Different ontogenetic patterns of testosterone production reflect divergent male reproductive strategies in chimpanzees and bonobos

Highlights

• Bonobos exhibit minimal increases in testosterone during puberty, unlike chimpanzees.

• Increases in testosterone with age are clear among chimpanzee, but not bonobo, males.

• Bonobos' stable testosterone levels are likely tied to reduced mating competition.

• Testosterone production across development may be shaped by adult mating strategies.

Abstract

Male reproductive effort is often strongly related to levels of the steroid hormone testosterone. However, little research has examined whether levels of testosterone throughout development might be tied to individual or species differences in the reproductive strategies pursued by adult males. Here, we tested the hypothesis that inter-specific differences in male reproductive strategy are associated with differences in the pattern of testosterone production throughout early life and puberty. We compared testosterone levels from infancy to adulthood in two closely related species where levels of mating competition and male–male aggression differ significantly, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We predicted that the reduction in male mating competition found in bonobos would be accompanied by a lesser developmental increase in testosterone production. We performed radioimmunoassay of salivary testosterone levels in a mixed-longitudinal sample of both species, collected from individuals living in semi free-ranging populations. This allowed us to examine the effects of development in a more naturalistic setting than possible in a zoo or laboratory. We found that among chimpanzees, testosterone levels declined slightly from infancy to juvenility, then remained low until increasing markedly during adolescence (with pubertal increases most pronounced among males). In contrast, there was little change in testosterone production with age in bonobos of either sex, with levels of testosterone consistent throughout infancy, juvenility, and the transition to adulthood. Our data are therefore consistent with the hypothesis that the ontogenetic pattern of testosterone production can be subject to rapid evolutionary change, shifting in association with species differences in male reproductive strategy.

Introduction

Investment in reproduction among males can be divided into both the production of gametes and the allocation of energy towards somatic and behavioral strategies that facilitate mating opportunities [1], [2]. The steroid hormone testosterone (abbreviated as T) is particularly important in influencing these latter two elements of male reproductive strategy, increasing muscle mass, enhancing libido, and stimulating aggressive and dominance behaviors in a given season or situation [3], [4], [5], [6].

While the association between testosterone and male reproductive effort has been well-documented in adults of numerous taxa, our understanding of how development mediates this relationship is less clear. According to life history theory, the production of testosterone across ontogeny should differ between species or individuals to facilitate the optimal allocation of energy toward growth, maintenance, and reproduction across the lifespan [1], [7]. Since high levels of testosterone can have a deleterious effect on the immune system [2], [8], production of testosterone may be minimized in situations or life stages where it is not sufficiently advantageous [5], [9]. Accordingly, testosterone levels typically remain low during juvenility, only beginning to increase at puberty in conjunction with reproductive maturation [10], [11], [12]. Despite this general developmental pattern being present across mammals, there may be important species differences in the precise patterns of testosterone production throughout development that reflect divergent male reproductive strategies in adulthood. This possibility is particularly compelling in light of the growing body of evidence that phenotypic changes between species commonly arise through evolutionary shifts in developmental trajectories [13], [14], [15].

Several studies have begun to investigate whether individual and species-level variation in the ontogeny of androgen production exist in association with differing adult reproductive strategies, using non-human primate models to examine these effects over an extended period of ontogeny. Within mandrills (Mandrillus sphinx) and chacma baboons (Papio hamadryas ursinus), individual differences in the production of testosterone during puberty have been found to correlate with dominance ranks among adult males [16], [17]. Similarly, in orangutans (Pongo pygmaeus), males who retained subadult body size into adulthood (a viable strategy in this species to obtain sneaky mating opportunities without overt physical competition) were found to show smaller increases in testosterone during adolescence than males who developed their body size fully [18]. In addition, differences between baboon species in the timing and magnitude of the pubertal testosterone increase have been found to reflect inter-specific variation in the length of alpha male tenure and the association between rank and mating success [19]. These results support the hypothesis that within and across species, variation in the developmental trajectory of androgen production is central to the relationship between testosterone and reproductive effort among adult males.

These prior studies of testosterone production throughout development have largely focused on the pubertal increase in testosterone levels, since the period of adolescence represents an important transition between an individual's focus on growth and its focus on reproduction. However, individuals or species may also vary in their production of testosterone even before puberty. In a number of species, from humans to yellow baboons (Papio cynocephalus) and cotton-top tamarins (Saguinus oedipus), males and females show a neonatal elevation in testosterone that lasts for the first few weeks or even months after birth [11], [20], [21]. Though there is considerable debate about the function of this neonatal testosterone elevation [22], [23], one possibility is that variation in its duration or magnitude contributes to differences in reproductive capabilities among adult males [20], [24].

