Evolutionary endocrinology and the problem of Darwin's tangled bank

Abstract

Like Darwin's tangled bank of biodiversity, the endocrine mechanisms that give rise to phenotypic diversity also exhibit nearly endless forms. This tangled bank of mechanistic diversity can prove problematic as we seek general principles on the role of endocrine mechanisms in phenotypic evolution. A key unresolved question is therefore: to what degree are specific endocrine mechanisms re-used to bring about replicated phenotypic evolution? Related areas of inquiry are booming in molecular ecology, but behavioral traits are underrepresented in this literature. Here, I leverage the rich comparative tradition in evolutionary endocrinology to evaluate whether and how certain mechanisms may be repeated hotspots of behavioral evolutionary change. At one extreme, mechanisms may be parallel, such that evolution repeatedly uses the same gene or pathway to arrive at multiple independent (or, convergent) origins of a particular behavioral trait. At the other extreme, the building blocks of behavior may be unique, such that outwardly similar phenotypes are generated via lineage-specific mechanisms. This review synthesizes existing case studies, phylogenetic analyses, and experimental evolutionary research on mechanistic parallelism in animal behavior. These examples show that the endocrine building blocks of behavior have some elements of parallelism across replicated evolutionary events. However, support for parallelism is variable among studies, at least some of which relates to the level of complexity at which we consider sameness (i.e. pathway vs. gene level). Moving forward, we need continued experimentation and better testing of neutral models to understand whether, how – and critically, why – mechanism A is used in one lineage and mechanism B is used in another. We also need continued growth of large-scale comparative analyses, especially those that can evaluate which endocrine parameters are more or less likely to undergo parallel evolution alongside specific behavioral traits. These efforts will ultimately deepen understanding of how and why hormone-mediated behaviors are constructed the way that they are.