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• W3119163890 abstract "In species with intense male competition, reproducing at the wrong time can have dire consequences for females. A new study of wild gelada monkeys finds that females delay or accelerate puberty to moderate the risks of inbreeding and infanticide. In species with intense male competition, reproducing at the wrong time can have dire consequences for females. A new study of wild gelada monkeys finds that females delay or accelerate puberty to moderate the risks of inbreeding and infanticide. Female mammals must overcome significant obstacles to breed successfully in the wild. Many of these challenges come from the physical environment, as females struggle to keep their babies warm and well fed. But, how do females deal with the threats posed by other members of their species, especially by males? Over 40 years ago, biologists studying laboratory mice demonstrated that exposing females to a novel male triggers a series of dramatic effects on reproduction. Because male mice are likely to kill any young offspring they have not sired, pregnant females spontaneously abort to avoid the costs of pregnancy (the ‘Bruce’ effect). By contrast, unmated females rapidly enter estrus, allowing them to breed with the new male (the ‘Whitten’ effect). Immature females undergo accelerated puberty for the same reason (the ‘Vandenbergh’ effect1Vandenbergh J.G. Effect of the presence of a male on the sexual maturation of female mice.Endocrinology. 1967; 81: 345-349Crossref PubMed Scopus (183) Google Scholar), but will delay puberty if the only males available are relatives. These effects do not require the physical presence of a male but are mediated by exposure to the chemical signals in male urine. So far, clear evidence for these effects has been limited to species with well-developed olfactory systems, primarily rodents and livestock, and in captivity where enclosed conditions make chemical signals easy to detect. Nevertheless, there has been an enduring fascination with the possibility that even humans could retain vestiges of these mechanisms2Comfort A. Likelihood of human pheromones.Nature. 1971; 230: 432-433Crossref PubMed Scopus (85) Google Scholar or may have replaced them with more elaborate ways of calibrating reproduction to social cues3Belsky J. Steinberg L. Draper P. Childhood experience, interpersonal development, and reproductive strategy: An evolutionary theory of socialization.Child Dev. 1991; 62: 647-670Crossref PubMed Google Scholar. A new study in this issue of Current Biology by Amy Lu, Jacinta Beehner, and colleagues4Lu A. Feder J.A. Snyder-Mackler N. Bergman T.J. Beehner J.C. Male-mediated maturation in wild geladas.Curr. Biol. 2021; 31: 214-219Abstract Full Text Full Text PDF PubMed Scopus (4) Google Scholar reports that turnovers in male leadership trigger reproductive maturation in female geladas, providing surprising evidence of the Vandenbergh effect in a wild primate. Geladas are large, baboon-like monkeys that thrive on the grasslands of highland Ethiopia. Geladas live in complex, multilevel social systems5Grueter C.C. Qi X. Li B. Li M. Multilevel societies.Curr. Biol. 2017; 27: R984-R986Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar. At first glance across the plateau, herds of geladas are reminiscent of wildebeest, with scores of monkeys shuffling across the landscape, methodically grunting and munching on grass. A closer look reveals smaller clusters (‘units’), each comprised of a few related females overseen by an ostentatiously-maned male who dwarves the females in size (Figure 1). These ‘leader’ males enjoy the privilege of exclusive mating rights to females in their units. At monkey-eye level, the apparent tranquillity gives way to a seething tension. Not all males have females of their own. Instead, bachelors loom near the established units, waiting for signs of weakness, harassing and threatening the leaders. Given the large number of roving males, leaders face a near constant risk of being deposed6Snyder-Mackler N. Alberts S.C. Bergman T.J. Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups.Proc. R. Soc. Lond. B Biol. Sci. 2012; 279: 3788-3795Crossref PubMed Scopus (55) Google Scholar. The consequences of a male takeover are swift and brutal. New leaders attack and kill the young infants that were sired by their predecessors, resulting in a 32-fold increase in infant deaths7Beehner J.C. Bergman T.J. Infant mortality following male takeovers in wild geladas.Am. J. Primatol. 2008; 70: 1152-1159Crossref PubMed Scopus (45) Google Scholar. Without having to nurse these infants, the females resume cycling sooner, giving the conquering male a head start at siring his own offspring. What is a female to do? The new study by Lu and colleagues4Lu A. Feder J.A. Snyder-Mackler N. Bergman T.J. Beehner J.C. Male-mediated maturation in wild geladas.Curr. Biol. 2021; 31: 214-219Abstract Full Text Full Text PDF PubMed Scopus (4) Google Scholar reveals one way that females can game this system. Observers assiduously tracked female reproductive maturation in multiple gelada units in Ethiopia's Simien Mountains National Park over a period of 14 years, observing 28 male takeovers. Conveniently for the researchers, female geladas flash a clear signal of their breeding condition in the form of a bubbly swelling on their chests. Females were nearly three times as likely to undergo puberty in the three months after a male takeover than at other times, conceiving about five months earlier than usual. Why does this matter? In the gelada population, male takeovers were frequent, occurring every 2.7 years on average. This is a tight window for females to fit the time it takes to conceive, gestate and nurse a young infant. If a female conceives early in a male’s tenure, there is a good chance her first infant will be old enough to be spared when the next male takes over. The researchers found that females who matured following a takeover had their first births at a younger age and earned an extra year to reproduce safely compared with females who matured at other times. The researchers also observed that daughters of a current leader male matured five months later than average. In combination, these effects allow