Trade-offs, pleiotropy, and shared molecular pathways: A unified view of constraints on adaptation

Abstract

The concept of trade-offs permeates our thinking about adaptive evolution because they are exhibited at every level of biological organization, from molecular and cellular processes to organismal and ecological functions. Trade-offs inevitably arise because different traits do not occur in isolation, but instead are imbedded within complex, integrated systems that make up whole organisms. The genetic and mechanistic underpinning of trade-offs can be found in the pleiotropic nodes that occur in the biological pathways shared between traits. Yet, often trade-offs are only understood as statistical correlations, limiting the ability to evaluate the interplay between how selection and constraint interact during adaptive evolution. Here, we first review the classic paradigms in which physiologists and evolutionary biologists have studied trade-offs and highlight the ways in which network and molecular pathway approaches unify these paradigms. We discuss how these approaches allow researchers to evaluate why trade-offs arise and how selection can act to overcome trait correlations and evolutionary constraints. We argue that understanding how the conserved molecular pathways are shared between different traits and functions provides a conceptual framework for evolutionary biologists, physiologists, and molecular biologists to meaningfully work together toward the goal of understanding why correlations and trade-offs occur between traits. We briefly highlight the melanocortin system and the hormonal control of osmoregulation as two case studies where an understanding of shared molecular pathways reveals why trade-offs occur between seemingly unrelated traits. While we recognize that applying such approaches poses challenges and limitations particularly in the context of natural populations, we advocate for the view that focusing on the biological pathways responsible for trade-offs provides a unified conceptual context accessible to a broad range of integrative biologists.