title: Prenatal stress effects in a wild, long-lived primate: predictive adaptive responses in an unpredictable environment.
abstract: Prenatal maternal stress affects offspring phenotype in numerous species including humans, but it is debated whether these effects are evolutionarily adaptive. Relating stress to adverse conditions, current explanations invoke either short-term developmental constraints on offspring phenotype resulting in decelerated growth to avoid starvation, or long-term predictive adaptive responses (PARs) resulting in accelerated growth and reproduction in response to reduced life expectancies. Two PAR subtypes were proposed, acting either on predicted internal somatic states or predicted external environmental conditions, but because both affect phenotypes similarly, they are largely indistinguishable. Only external (not internal) PARs rely on high environmental stability particularly in long-lived species. We report on a crucial test case in a wild long-lived mammal, the Assamese macaque (Macaca assamensis), which evolved and lives in an unpredictable environment where external PARs are probably not advantageous. We quantified food availability, growth, motor skills, maternal caretaking style and maternal physiological stress from faecal glucocorticoid measures. Prenatal maternal stress was negatively correlated to prenatal food availability and led to accelerated offspring growth accompanied by decelerated motor skill acquisition and reduced immune function. These results support the 'internal PAR' theory, which stresses the role of stable adverse internal somatic states rather than stable external environments.
authors.affiliation: Department of Behavioural Ecology, University of Göttingen, 37077 Göttingen, Germany abergha@gwdg.de.
authors.forename: Andreas
authors.identifier: 0000-0002-3317-3392
authors.initials: A
authors.lastname: Berghänel
authors.affiliation: Endocrinology Laboratory, German Primate Center, 37077 Göttingen, Germany.
authors.forename: Michael
authors.initials: M
authors.lastname: Heistermann
authors.affiliation: Department of Behavioural Ecology, University of Göttingen, 37077 Göttingen, Germany Research Group Primate Social Evolution, German Primate Center, 37077 Göttingen, Germany.
authors.forename: Oliver
authors.initials: O
authors.lastname: Schülke
authors.affiliation: Department of Behavioural Ecology, University of Göttingen, 37077 Göttingen, Germany Research Group Primate Social Evolution, German Primate Center, 37077 Göttingen, Germany.
authors.forename: Julia
authors.initials: J
authors.lastname: Ostner
mesh_terms: D000222:Adaptation, Physiological; D000818:Animals; D004777:Environment; D005260:Female; D008251:Macaca / Q000502:physiology*; D010641:Phenotype; D011247:Pregnancy; D011297:Prenatal Exposure Delayed Effects; D012098:Reproduction; D013312:Stress, Physiological
keywords: developmental constraints; developmental origins of health and disease; gestational stress; life history; resource allocation; silver spoon