females to avoid the risk of inbreeding and switch rapidly to reproductive condition when an unrelated male comes along. The timing was no mere coincidence: using fecal samples, the researchers were able to document an abrupt change in reproductive hormones in all young females following male takeovers. For some females, estrogen levels spiked too early in development to have any effect, but the older a female was, the more likely she would begin having reproductive cycles. Without the luxury of controlled experimental conditions, data from wild primates are notoriously noisy. Thus, it is notable how unambiguous the gelada results of Lu and colleagues4Lu A. Feder J.A. Snyder-Mackler N. Bergman T.J. Beehner J.C. Male-mediated maturation in wild geladas.Curr. Biol. 2021; 31: 214-219Abstract Full Text Full Text PDF PubMed Scopus (4) Google Scholar are. Male takeovers induced a rapid and dramatic physiological response in females that is clearly consistent with the Vandenbergh effect. Geladas are also the only primate to show clear evidence of the Bruce effect: some 80% of pregnant geladas abort, within a matter of days, if a male takeover occurs8Roberts E.K. Lu A. Bergman T.J. Beehner J.C. A Bruce effect in wild geladas.Science. 2012; 335: 1222-1225Crossref PubMed Scopus (81) Google Scholar. These responses are unlikely to be mere evolutionary vestiges of the chemosensory mechanisms observed in rodents. Geladas, like most monkeys and apes, lack a functional vomeronasal organ, the specialized olfactory system that other species use to process chemical signals. Vision and vocal communication offer more versatility for primates that are active in the daytime and live in tight-knit social groups. Indeed, geladas live in close proximity to hundreds of other individuals and traverse the same spaces, so females are naturally exposed to a barrage of sensory cues from dozens of males. To accomplish the same effects observed in rodents, geladas would require entirely new mechanisms. Lu and colleagues4Lu A. Feder J.A. Snyder-Mackler N. Bergman T.J. Beehner J.C. Male-mediated maturation in wild geladas.Curr. Biol. 2021; 31: 214-219Abstract Full Text Full Text PDF PubMed Scopus (4) Google Scholar propose that social cues are cognitively processed, allowing the monkeys to evaluate a diverse array of information. This would make it less likely that female biology is simply being hijacked by a mechanism that benefits the male. Monkeys are known to have a sophisticated understanding of their social worlds9Cheney D.L. Seyfarth R.M. Baboon Metaphysics: The Evolution of a Social Mind. University of Chicago Press, Chicago, IL2008Google Scholar, but we do not yet understand how such knowledge could become so directly biologically embedded10Beehner J.C. Lu A. Reproductive suppression in female primates: A review.Evol. Anthropol. 2013; 22: 226-238Crossref PubMed Scopus (45) Google Scholar. Psychosocial stress is one well-known pathway by which neurocognitive processing of social information can exert rapid, profound effects on physiology11Sapolsky R.M. Why Zebras Don't Get Ulcers. W.H. Freeman and Co, New York1998Google Scholar. In this case, it is doubtful that the young geladas experience takeovers as a psychological trauma, as they face little immediate danger. In a related baboon species, risky male takeovers did not induce stress in females unless they were pregnant or nursing young infants12Beehner J.C. Bergman T.J. Cheney D.L. Seyfarth R.M. Whitten P.L. The effect of new alpha males on female stress in free-ranging baboons.Anim. Behav. 2005; 69: 1211-1221Crossref Scopus (112) Google Scholar. Could other cases of the Vandenbergh effect be hidden in plain sight, perhaps even in humans? This possibility was raised 30 years ago after studies documented accelerated menarche among girls whose fathers were absent from the home13Surbey M.K. Family composition, stress, and the timing of human menarche.in: Ziegler T.E. Bercovitch F.B. Socioendocrinology of Primate Reproduction. Wiley-Liss, New York1990: 11-32Google Scholar. Perhaps, it has been argued, it is adaptive for girls to use cues from men in the household to program future reproductive strategies, starting with a younger or older age of childbirth3Belsky J. Steinberg L. Draper P. Childhood experience, interpersonal development, and reproductive strategy: An evolutionary theory of socialization.Child Dev. 1991; 62: 647-670Crossref PubMed Google Scholar. Does the work on geladas lend credence to these hypotheses? It is sure to be cited as doing so. These findings demonstrate the potential for psychosocial mechanisms to impact development in a long-lived species with a reproductive system not so different from our own. However, the analogy between humans and non-humans is weak. The effects in geladas, as in rodents, occur in the context of two powerful selection pressures — inbreeding risk and male infanticide — that are minimally relevant in human families. Moreover, the effects of males on the age of maturity in geladas are probably incidental. Instead, females mature when the timing is right, in spite of their age. Even the gelada study’s authors urge appropriate caution in interpreting whether the mechanisms they report are specifically adaptive for females. Messing with the natural course of puberty might have negative consequences, particularly if smaller females are less successful. Ultimately, gelada females appear to make the best of a very difficult situation, and they surely hold more secrets to be discovered. In the battle of the sexes, male geladas come armed to the teeth, while the females are quietly playing chess. Male-Mediated Maturation in Wild GeladasLu et al.Current BiologyNovember 5, 2020In BriefThis is the first report of male-mediated maturation in a wild primate. Lu et al. find that maturations in wild geladas are more likely after a new male arrives. While new males accelerate maturations, this is countered by overlap with her father. All females, even those too young to mature, showed elevations in estrogens upon new male arrival. Full-Text PDF" @default.
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• W3119163890 title "Primate Reproduction: When Timing Is Everything" @default.
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