Phenotypic integration and independence: Hormones, performance, and response to environmental change

Abstract

Hormones coordinate the co-expression of behavioral, physiological, and morphological traits, giving rise to correlations among traits and organisms whose parts work well together. This article considers the implications of these hormonal correlations with respect to the evolution of hormone-mediated traits. Such traits can evolve owing to changes in hormone secretion, hormonal affinity for carrier proteins, rates of degradation and conversion, and interaction with target tissues to name a few. Critically, however, we know very little about whether these changes occur independently or in tandem, and thus whether hormones promote the evolution of tight phenotypic integration or readily allow the parts of the phenotype to evolve independently. For example, when selection favors a change in expression of hormonally mediated characters, is that alteration likely to come about through changes in hormone secretion (signal strength), changes in response to a fixed level of secretion (sensitivity of target tissues), or both? At one extreme, if the phenotype is tightly integrated and only the signal responds via selection's action on one or more hormonally mediated traits, adaptive modification may be constrained by past selection for phenotypic integration. Alternatively, response to selection may be facilitated if multivariate selection favors new combinations that can be easily achieved by a change in signal strength. On the other hand, if individual target tissues readily "unplug" from a hormone signal in response to selection, then the phenotype may be seen as a loose confederation that responds on a trait-by-trait basis, easily allowing adaptive modification, although perhaps more slowly than if signal variation were the primary mode of evolutionary response. Studies reviewed here and questions for future research address the relative importance of integration and independence by comparing sexes, individuals, and populations. Most attention is devoted to the hormone testosterone (T) and a songbird species, the dark-eyed junco (Junco hyemalis).

Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes

“…This result strongly suggests that sensitivity to plasma steroid manipulations differs between the morphs. Other authors have suggested that steroid-sensitive behaviors are often better correlated with steroid receptors than with plasma steroid levels (10,11,(32)(33)(34). In dark-eyed juncos (Junco hyemalis), a relative of white-throated sparrows, aggressive responses to STI were positively correlated with ERα mRNA expression in the ventral telencephalon, which contains MeA, and negatively correlated with it in the hypothalamus (11).…”

Hormonally mediated maternal effects, individual strategy and global change

“…Because of the link between environmental cues and the resulting phenotype, hormones have been suggested to be critical in shaping evolution to changing environments. However, a single hormone can affect the expression of multiple traits (physiological epistasis, [44,51] or hormonal pleiotropy, [52], hence selection acting on one trait may be constrained by the underlying correlational structure with other traits. In particular, when the covariation between a trait and fitness is conditional on several traits, selection acting on a trait is correlational; the magnitude and direction of selection coefficients depend on the product of two traits.…”

“…Phenotypic integration that arises from hormonemediated expression of correlated traits has been implied to present limited opportunity for rapid evolution in response to climate-change scenarios [52]. However, phenotypic integration does not necessarily suggest phenotypic rigidity [151].…”

Animal cognition in a human-dominated world

“…Hendry et al (2008) undertook a metaanalysis of over 3000 rates of recent phenotypic change in 68 systems and found that rates of phenotypic change are greater in anthropogenic contexts than in natural contexts. Research to date has focused heavily on phenotypic plasticity in the context of reproduction, including competition and selection of mates, as well communication (for reviews, see Brown 2012;Ketterson et al 2009;Lowry et al 2013;Sol et al 2013;Wong and Candolin 2015).…”