliated, and activity budget data in a small group of 4 female gorillas while taking CBC pills. These CBC pills contain both synthetic estrogen and progestin followed by a week of placebo or sugar pills; they suppress the activity of the HPG axis and instead promote follicle development, release and proliferation of uterine wall (Safarty et al., 2011). CBC is considered to be highly effective in lowland gorillas and is a popular choice of contraception throughout U.S. zoos for controlling reproduction (Safarty et al., 2011). The effects of CBC on other non-human primates have been documented already; one of which shows that macaques behave more aggressively and that mating behavior in chimpanzees is reduced (Safarty et al., 2011). Desirable features of a contraceptive method include efficacy and having little to no effect on the social, sexual behavior of the animal. Compared to previous studies of uncontracepted gorillas that exhibited a peak of proceptive and receptive sexual behavior at time of ovulation (2nd week of menstrual cycle) which has also been observed in uncontracepted human females, the sexual behavior of contracepted gorillas in this study occurred in week 1 of menstrual cycle instead (Safarty et al., 2011). Also, 3 of the 4 female gorillas in this study showed aggressive behavior evenly throughout the cycle weeks (Safarty et al., 2011). This study shows that human based contraceptive methods such as CBC does not alter the endocrinology of female gorillas, but it does influence aggressive behavior as well as altered timing of sexual behaviors. Overall, human based methods can be administered to non-human primates specifically to aid in conservation efforts for breeding endangered non-human primate species, and still express the same level of efficacy.

Conclusion

The reproductive characteristics and behaviors of non-human primates vary between species and the presence and appropriate concentration of associated steroid hormones are vital to the efficacy of these mechanisms. The main hormones that drove the sexual swelling include estrogen and progesterone. The hormones associated with the social dominance hierarchies include cortisol and possibly elevated levels of testosterone, specifically in orangutans. Primate females that live in large social groups utilize promiscuous mating to combat the infanticidal incoming alpha males to save the lives of their children. Some primate species use more than one characteristic or behavior or a combination based on mating patterns or social hierarchy present within the species’ society. The various sex hormones involved in these characteristics and behaviors tend to be present at certain times (during ovulation or conception cycles), and at different concentrations to ensure correct functionality of the reproductive processes and to secure successful reproduction by producing offspring in the next generation. Since non-human primates share so many aspects of biology with humans due to common evolutionary ancestry, non-human primates are the most suitable model for developing safe breeding techniques for captive primate populations, as well as fertility agents for both men and women.

Acknowledgements

I would like to give a special thank you to the Barnard College Writing Center, my peers from the Fall 2014 Biology Senior Seminar course, and Professor Rebecca Calisi for taking out time to edit this semester-long project.

