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 populationsexperiencing 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 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. 3 4. In sum, our study suggests that fish may diverge toward a lower standard metabolic rate in a warming world, but this might depend on connectivity and gene flow between different thermal habitats.

Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance inDrosophila subobscura

“…In the same way, studies of selection for stress resistance have found a reduction of metabolic rate in selected lines (Harshmann et al, 1999; Padfield et al, 2016). In addition, a study reported that populations of sticklebacks inhabiting geothermally warmed lakes showed a lower RMR than populations from cold lakes, but that this difference was only detected when both populations were acclimated to different temperatures (Pilakouta et al, 2020). However, our results agree a study published by Messamah et al (2017), who reported that the variation in the metabolic rate of 65 Drosophila species was not related to the annual mean temperature of their habitats of origin.…”

“…In ectotherms, metabolism increases with environmental temperatures, inducing high metabolic costs in individuals exposed to heat stress as expected by global warming (Lighton & Turner, 2004; Huey & Kingsolver, 2019). Therefore, metabolic depression could be an important strategy to prevent that metabolism exceeds the physiological limits and energy expenditure, which has adversely effects on fitness under extreme heat conditions (Marshall & McQuaid, 2011; González-Tokman et al, 2020; Pilakouta et al, 2020). This metabolic response to high temperature could partially explain the counter gradient variation proposed in metabolic cold adaptation hypothesis (Addo-Bediako, 2002; Gaston et al, 2009), which establishes that ectotherm species from temperate habitats have lower metabolic rates than those living in colder environments (Addo-Bediako et al, 2002; Sylvestre et al, 2007; Schaefer & Walters 2010; Bruning et al, 2013; Sinnatamby et al, 2015; Pilakouta et al, 2020).…”

“…Therefore, metabolic depression could be an important strategy to prevent that metabolism exceeds the physiological limits and energy expenditure, which has adversely effects on fitness under extreme heat conditions (Marshall & McQuaid, 2011; González-Tokman et al, 2020; Pilakouta et al, 2020). This metabolic response to high temperature could partially explain the counter gradient variation proposed in metabolic cold adaptation hypothesis (Addo-Bediako, 2002; Gaston et al, 2009), which establishes that ectotherm species from temperate habitats have lower metabolic rates than those living in colder environments (Addo-Bediako et al, 2002; Sylvestre et al, 2007; Schaefer & Walters 2010; Bruning et al, 2013; Sinnatamby et al, 2015; Pilakouta et al, 2020). On other hand, experimental populations exposed to warm environmental conditions during several generations showed an evolutionary increase of their thermal tolerance accompanied with a reduced metabolic rate (Padfield et al, 2016, but see Mallard et al, 2018).…”

Multigenerational exposure to increased temperature reduces metabolic rate but increases boldness in Gambusia affinis

“…Geothermally heated habitats can offer valuable natural experiments that overcome the limitations of other natural thermal gradients and experimental approaches. For example, the use of geothermal or artificially heated waterways has recently demonstrated that long‐term exposure (e.g., 1000s of years) to increased temperatures may reduce the temperature sensitivity of metabolism in freshwater fishes (Bruneaux et al, 2014; Pilakouta et al, 2020). Similar reductions in metabolic temperature sensitivity may occur over shorter time scales (e.g., 10s to 100s of years) congruent with current environmental warming caused by climate change (Moffett et al, 2018; Sandblom et al, 2016; White & Wahl, 2020).…”

Plasticity and evolution shape the scaling of metabolism and excretion along a geothermal temperature gradient

“…Populations from warmer environments commonly display metabolic rates below expectations, suggesting that evolutionary adaptation can reduce E (‘countergradient variation’, ‘metabolic cold adaptation hypothesis’; Pilakouta et al., 2020; White et al., 2012; although see Alton et al., 2017). Studies of fish species have recently demonstrated that metabolic reduction at warmer temperatures can arise over few generations (<100 years), but these studies have not assessed the relative contribution of evolutionary change versus plasticity in shaping these patterns (Moffett et al., 2018; Pilakouta et al., 2020).…”