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

Benavente, Javiera N.; Fryxell, David C.; Kinnison, Michael T.; Palkovacs, Eric P.; Simon, Kevin S.

doi:10.1111/1365-2435.14020

Cited by 3 publications

(1 citation statement)

References 89 publications

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“…In addition to mass dependency, the metabolic rate response of organisms to temperature might be adaptively adjusted in specific environments through phenotypic plasticity or genotype evolution ( Benavente et al, 2022 ; Kefford et al, 2022 ; Terblanche et al, 2009 ). A species' thermal tolerance and metabolism also varies with latitude and between climate zones ( Hoffmann et al, 2005 ; Nati et al, 2021 ; Terblanche and Chown, 2006 ).…”

Section: Introductionmentioning

confidence: 99%

Metabolic rate and climate change across latitudes: evidence of mass-dependent responses in aquatic amphipods

Shokri

Cozzoli

Vignes

et al. 2022

Journal of Experimental Biology

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Predictions of individual responses to climate change are often based on the assumption that temperature affects individuals’ metabolism independently of their body mass. However, empirical evidence indicates that interactive effects exist. Here, we investigated the response of individual Standard Metabolic Rate (SMR) to annual temperature range and forecasted temperature rises of 0.6-1.2°C above the current maxima, under the conservative climate change scenario IPCC-RCP2.6. As a model organism we used the amphipod Gammarus insensibilis, collected across latitudes along the western coast of the Adriatic Sea down to the southernmost limit of the species’ distributional range, with individuals varying in body mass (0.4-13.57mg). Overall, we found that the effect of temperature on SMR is mass-dependent. Within the annual temperature range, the mass-specific SMR of small/young individuals increased with temperature at a greater rate (activation energy: E=0.48 eV) than large/old ones (E=0.29 eV), with a higher metabolic level for high-latitude than low-latitude populations. However, under the forecasted climate conditions, the large individuals’ mass-specific SMR responded differently across latitudes. Unlike the higher-latitude population, whose mass-specific SMR increased in response to the forecasted climate change across all size classes, in the lower-latitude populations, this increase was not seen in large individuals. The larger/older conspecifics at lower latitudes could therefore be the first to experience the negative impacts of warming on metabolism-related processes. Although the ecological collapse of such a basic trophic level (aquatic amphipods) due to climate change would have profound consequences for population ecology, the risk is significantly mitigated by phenotypic and genotypic adaptation.

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Section: Introductionmentioning

confidence: 99%

Metabolic rate and climate change across latitudes: evidence of mass-dependent responses in aquatic amphipods

Shokri

Cozzoli

Vignes

et al. 2022

Journal of Experimental Biology

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The Effect of Pregnancy On Metabolic Scaling and Population Energy Demand in the Viviparous Fish Gambusia affinis

Moffett

Fryxell

Benavente

et al. 2022

Integrative and Comparative Biology

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Synopsis Metabolism is a fundamental attribute of all organisms that influences how species affect and are affected by their natural environment. Differences between sexes in ectothermic species may substantially alter metabolic scaling patterns, particularly in viviparous or live-bearing species where females must support their basal metabolic costs and that of their embryos. Indeed, if pregnancy is associated with marked increases in metabolic demand and alters scaling patterns between sexes, this could in turn interact with natural sex ratio variation in nature to affect population-level energy demand. Here, we aimed to understand how sex and pregnancy influence metabolic scaling and how differences between sexes affect energy demand in Gambusia affinis (Western mosquitofish). Using the same method, we measured routine metabolic rate in the field on reproductively active fish and in the laboratory on virgin fish. Our data suggest that changes in energy expenditure related to pregnancy may lead to steeper scaling coefficients in females (b = 0.750) compared to males (b = 0.595). In contrast, virgin females and males had similar scaling coefficients, suggesting negligible sex differences in metabolic costs in reproductively inactive fish. Further, our data suggest that incorporating sex differences in allometric scaling may alter population-level energy demand by as much as 20–28%, with the most pronounced changes apparent in male-biased populations due to the lower scaling coefficient of males. Overall, our data suggest that differences in energy investment in reproduction between sexes driven by pregnancy may alter allometric scaling and population-level energy demand.

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Non‐concordant epigenetic and transcriptional responses to acute thermal stress in western mosquitofish (Gambusia affinis)

Ren,

Zhao,

2024

Molecular Ecology

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Climate change is intensifying the frequency and severity of extreme temperatures. Understanding the molecular mechanisms underlying the ability to cope with acute thermal stress is key for predicting species' responses to extreme temperature events. While many studies have focused on the individual roles of gene expression, post‐transcriptional processes and epigenetic modifications in response to acute thermal stress, the relative contribution of these molecular mechanisms remains unclear. The wide range of thermal limits of western mosquitofish (Gambusia affinis) provides an opportunity to explore this interplay. Here, we quantified changes in gene expression, alternative splicing, DNA methylation and microRNA (miRNA) expression in muscle tissue dissected from mosquitofish immediately after reaching high (CTmax) or low thermal limit (CTmin). Although the numbers of genes showing expression and splicing changes in response to acute temperature stress were small, we found a possibly larger and non‐redundant role of splicing compared to gene expression, with more genes being differentially spliced (DSGs) than differentially expressed (DEGs), and little overlap between DSGs and DEGs. We also identified a small proportion of CpGs showing significant methylation change (i.e. differentially methylated cytosines, DMCs) in fish at thermal limits; however, there was no overlap between DEGs and genes annotated with DMCs in both CTmax and CTmin experiments. The weak interplay between epigenetic modifications and gene expression was further supported by our discoveries of no differentially expressed miRNAs. These findings provide novel insights into the relative role of different molecular mechanisms underlying immediate responses to extreme temperatures and demonstrate non‐concordant responses of epigenetic and transcriptional mechanisms to acute temperature stress.

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

Cited by 3 publications

References 89 publications

Metabolic rate and climate change across latitudes: evidence of mass-dependent responses in aquatic amphipods

Metabolic rate and climate change across latitudes: evidence of mass-dependent responses in aquatic amphipods

The Effect of Pregnancy On Metabolic Scaling and Population Energy Demand in the Viviparous Fish Gambusia affinis

Non‐concordant epigenetic and transcriptional responses to acute thermal stress in western mosquitofish (Gambusia affinis)

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