Selection on the morphology–physiology-performance nexus: Lessons from freshwater stickleback morphs

Abstract

Conspecifics inhabiting divergent environments frequently differ in morphology, physiology, and performance, but the interrelationships amongst traits and with Darwinian fitness remains poorly understood. We investigated population differentiation in morphology, metabolic rate, and swimming performance in three-spined sticklebacks (Gasterosteus aculeatus L.), contrasting a marine/ancestral population with two distinct freshwater morphotypes derived from it: the “typical” low-plated morph, and a unique “small-plated” morph. We test the hypothesis that similar to plate loss in other freshwater populations, reduction in lateral plate size also evolved in response to selection. Additionally, we test how morphology, physiology, and performance have evolved in concert as a response to differences in selection between marine and freshwater environments. We raised pure-bred second-generation fish originating from three populations and quantified their lateral plate coverage, burst- and critical swimming speeds, as well as standard and active metabolic rates. Using a multivariate QST-FST framework, we detected signals of directional selection on metabolic physiology and lateral plate coverage, notably demonstrating that selection is responsible for the reduction in lateral plate coverage in a small-plated stickleback population. We also uncovered signals of multivariate selection amongst all bivariate trait combinations except the two metrics of swimming performance. Divergence between the freshwater and marine populations exceeded neutral expectation in morphology and in most physiological and performance traits, indicating that adaptation to freshwater habitats has occurred, but through different combinations of traits in different populations. These results highlight both the complex interplay between morphology, physiology and performance in local adaptation, and a framework for their investigation.