Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America.

Maria Carolina Romero,Adalto Bianchini,Samuel Coelho Faria,Mariana Machado Lauer,Federico Tapella,Ana Lúcia Ribeiro Latorre Zimbardi,John Campbell McNamara

doi:10.3389/fphys.2020.00312

Abstract

Temperature is an important abiotic factor that drives the evolution of ectotherms owing to its pervasive effects at all levels of organization. Although a species’ thermal tolerance is environmentally driven within a spatial cline, it may be constrained over time due to differential phylogenetic inheritance. At the limits of thermal tolerance, hemolymph oxygen is reduced and lactate formation is increased due to mismatch between oxygen supply and demand; imbalance between enzyme flexibility/stability also impairs the ability to generate energy. Here, we characterized the effects of lower (LL50) and upper (UL50) critical thermal limits on selected descriptors of aerobic and anaerobic metabolism in 12 intertidal crab species distributed from northern Brazil (≈7.8°S) to southern Patagonia (≈53.2°S), considering their phylogeny. We tested for (i) functional trade-offs regarding aerobic and anaerobic metabolism and LDH kinetics in shaping thermal tolerance; (ii) influence of shared ancestry and thermal province on metabolic evolution; and (iii) presence of evolutionary convergences and adaptive peaks in the crab phylogeny. The tropical and subtropical species showed similar systemic and kinetic responses, both differing from the sub-Antarctic crabs. The lower UL50’s of the sub-Antarctic crabs may reflect mismatch between the evolution of aerobic and anaerobic metabolism since these crabs exhibit lower oxygen consumption but higher lactate formation than tropical and subtropical species also at their respective UL50’s. LDH activity increased with temperature increase, while KmPyr remained fairly constant; catalytic coefficient correlated negatively with thermal niche. Thermal tolerance may rely on a putative evolutionary trade-off between aerobic and anaerobic metabolism regarding energy supply, while temperature compensation of kinetic performance is driven by thermal habitat as revealed by the LDH affinity/efficiency equilibrium. The overall physiological evolution revealed two homoplastic adaptive peaks in the sub-Antarctic crabs with a further shift in the tropical/subtropical clade. The physiological traits at UL50 have evolved in a phylogenetic manner while all others were more plastic. Thus, shared inheritance and thermal environment have driven the crabs’ thermal tolerance and metabolic evolution, revealing physiological transformations that have arisen in both colder and warmer climes, especially at higher levels of biological organization and phylogenetic diversity.

Highlights

Biological systems are thermodynamically open, owing to the continuous flux of energy and matter with the surrounding environment (Cannon, 1929; Recordati and Bellini, 2004)
We investigate physiological and evolutionary patterns of thermal tolerance in this crab clade (Faria et al, 2017), characterizing the effects of critical thermal limits (LL50 and UL50) on selected descriptors of aerobic and anaerobic metabolism at the systemic and kinetic levels
We found that tropical and subtropical intertidal crab species showed similar subcellular and organismic responses to acute thermal stress, differing from their sub-Antarctic relatives

Summary

Introduction

Biological systems are thermodynamically open, owing to the continuous flux of energy and matter with the surrounding environment (Cannon, 1929; Recordati and Bellini, 2004). At the critical thermal limits, hemolymph oxygen levels are reduced due to the mismatch between oxygen supply and demand, imposing limitations on temperature tolerance (Pörtner, 2002) This limitation to systemic oxygen availability creates a hypoxic state, which is unable to sustain tissue demand, leading to anaerobic metabolism at the critical thermal limits as a consequence of elevated oxygen demand or insufficient aerobic capacity (Giomi and Pörtner, 2013). The recruitment of chaperone molecules and anti-oxidant defenses may extend survival, albeit with reduced performance at the molecular level, reverberating at the whole animal level and leading to death This unifying principle known as “oxygen and capacity limitation of thermal tolerance” (OCLTT) characterizes sensitivity to thermal stress in aquatic invertebrates (Pörtner and Gutt, 2016; Verberk et al, 2016). Air-breathers and amphibious species can attain higher hemolymph oxygen concentrations and increase oxygen diffusion, which may enhance their thermal tolerance by extending aerobic scope (Giomi et al, 2014)

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