Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2020 Oct 6;117(40):24909-24919.
doi: 10.1073/pnas.2004018117. Epub 2020 Sep 21.

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

Chelsea J Weibel  1 , Jenny Tung  2   3   4   5 , Susan C Alberts  2   3   4   5 , Elizabeth A Archie  1   4
Affiliations

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

Chelsea J Weibel et al. Proc Natl Acad Sci U S A. .

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.

Keywords: adaptive developmental plasticity; early-life adversity; fitness; internal predictive adaptive response model; life history.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Visual depiction of the fitness crossovers predicted by the iPAR model. The plot shows the iPAR model’s predicted patterns of LRS (y axis) as a function of the quality of the early-life environment or adult somatic state (x axis: good or poor for each predictor), stratified by the pace of reproduction (accelerated or typical/delayed). Specifically, Nettle and Bateson’s (60) second prediction is that accelerated reproduction (solid blue line) promotes higher LRS when individuals experience poor early-life conditions, compared with those with delayed reproduction (dashed purple line). However, accelerated reproduction results in reduced LRS when early-life conditions are good. Their third prediction is a logical extension of the first two predictions: individuals who exhibit poor somatic states in adulthood will experience higher LRS if they accelerate reproduction, and those with good somatic states will experience higher LRS if they delay reproduction. The fitness crossover is necessary for adaptive developmental plasticity because it requires the optimal phenotype (i.e., the optimal reproductive strategy) to be state dependent. If the fitness crossover does not exist, then one phenotype is optimal under all conditions, making it adaptive, but not an adaptive response to developmental conditions. The figure is adapted from Monaghan (37) and Nettle and Bateson (60).
Fig. 2.
Fig. 2.
Cumulative early-life adversity is not linked to the timing or pace of reproduction in female baboons (full model results are in SI Appendix, Table S4). Plots depict the relationship between cumulative early-life adversity and age at first live birth (n = 211; P = 0.66) (A), duration of surviving IBIs (plotted on a log scale; n = 452; P = 0.69) (B), and the combined reproductive pace (n = 32; P = 0.73) (C). Colors indicate the number of adverse conditions occurring in early life. All points are jittered along the x axis to increase readability.
Fig. 3.
Fig. 3.
Accelerated reproduction does not result in higher LRS for individuals that experienced early-life adversity. (A) Predicted relationships between early-life adversity and LRS under the iPAR model (Top) and an alternative in which accelerated reproduction is advantageous, independent of early-life experience (Bottom). (B–E) The relationship between LRS and measures of early-life adversity, stratified by pace of reproduction. The four rows show the results for each of the four measures of early-life adversity: cumulative early-life adversity (B), maternal death (C), competing sibling (D), and maternal social isolation (E). The three columns show the results for each of the three measures of reproductive pace: age at first birth (Left), average surviving IBI (Middle), and combined reproductive pace (Right). The points represent the raw data, based on whether the pace of reproduction value was above (accelerated: blue circles) or below (delayed: purple triangles) the median value. Lines show predicted values from the linear model that best fit the data when holding pace of reproduction at the bottom 25th percentile (delayed: purple dashed) or the top 25th percentile (accelerated: blue solid). All results were more similar to the alternative prediction (A, Bottom) than the iPAR model prediction (A, Top). The only case of a statistically supported interaction (C, Right) was in the opposite direction predicted by the iPAR model, such that accelerated reproduction only predicted higher fitness in the absence of early-life adversity. Data points in B–D are jittered along the x axis to increase readability.
Fig. 4.
Fig. 4.
Accelerated reproduction is not linked to higher LRS for females with short lifespans. Plots depict the relationship between female lifespan, as a measure of her somatic quality, and her LRS, partitioned by whether the female’s pace of reproduction measure was above (accelerated: blue circles) or below (delayed: purple triangles) the median value of the dataset. A is partitioned by age at first live birth, B is partitioned by mean IBI, and C is partitioned by the combined reproductive pace measure. On each plot, the points represent the raw data, and the lines represent the predicted values from the linear model that best fit the data when holding pace of reproduction at the bottom 25th percentile (delayed: purple dashed) or the top 25th percentile (accelerated: blue solid). For all of these analyses, the model with the interaction was a better fit for the data (age at first birth: ΔAIC = 4.064 [n = 145]; IBI: ΔAIC = 23.553 [n = 110]; combined reproductive pace: ΔAIC = 17.381 [n = 81]). However, the interaction was in the direction opposite the iPAR model’s prediction: females only accrued higher LRS by accelerating reproduction if they also led long lives.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Felitti V. J. et al. ., Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study. Am. J. Prev. Med. 14, 245–258 (1998). - PubMed
    1. Lynch J., Smith G. D., A life course approach to chronic disease epidemiology. Annu. Rev. Public Health 26, 1–35 (2005). - PubMed
    1. O’Rand A. M., Hamil-Luker J., Processes of cumulative adversity: Childhood disadvantage and increased risk of heart attack across the life course. J. Gerontol. B Psychol. Sci. Soc. Sci. 60, 117–124 (2005). - PubMed
    1. Roseboom T., de Rooij S., Painter R., The Dutch famine and its long-term consequences for adult health. Early Hum. Dev. 82, 485–491 (2006). - PubMed
    1. Miller G. E., Chen E., Parker K. J., Psychological stress in childhood and susceptibility to the chronic diseases of aging: Moving toward a model of behavioral and biological mechanisms. Psychol. Bull. 137, 959–997 (2011). - PMC - PubMed

Publication types

LinkOut - more resources