References

1. Albrecht, E. D., G. W. Aberdeen, and G. J. Pepe. “The Role of Estrogen in the Maintenance of Primate Pregnancy.” Am J Obstet Gynecol 182.2 (2000): 432–38. Print.
2. Anestis, S. F. “Testosterone in Juvenile and Adolescent Male Chimpanzees (Pan Troglodytes): Effects of Dominance Rank, Aggression, and Behavioral Style.” <i>AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY</i> 130 (2006): 536–45. Wiley InterScience. Web. 1 Dec. 2014. &lt;http://onlinelibrary.wiley.com/doi/10.1002/ajpa.20387/pdf&gt;.
3. Barbazanges, Amaud, Pier V. Piazza, Michel Le Moal, and Stefania Maccari. “Maternal Glucocorticoid Secretion Mediates Long-Term Effects of Prenatal Stress.” <i>The Journal of Neuroscience</i> 16.12 (1996): 3943–949. Print.
4. Barelli, C., M. Heistermann, C. Boesch, and U. H. Reichard. “Sexual Swellings in Wild White-handed Gibbon Females (Hylobates Lar) Indicate the Probability of Ovulation.” <i>Hormones and Behavior</i> 51 (2007): 221–30. Print.
5. Bazer, F. W., and T. E. Spencer. “Hormones and Pregnancy in Eutherian Mammals.” Hormones and Reproduction of Vertebrates. Vol. 5. Elsevier, 2011. 73–93. Print.
6. Bellem, A. C., S. L. Monfort, and K. L. Goodrowe. “Monitoring Reproductive Development, Menstrual Cyclicity, and Pregnancy in the Lowland Gorilla (Gorilla Gorilla) by Enzyme Immunoassay.” Journal of Zoo and Wildlife Medicine 26.1 (1995): 24–31. Print.
7. Berenstain, L., and T. D. Wade. “Intrasexual Selection and Male Mating Characteristics/behaviors in Baboons and Macaques.” International Journal of Primatology 4.2 (1983): 201–35. Print.
8. Boer, Michael, and Volker Sommer. “Evidence for Sexually Selected Infanticide in Captive Cercopithecus Mitis, Cercocebus Torquatus, and Mandrillus Leucphaeus.” <i>Primates</i> 33.4 (1992): 557–63. Print.
9. Cameron, J. L. “Regulation of Reproductive Hormone Secretion in Primates by Short-term Changes in Nutrition.” Reviews of Reproduction 1 (1996): 117–26. Print.
10. Czekala, N. M., K. Benirschke, H. McClure, and B.L. Lasley. “Urinary Estrogen Excretion During Pregnancy in the Gorilla (Gorilla Gorilla), Orangutan (Pongo Pygmaeus) and the Human (Homo Sapiens)1.” <i>Biology of Reproduction</i> 28 (1983): 289–94. Print.
11. Czekala, N., and P. Sicotte. “Reproductive Monitoring of Free-Ranging Female Mountain Gorillas by Urinary Hormone Analysis.” American Journal of Primatology 51 (2000): 209–15. Print.
12. Deschner, Tobias, Michael Heistermann, Keith Hodges, and Christophe Boesch. “Female Sexual Swelling Size, Timing of Ovulation, and Male Behavior in Wild West African Chimpanzees.” <i>Elsevier</i> 3 (2004): 1–12. Print.
13. Ellis, Lee. “Dominance and Reproductive Success Among Non-human Animals: A Cross-Species Comparison.” <i>Ethology and Sociobiology</i> 16 (1995): 257–333. Print.
14. Emery, Melissa A., and Patricia L. Whitten. “Size of Sexual Swellings Reflects Ovarian Function in Chimpanzees (Pan Troglodytes).” <i>Behavior Ecology Sociobiology</i> 54 (2003): 340–51. Print.
15. Hawkes, Kristen, and Smith, Ken R. “Do Women Stop Early? Similarities in Fertility Decline in Humans and Chimpanzees.” <i>Ann N Y Acad Sci., NIHPA Author Manuscripts</i> 1204 (2010): 43–53. Print.
16. Hrdy, S. B. “Infanticide Among Animals: A Review, Classification, and Examination of the Implications for the Reproductive Characteristics/behaviors of Females.” Ethology and Sociobiology 1 (1979): 3–40. Print.
17. King, F. A., C. J. Yarbrough, D. C. Anderson, T. P. Gordon, and K. G. Gould. “Primates.” Science 240.4858 (1988): 1475–482. Print.
18. Knott, C. D., M. E. Thompson, R. M. Stumpf, and M. H. McIntyre. “Female Reproductive Characteristics/behaviors in Orangutans, Evidence for Female Choice and Countercharacteristics/behaviors to Infanticide in a Species with Frequent Sexual Coercion.” Biological Sciences 277.1678 (2010): 105–13. Print.
19. Olweus, D., Mattsson, A., Schalling, D., and Low, H. “Circulating Testosterone Levels and Aggression in Adolescent Males: A Causal Analysis.” <i>Psychosomatic Medicine</i> 50 (1988): 261–72. Print.
