Hormones, developmental plasticity, and adaptive evolution: Endocrine flexibility as a catalyst for 'plasticity-first' phenotypic divergence

Abstract

Explaining how populations adapt to environments is among the foremost objectives of evolutionary theory. Over generations, natural selection impels the phenotypic distribution of a population based on individual variation in phenotype and fitness. However, environmental conditions can also shape how individuals develop within their lifetime to influence which phenotypes are expressed in a population. It has been proposed that such environmentally-initiated phenotypic variation - also termed developmental plasticity - may enable adaptive evolution under some scenarios. As dynamic regulators of development and phenotypic expression, hormones are important physiological mediators of developmental plasticity. Patterns of hormone secretion, hormone transport, and the sensitivity of tissues to hormones can each be altered by environmental conditions, and understanding how endocrine regulation shapes phenotypic development in an ecologically-relevant context has much to contribute toward clarifying the role of plasticity in evolutionary adaptation. This article explores how the environmental sensitivity of endocrine regulation may facilitate 'plasticity-first' evolution by generating phenotypic variants that precede adaptation to altered or novel environments. Predictions arising from 'plasticity-first' evolution are examined in the context of thyroid hormone mediation of morphological plasticity in Cyprinodon pupfishes from the Death Valley region of California and Nevada, USA. This clade of extremophile fishes diversified morphologically over the last ~20,000 years, and observations that some populations experienced contemporary phenotypic differentiation under recent habitat change provide evidence that hormone-mediate plasticity preceded genetic assimilation of morphology in one of the region's species: the Devils Hole pupfish, Cyprinodon diabolis. This example illustrates how conceptualizing hormones not only as regulators of homeostasis, but also as developmental intermediaries between environment conditions and phenotypic variation at the individual-, population-, and species-levels can enrich our understanding of endocrine regulation both as a facilitator of phenotypic change under shifting environments, and as important proximate mechanisms that may initiate 'plasticity-first' evolutionary adaptation.

Keywords: Adaptation; Devils hole pupfish; Genetic assimilation; Phenotypic plasticity; Plasticity-first evolution; Thyroid hormone.