Evolutionary endocrinology: Integrating proximate mechanisms, ontogeny, and evolved function

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Natural selection leads to the evolution of strategies that tend to optimize the allocation of resources to the competing somatic and reproductive demands faced by any organism. This theoretical approach, known as life history theory, is useful for understanding unavoidable trade-offs in resource allocation and the resulting variation in phenotypes (e.g., physical attributes, expressed behaviors, the number and size of offspring, etc.) (Charnov 1993; Stearns 1992). In recent years, life history theory has begun to influence research on the proximate mechanisms mediating ontogenetic strategies. The endocrine system plays a central role in coordinating ontogenetic processes and modulating cross-talk among different functional domains (e.g., hypothalamic–pituitary–gonadal and hypothalamic–pituitary–adrenal axes). These processes are integral to the evolution of phenotypic plasticity (a key feature of adaptive responses) in developmental schedules and other life-history traits. From conception to death, hormones orchestrate growth, differentiation, maintenance, reproduction, and senescence. Pheromones may help parents-to-be to attract each other (Kohl et al., 2001; Hays, 2003). Androgen steroids increase libido encouraging them to mate (Hutchinson, 1995; Stern and McClintock, 1998). Gonadotrophins and gonadal steroids mediate gamete maturation and release. Endometrial steroids intervene in the capacitation of spermatozoa and chemotaxis, luring them towards the oocyte. Recognition, binding, and fusion between sperm and oocyte, and the consequent activation of the egg are mediated by a multitude of hormones (Sun et al., 2005). After fertilization, but before development of the endocrine system, chemical signals help guide cleavage, cell differentiation, migration, and growth. Once developed, the endocrine system transmits information between cells regarding internal and external conditions, coordinating a intricate dance between the epigenome and the genome, steering the organism through its ontogenetic road map. All organisms of a given species follow a similar ontogenetic road map. Yet, as environmental opportunities, restrictions, and challenges are heterogeneously distributed between and within populations, each individual passes life-history mileposts at its own speed and according to its own strategy. The endocrine system is an integral part of the mechanisms that provide organisms with the plasticity and dynamism that are crucial for adapting to their individual contexts. The challenges to be met are broad in type and temporal scales. Some challenges involve almost all biologic systems and take place over long periods of time, such as coordinating proportionate growth or undergoing sexual maturation. Others involve fewer tissues but need to be achieved within minutes or hours, such as adjusting oxygen or blood glucose levels. Some challenges are predictable, such as the sequences of night and day, or the succession of changes that follow conception. Other challenges, such as a tornado or an aneurysm, may be less predictable. Organisms rely on the endocrine system to regulate responses to these challenges as well as to inform ontogenetic strategies based on them. When and how much to grow at each life stage, when to begin sexual maturation, when to stop growing, the timing of the first reproductive venture, the length of inter-birth intervals, and when to stop reproducing are just a few examples of critical life history ‘‘decisions’’ mediated by hormonal pathways. Ontogenetic strategies are modified through neuroendocrine cues that trigger changes in gene expression. Phenotypic plasticity is ultimately achieved by changes in DNA methylation patterns and chromatin remodeling. These epigenetic changes provide great dynamism to genotypic expression. Recent research developments suggest that while some epigenetic DNA methylation patterns are preserved through multiple generations, others are not as stable as originally believed and can change in response to postnatal environmental stimuli at different times within an individual’s life span (McGowan et al., 2008; Szyf et al., 2008). The epigenome, informed by neuro-endocrine cues, is critical for fine tuning the expression of the more static genotype in response to the demands that the environment places on the phenotype. Given the dynamic and complex nature of the endocrine system, a holistic approach to its study should consider not only the longitudinal variation of hormones across days, seasons, and life stages, but also its interactions with the nervous system and the epigenome. Anthropologists are in the privileged position necessary for conducting the multidisciplinary research that will help to realize this admittedly daunting research agenda. The collection of high quality longitudinal data achieved through an intimate knowledge of study participants allows for the description of normal ranges of endocrine function and its variability in response to environmental challenges in nonclinical populations exposed to a broad range of social, economic, and physical contexts. The 2008 Plenary Session of the Human Biology Association explored recent advances in the study of endocrine pathways approached from this holistic perspective. The