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

FARIA, SAMUEL COELHO; BIANCHINI, ADALTO; LAUER, MARIANA MACHADO; ZIMBARDI, ANA LÚCIA RIBEIRO LATORRE; TAPELLA, FEDERICO; ROMERO, MARIA CAROLINA; MCNAMARA, JOHN CAMPBELL

Frontiers in Physiology

University of Aberdeen, United Kingdom

Año: 2020 vol. 11

Temperature is an important abiotic factor that drives the evolution of ectothermsowing to its pervasive effects at all levels of organization. Although a species? thermaltolerance is environmentally driven within a spatial cline, it may be constrained overtime due to differential phylogenetic inheritance. At the limits of thermal tolerance,hemolymph oxygen is reduced and lactate formation is increased due to mismatchbetween oxygen supply and demand; imbalance between enzyme flexibility/stabilityalso 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 andanaerobic metabolism in 12 intertidal crab species distributed from northern Brazil(7.8S) to southern Patagonia (53.2S), considering their phylogeny. We testedfor (i) functional trade-offs regarding aerobic and anaerobic metabolism and LDHkinetics in shaping thermal tolerance; (ii) influence of shared ancestry and thermalprovince on metabolic evolution; and (iii) presence of evolutionary convergences andadaptive peaks in the crab phylogeny. The tropical and subtropical species showedsimilar systemic and kinetic responses, both differing from the sub-Antarctic crabs.The lower UL50?s of the sub-Antarctic crabs may reflect mismatch between theevolution of aerobic and anaerobic metabolism since these crabs exhibit lower oxygenconsumption but higher lactate formation than tropical and subtropical species also attheir respective UL50?s. LDH activity increased with temperature increase, while KmPyrremained fairly constant; catalytic coefficient correlated negatively with thermal niche.Thermal tolerance may rely on a putative evolutionary trade-off between aerobic andanaerobic metabolism regarding energy supply, while temperature compensation ofkinetic performance is driven by thermal habitat as revealed by the LDH affinity/efficiencyequilibrium. The overall physiological evolution revealed two homoplastic adaptive peaks in the sub-Antarctic crabs with a further shift in the tropical/subtropical clade. Thephysiological traits at UL50 have evolved in a phylogenetic manner while all others weremore plastic. Thus, shared inheritance and thermal environment have driven the crabs?thermal tolerance and metabolic evolution, revealing physiological transformations thathave arisen in both colder and warmer climes, especially at higher levels of biologicalorganization and phylogenetic diversity.