Multigenerational exposure to elevated temperatures leads to a reduction in standard metabolic rate in the wild.

Natalie Pilakouta,Shaun S Killen,Neil B Metcalfe,Kevin J Parsons,Skúli Skúlason,Bjarni K Kristjánsson,Jan Lindström,Craig White

doi:10.1111/1365-2435.13538

Abstract

In light of global climate change, there is a pressing need to understand and predict the capacity of populations to respond to rising temperatures. Metabolic rate is a key trait that is likely to influence the ability to cope with climate change. Yet, empirical and theoretical work on metabolic rate responses to temperature changes has so far produced mixed results and conflicting predictions.Our study addresses this issue using a novel approach of comparing fish populations in geothermally warmed lakes and adjacent ambient‐temperature lakes in Iceland. This unique ‘natural experiment’ provides repeated and independent examples of populations experiencing contrasting thermal environments for many generations over a small geographic scale, thereby avoiding the confounding factors associated with latitudinal or elevational comparisons. Using Icelandic sticklebacks from three warm and three cold habitats, we measured individual metabolic rates across a range of acclimation temperatures to obtain reaction norms for each population.We found a general pattern for a lower standard metabolic rate (SMR) in sticklebacks from warm habitats when measured at a common temperature, as predicted by Krogh's rule. Metabolic rate differences between warm‐ and cold‐habitat sticklebacks were more pronounced at more extreme acclimation temperatures, suggesting the release of cryptic genetic variation upon exposure to novel conditions, which can reveal hidden evolutionary potential. We also found a stronger divergence in metabolic rate between thermal habitats in allopatry than sympatry, indicating that gene flow may constrain physiological adaptation when dispersal between warm and cold habitats is possible.In sum, our study suggests that fish may diverge toward a lower SMR in a warming world, but this might depend on connectivity and gene flow between different thermal habitats. A free Plain Language Summary can be found within the Supporting Information of this article.

Highlights

Climate change poses a substantial threat to biodiversity, as rising temperatures are altering biotic and abiotic environmental conditions and imposing novel selection pressures on organisms (Crozier & Hutchings, 2014)
We found a general pattern for a lower standard metabolic rate (SMR) in sticklebacks from warm habitats when measured at a common temperature, as predicted by Krogh's rule
We found a general pattern for a lower Standard metabolic rate (SMR) in sticklebacks originating from warm habitats, the extent of this effect varied depending on the population pair and acclimation temperature

Summary

| INTRODUCTION

Climate change poses a substantial threat to biodiversity, as rising temperatures are altering biotic and abiotic environmental conditions and imposing novel selection pressures on organisms (Crozier & Hutchings, 2014). High-latitude Drosophila melanogaster populations tend to have elevated metabolic rates compared to low-latitude populations as predicted by Krogh's rule (Berrigan & Partridge, 1997), but latitudinal comparisons of snail populations and altitudinal comparisons of isopod populations offer no support for this rule (Gaitán-Espitia & Nespolo, 2014; Lardies, Catalán, & Bozinovic, 2004) Another approach that has been used to study metabolic rate adaptation is experimental evolution. Global-scale analyses of 346 insect species (Addo-Bediako et al, 2002) and 37 fish species (White, Frappell, & Chown, 2011) showed support for Krogh's rule, but an analysis of 65 Drosophilidae species did not (Messamah, Kellermann, Malte, Loeschcke, & Overgaard, 2017) We address this question using a novel approach of comparing populations of threespine sticklebacks Gasterosteus aculeatus found in geothermally warmed lakes and adjacent ambienttemperature lakes in Iceland. Given the potential importance of physiological adaptation for population persistence (Donelson et al, 2011; Sinclair et al, 2016), our study could provide valuable insights into the capacity of ectotherms to cope with global climate change

| MATERIALS AND METHODS

Findings

| DISCUSSION