20. Nadler, R. D., D. C. Collins, L. C. Miller, and C. E. Graham. “Menstrual Cycle Patterns of Hormones and Sexual Behavior in Gorillas.” Hormones and Behavior 17 (1983): 1–17. Print.
21. Nunn, C. L., C. P. Van Schaik, and D. Zinner. “Do Exaggerated Sexual Swellings Function in Female Mating Competition in Primates? A Comparative Test of the Reliable Indicator Hypothesis.” <i>Behavioral Ecology</i> 12.5 (2001): 646–54. Print.
22. Saltzman, W., N. J. Schultz-Darken, F. H. Wegner, D. J. Wittwer, and D. H. Abbott. “Suppression of Cortisol Levels in Subordinate Female Marmosets: Reproductive and Social Contributions.” Hormones and Behavior 33 (1998): 58–74. Print.
23. Saltzman, W., N. J. Schultz-Darken, G. Scheffler, F. H. Wegner, and D. H. Abbott. “Social and Reproductive Influences on Plasma Cortisol in Female Marmoset Monkeys.” Physiology & Behavior 56.4 (1994): 801–10. Print.
24. Sarfaty, A., S. W. Margulis, and S. Atsalis. “Effects of Combination Birth Control on Estrous Behavior in Captive Western Lowland Gorillas, Gorilla Gorilla Gorilla.” Zoo Biology 31 (2011): 350–61. Print.
25. Schurmann, C. L., and Jan A. R. A. M. Van Hoff. “Reproductive Characteristics/behaviors of the Orang-Utan: New Data and a Reconsideration of Existing Sociosexuai Models.” International Journal of Primatology 7.3 (1986): 265–87. Print.
26. Shetty, G., Krishnamurthy, H., Krishnamurthy, H. N., Bhatnagar, Ajay S., Moudgal, R. N. “Effect of Estrogen Deprivation on the Reproductive Physiology of Male and Female Primates.” J. Steroid Biochem. Molec. Biol. 61.3–6 (1997): 157–66. Print.
27. Shimizu, K., T. Udono, C. Tanaka, E. Narushima, M. Yoshihara, M. Takeda, A. Tanahashi, L. Van Elsackar, M. Hayashi, and O. Takenaka. “Comparative Study of Urinary Reproductive Hormones in Great Apes.” Primates 44 (2003): 183–90. Springer Link. Japan Monkey Centre and Springer-Verlag. Web. 1 Oct. 2014. <http://link.springer.com/article/10.1007/s10329-002-0021-9#page-1>.
28. Stokes, E. J., R. J. Parnell, and C. Olejniczak. “Female Dispersal and Reproductive Success in Wild Western Lowland Gorillas (Gorilla Gorilla Gorilla).” Behavior Ecology Sociobiology 54 (2003): 329–39. Springer Link. Springer-Verlag. Web. 1 Oct. 2014. <http://link.springer.com/article/10.1007/s00265-003-0630-3#page-1>.
29. Thompson, M. E. “Reproductive Endocrinology of Wild Female Chimpanzees (Pan Troglodytes Schweinfurthii): Methodological Considerations and the Role of Hormones in Sex and Conception.” American Journal of Primatology 67 (2005): 137–58. Print.
30. Thompson, M. E., A. Zhou, and C. D. Knott. “Low Testosterone Correlates with Delayed Development in Male Orangutans.” <i>PLoS ONE</i> 7.10 (2012): E47282. <i>PLOS One</i>. 10.1371/journal.pone.0047282. Web. 1 Oct. 2014. &lt;http://www.plosone.org/article/info:doi/10.1371/journal.pone.0047282#pone-0047282-g002&gt;.
31. Thompson, Melissa Emory, James H. Jones, Anne E. Pusey, Stella Brewer-Marsden, Jane Goodall, David Marsden, Tetsuro Matsuzawa, Toshisada Nishida, Vernon Reynolds, Yukimaru Sugiyama, and Richard W. Wrangham. “Aging and Fertility Patterns in Wild Chimpanzees Provide Insights into the Evolution of Menopause.” <i>Current Biology</i> 17.24 (2007): 2150–156. <i>Science Direct</i>. Elsevier. Web. 1 Dec. 2014. &lt;http://www.sciencedirect.com/science/article/pii/S0960982207022725&gt;.
32. Tutin, Caroline E. G. “Mating Patterns and Reproductive Characteristics/behaviors in a Community of Wild Chimpanzees (Pan Troglodytes Schweinfurthii).” Behavioral Ecology and Sociobiology 6 (1979): 29–38. Print.
33. Van Schaik, Carel P., and Peter M. Kappeler. “Infanticide Risk and the Evolution of Male^female Association in Primates.” <i>Primate Social Evolution</i> 264 (1997): 1687–694. Print.
34. Ziegler, T. E., G. Scheffler, and C. T. Snowdon. “The Relationship of Cortisol Levels to Social Environment and Reproductive Functioning in Female Cotton-top Tamarins, Saguinus Oedipus.” Hormones and Behavior 29 (1995): 407–24. Print.