Testing the evolutionary basis of the predictive adaptive response hypothesis in a preindustrial human population

Abstract

Background and objectives: The thrifty phenotype hypothesis proposes that late-life metabolic diseases result from mismatch between early-life and adulthood nutrition. More recently, the predictive adaptive response (PAR) hypothesis has suggested that poor early-life environmental conditions induce metabolic changes that maximize health and fitness in similarly poor adult conditions, but reduce fitness if conditions later improve. Therefore, later-life survival and reproduction should be maximized where environmental conditions during development and adulthood match, but few studies in humans have addressed the consequences of poor early conditions on fitness traits in varying later conditions.Methodology: We tested key evolutionary predictions of the PAR hypothesis using detailed longitudinal data with several environmental parameters from a natural fertility preindustrial human population, to investigate how combinations of early- and late-life environmental conditions affected annual probabilities of survival and reproduction.Results: We found no suggestion that fitness was maximised when developmental and later-life conditions matched, but rather poor environmental conditions during development or later life and their combinations were associated with lower survival.Conclusions and implications: Our results are more consistent with predictions of ‘silver spoon’ models, whereby adverse early-life conditions are detrimental to later health and fitness across all environments. Future evolutionary research on understanding metabolic disease epidemiology should focus on determining whether adaptive prediction maximizes infant survival where conditions match during development and immediately after birth, rather than drawing attention to the unlikely long-term fitness benefits of putative metabolic changes associated with poor early nutrition.