Wiley-Liss Plenary Symposium Ancient Origins of Human Developmental Plasticity

Animals have the ability to alter development, physiology, growth, and behavior in response to different environmental conditions. These responses represent critical assessments of both external and internal factors. For example, the timing of metamorphosis, hatching, or birth depends on the trade-offs between growth opportunity and mortality risk in the developmental habitat. Physiological sensors compute these trade-offs as a function of energy balance and environmental stress, and effectors initiate physiological, developmental, and behavioral responses to these determinations. The neuroendocrine stress axis provides a means for animals to integrate information from multiple sources and to respond accordingly. Considerable evidence now supports the view that the secretion of hormones critical to development (corticosteroid and thyroid hormones) is controlled by a common neuroendocrine stress pathway involving corticotropin-releasing factor (CRF) and related peptides. CRF produced in the hypothalamus stimulates the biosynthesis and secretion of both thyroid and corticosteroid hormones, leading to accelerated tadpole metamorphosis. Similarly, in mammals CRF of fetal and placental origin has been shown to influence the timing of birth. Studies in several experimental animal models and in humans show that early life experience can have long-term phenotypic consequences. Furthermore, there is evidence that phenotypic expression is strongly influenced by the actions of stress hormones produced during development. The integrated neuroendocrine response to stress, and its role in timing critical life history transitions and establishing long-term phenotypic expression, arose early in the evolution of vertebrates. Am. J. Hum. Biol. 17:44–54, 2005. # 2004 Wiley-Liss, Inc. There are numerous examples in animals and plants in which a given genotype can generate multiple phenotypes depending on the environmental conditions experienced by the organism during development (Stearns, 1991). Indeed, recent studies show that the environment experienced by the mother can have profound influence on phenotypic expression in the offspring, and these effects can be transmitted through multiple generations (‘‘maternal environmental effects’’) (Champagne et al., 2003; Mousseau and Fox, 1998; Wolf et al., 1998). Similar phenomena have been described in humans (Barker, 1992, 1994; Barker and Clark, 1997; Kaplan, 1954; Lasker, 1969), and the importance of environmental effects during early development for human health has received increasing attention in recent years (Bateson et al., 2004). However, we still understand little about environmental effects on human development, and the underlying developmental and physiological mechanisms. Themorphological, physiological, and behavioral characters of modern humans arose through hundreds of millions of years of vertebrate evolution. Most of the basic mechanisms that govern human development and physiology are present in primitive extant vertebrates, and even invertebrate species (Denver, 1999; Gilbert and Bolker, 2001; Shubin et al., 1997). Thus, it is not surprising that the adaptive solutions that humans have developed are derived evolutionarily from mechanisms that were in place in the earliest vertebrates. This review will focus on the underlyingphysiological basis for developmental plasticity as discovered through the study of experimental animals. The vertebrate animals 2004 Wiley-Liss, Inc. Contract grant sponsor: National ScienceFoundation (NSF); Contract grant numbers: IBN 9974672; IBN 0235401 (to R.J.D.). *Correspondence to: Dr. Robert J. Denver, Department of Molecular, Cellular andDevelopmentalBiology, 3065CNatural Science Building, The University of Michigan, Ann Arbor, MI 48109-1048. E-mail: [email protected] Received 7 September 2004; Accepted 1 October 2004 Published online in Wiley InterScience (www.interscience. wiley.com). DOI: 10.1002/ajhb.20098 AMERICAN JOURNAL OF HUMAN BIOLOGY 17:44–54 (2005)