Here we test the hypothesis that species differences in male mating strategy are associated with variation in the ontogenetic patterns of testosterone production across the entire lifespan. We do so by comparing testosterone levels from infancy into adulthood in two closely-related ape species, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Chimpanzees and bonobos provide an ideal test case for this hypothesis, as they have been found to differ in both their reproductive strategy and in broader aspects of their ontogeny, despite having diverged from one another as recently as 850 kya [25].

Differences in male reproductive strategy between chimpanzees and bonobos appear to derive largely from the increased social gregariousness and sexual receptivity of bonobo females relative to chimpanzee females, presuming that the last common ancestor of the two species was chimpanzee-like [26], [27]. Bonobo females associate with males and engage in extensive non-conceptive sexual behavior throughout their menstrual cycle, while associations between male and female chimpanzees peak during the period of female sexual swelling, with copulations largely limited to this period [28], [29], [30], [31]. Correspondingly, it has been argued that competition for dominance rank and coercive aggression are less effective means of obtaining conceptive mating opportunities for bonobo males than for male chimpanzees [27], [32], [33], [34]. In support of this argument, bonobo males exhibit less frequent and less severe displays of aggressive behavior of all types than chimpanzee males, be it intra-group aggression, inter-group aggression, or even inter-specific predation [26], [35], [36], [37], [38], [39], [40]. Bonobos have also been found to show a lesser sex difference in androgen production relative to chimpanzees, lesser increases in male androgen levels when females are peri-ovulatory than found among male chimpanzees, and a weaker correlation on the whole between basal testosterone level and dominance rank among adult males [41], [42], [43], [44]. These two species therefore provide an excellent opportunity to test whether divergent male reproductive strategies in closely-related taxa are associated with broader differences in their endocrine maturation.

In addition to their divergent reproductive strategies, bonobos and chimpanzees have been found to differ in numerous aspects of their development. In particular, bonobos exhibit delays in development relative to chimpanzees in features of their morphology [45], [46], behavior [14], [15], [47], and cognition [14]. These distinctions provide support for the possibility that the ontogenetic pattern of testosterone production has also shifted between these two species, given the evidence from numerous taxa that hormones are a central mechanism in facilitating the pace of developmental transitions [48], [49].

No evidence exists at present to compare endocrine maturation between bonobos and chimpanzees, since to our knowledge no prior study of bonobo endocrine ontogeny has been performed. Existing studies of endocrine maturation in chimpanzees have consistently found that male testosterone levels increase during puberty, with these increases coinciding with growth in body weight and testicular volume [50], [51], [52], [53], [54], [55], [56], [57]. In captive populations, male chimpanzees begin to show elevations in testosterone between 6 and 7 years of age [50], [51], [52], [54], [57], with the onset of spermatogenesis occurring between 7 and 9 years of age [58], [59]. The only existing study of testosterone development among a small sample of wild chimpanzees indicates a similar developmental increase, occurring at a slightly later age [56]. Despite the relatively large number of studies documenting patterns of testosterone production throughout chimpanzee development, few have incorporated individuals from a broad developmental window (encompassing infancy, juvenility, adolescence, and adulthood). Moreover, these studies have primarily been conducted in laboratory environments, where asocial or minimally social housing conditions may have diminished any effects of dominance rank or social behavior on testosterone production [60]. This study represents one of the first opportunities to investigate testosterone production in chimpanzees ranging from infancy into adulthood, utilizing semi free-ranging study populations where individuals live in mixed-age and sex groups closely resembling those found in the wild [61].

Our major prediction was that bonobos would show a lesser developmental increase in testosterone production than chimpanzees, given their lesser mating competition as adults and their maintenance of numerous juvenile characteristics in adulthood [15], [27]. Our alternative hypothesis was that bonobos and chimpanzees would differ little in their ontogeny of testosterone production, given their genetic similarity [25]. We tested these predictions by measuring salivary testosterone levels from infancy into adulthood among bonobos and chimpanzees, making it possible for us to examine the contributions of both neonatal and pubertal testosterone elevations to the overall trajectory of testosterone production in each species. We examined testosterone in both sexes to assess the degree to which male patterns of development diverged from those of females.