Conserved and convergent mechanisms underlying performance–life-history trade-offs

Abstract

Phenotypic trade-offs are inevitable in nature, but the mechanisms driving them are poorly understood. Movement and oxygen are essential to all animals, and as such, the common ancestor to all living animals passed on mechanisms to acquire oxygen and contract muscle, sometimes at the expense of other activities or expression of traits. Nevertheless, convergent pathways have also evolved to deal with critical trade-offs that are necessary to survive ubiquitous environmental challenges. We discuss how whole-animal performance traits, such as locomotion, are important to fitness, yet costly, resulting in trade-offs with other aspects of the phenotype via specific conserved and convergent mechanistic pathways across all animals. Specifically, we discuss conserved pathways involved in muscle structure and signaling, insulin/insulin-like signaling, sirtuins, mitochondria and hypoxia-inducible factors, as well as convergent pathways involved in energy regulation, development, reproductive investment and energy storage. The details of these mechanisms are only known from a few model systems, and more comparative studies are needed. We make two main recommendations as a framework for future studies of animal form and function. First, studies of performance should consider the broader life-history context of the organism, and vice versa, as performance expression can require a large portion of acquired resources. Second, studies of life histories or mechanistic pathways that measure performance should do so in meaningful and standardized ways. Understanding proximate mechanisms of phenotypic trade-offs will not only better explain the phenotypes of the organisms we study, but also allow predictions about phenotypic variation at the evolutionary scale.

Sex‐specific effects of immune challenges on green anole lizard metabolism

“…Such tradeoffs can be due to genetic covariances (“evolutionary costs” of Schmid‐Hempel, 2003) or energetic reallocation of acquired resources due to maintenance of immune function and activation of immune responses (“use costs” of Schmid‐Hempel, 2003). These latter tradeoffs manifest during environmental challenges when there is resource limitation and prioritization of other fitness‐enhancing traits, and due to shared mechanistic pathways of the traits involved in the tradeoffs (Husak & Lailvaux, 2022) such as seen with “pleiotropic” effects of altered hormone concentrations (Ketterson et al, 2009; Mauro & Ghalambor, 2020). The fact that enhanced immune function shifts limited resources away from other aspects of the phenotype suggests that the immune system is metabolically costly (Martin et al, 2008).…”

A fast fish swimming protocol that provides similar insights as critical sustained swimming speed

“…The capacity to move fast enough to catch prey or long enough to disperse to new habitats will determine the success of animals in their natural environment (Denton et al, 2017; Domenici et al, 2019; Wu and Seebacher, 2022). Locomotor performance is therefore closely related to fitness, but it may also be costly so that there are trade-offs that determine individual fitness (Husak and Lailvaux, 2022). Environmental conditions can impact these responses and measures of locomotor performance are important to assess the impacts of environmental change on animals (Domenici et al, 2019; Killen et al, 2017; Killen et al, 2021).…”

Combined effects of ambient temperature and food availability on induced innate immune response of a fruit-eating bat (Carollia perspicillata)

“…Sensitivity to these changes can be analyzed by measuring the performance capacity of a given species, that is, its capacity to execute activities that are relevant to its fitness when exposed to these changes. These activities can be associated to aspects related to movement (dynamic performance) or to the ability to regulate physiological processes that mediate the overall responses to these changes, such as thermal performance, regulation of reproduction, growth and the immune system (regulatory performance) [5,6].…”