Commentary: Hierarchical reductionism approach to understanding adaptive variation in animal performance

Abstract

Aerobic capacity is a complex performance trait with important consequences for fitness, and is determined by the integrated function of the O2 transport pathway. The components of the O2 pathway interact and function as an integrated physiological system, which could strongly influence the contribution of each component to variation in aerobic capacity. In this commentary, we highlight the value of hierarchical reductionism - combining studies of how component parts work in isolation with studies of how components interact within integrated systems - for understanding the evolution of aerobic capacity. This is achieved by focussing on the role of haemoglobin in adaptive increases in aerobic capacity in high-altitude deer mice (Peromyscus maniculatus). High-altitude deer mice have evolved increased aerobic capacity in hypoxia, in association with evolved changes in several subordinate traits across the O2 pathway. This includes an evolved increase in Hb-O2 affinity - which helps safeguard arterial O2 saturation in hypoxia - and reductionist approaches have been successful at identifying the genetic, structural, and biochemical underpinnings of variation in this trait. However, theoretical modelling and empirical measurements suggest that increased Hb-O2 affinity may not augment aerobic capacity on its own. The adaptive benefit of increased Hb-O2 affinity in high-altitude deer mice appears to have been contingent upon antecedent changes in other traits in the O2 pathway, particularly an increased capacity for O2 diffusion and utilization in active tissues. These findings highlight the importance of understanding the interactions between the components of integrated systems for fully appreciating the evolution of complex performance phenotypes.