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

Abstract

1. 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.2. 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.3. 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. 4. 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. K E Y W O R D S climate change, countergradient variation, Gasterosteus aculeatus, Krogh's rule, metabolic cold adaptation, physiology, threespine stickleback 1206 | Functional Ecology PILAKOUTA eT AL.

Metabolic adaptation to warm water in fish

“…Confounds may still include for example indirect ecosystem effects of temperature that could mimic direct thermal effects, which could be difficult to detect and account for. As the metabolic rates changed in the predicted direction, that explanation appears unlikely in this case (Pilakouta et al, 2020).…”

“…Thermal adaptation over the time‐scale of decades to millennia is still underexplored, with very few model systems available. The experiment by Pilakouta et al (2020) on sticklebacks from cold and warm lakes (red and dark blue circles) in the time‐scale of millennia (D) reveal metabolic adaptation. Local adaptation in metabolic rates in populations diverged in even deeper time (E) has been demonstrated, for example, Sylvestre et al (2007).…”

“…In this current issue of Functional Ecology , Pilakouta et al (2020) describe populations of three‐spined sticklebacks Gasterosteus aculeatus adapted to geothermally heated lakes on Iceland. These sticklebacks provide exciting opportunities for exploring many questions regarding thermal adaptation in fish (Figure 1D).…”

“…Pilakouta et al (2020) compared these unique stickleback populations adapted to geothermally heated lakes with nearby populations adapted to cold habitats. Both warm‐ and cold‐adapted fish were acclimated to three temperatures (10, 15, 20°C) before measurements of standard‐ and maximum metabolic rates.…”

“…The rate and magnitude of such adaptation, however, will likely differ between species and contexts. One important implication of the findings in Pilakouta et al (2020) is that modelling of fish performance in warming scenarios using standard metabolic rates need to account for this adaptation when for example estimating energy expenditure.…”