Accelerated reproduction is not an adaptive response to early-life adversity in wild baboons

Abstract

In humans and other long-lived species, harsh conditions in early life often lead to profound differences in adult life expectancy. In response, natural selection is expected to accelerate the timing and pace of reproduction in individuals who experience some forms of early-life adversity. However, the adaptive benefits of reproductive acceleration following early adversity remain untested. Here, we test a recent version of this theory, the internal predictive adaptive response (iPAR) model, by assessing whether accelerating reproduction following early-life adversity leads to higher lifetime reproductive success. We do so by leveraging 48 y of continuous, individual-based data from wild female baboons in the Amboseli ecosystem in Kenya, including prospective, longitudinal data on multiple sources of nutritional and psychosocial adversity in early life; reproductive pace; and lifetime reproductive success. We find that while early-life adversity led to dramatically shorter lifespans, individuals who experienced early adversity did not accelerate their reproduction compared with those who did not experience early adversity. Further, while accelerated reproduction predicted increased lifetime reproductive success overall, these benefits were not specific to females who experienced early-life adversity. Instead, females only benefited from reproductive acceleration if they also led long lives. Our results call into question the theory that accelerated reproduction is an adaptive response to both nutritional and psychosocial sources of early-life adversity in baboons and other long-lived species.

Male-Mediated Maturation in Wild Geladas

“…Moreover, a recent study on yellow baboons (Papio cynocephalus) demonstrated that the fitness effects of a longer life far outweigh the fitness effects of an accelerated reproductive schedule. 52 This opens the door to a third hypothesis: that male-mediated maturation is not adaptive but simply the Please cite this article in press as: Lu et al, Male-Mediated Maturation in Wild Geladas, Current Biology (2020), https://doi.org/10.1016/ j.cub.2020.10.003 Report byproduct of selection for females to retain sensitivity to new breeding males. Specifically, the Bruce effect (male-mediated pregnancy loss) can mitigate the costs of infanticide across the life course.…”

The Goldilocks effect: female geladas in mid-sized groups have higher fitness

“…Based on a recent analysis on female maturations for this population [ 65 ], we expect that females in small units will have later ages at maturation and first birth to avoid inbreeding (since their fathers have longer tenures), and we expect that females in large units will have earlier ages at maturation and first birth due to the ‘Vandenbergh effect’ that accompanies male takeovers. However, even if these predictions are supported in future analyses, we do not expect these unit size differences to significantly alter our reproductive success estimates for two reasons: first, the observed range in age at first birth in this population is narrow [ 57 ], and second, in similarly long-lived primates, age at first birth had a very modest impact on variation in lifetime fitness [ 66 , 67 ]. Future analyses that address the potential for different female reproductive strategies, which require more complete female lifespans than we have currently, will allow us to determine the effects of unit size on realized lifetime reproductive success.…”

Birth timing generates reproductive trade-offs in a non-seasonal breeding primate

“…Several reasons might explain why offspring survival might be prioritized over maternal reproductive pace. First, lifespan and offspring survival are the primary components of female lifetime reproductive success in long-lived species such as baboons, while reproductive pace may be less important [52]. Second, shorter IBIs might compromise infant survival independently of the effect of birth timing and are thus not necessarily adaptive [7].…”