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Metabolic plasticity confers increased resilience to climate variability in temperate compared to tropical lizards

ABSTRACT:

Patterns in functional diversity of organisms at large spatial scales can provide insight into possible responses to future climate change, but it remains a challenge to link large-scale patterns at the organismal level to their underlying physiological mechanisms. The climate variability hypothesis predicts that temperate ectotherms will be less vulnerable to climate warming than tropical ectotherms, due to their superior acclimatization capacity. However, metabolic acclimatization occurs over multiple levels of the biological hierarchy, from the enzyme and cellular level, through organ systems, to whole-organism metabolic rate. Previous studies have focused on one or a few biological hierarchy levels, leaving us without a general understanding of how metabolic acclimatization might differ between tropical and temperate species. Here, we investigate thermal acclimatization of 3 species of Takydromus lizards distributed along a broad latitudinal gradient in China, by studying metabolic modifications at the level of the whole organism, organ, mitochondria, metabolome and proteome. As predicted by the climate variability hypothesis, the 2 temperate species T. septentrionalis and T. wolteri had an enhanced acclimation response at the whole organism level compared to the tropical species T. sexlineatus, as measured by respiratory gas exchange rates. However, the mechanisms by which whole organism performance was modified was strikingly different in the 2 temperate species: widespread T. septentrionalis modified organ sizes, while the narrowly distributed T. wolteri relied on mitochondrial, proteomic and metabolomic regulation. We suggest that these 2 mechanisms of thermal acclimatization may represent general strategies used by ectotherms, with distinct ecological costs and benefits. Lacking either of these mechanisms of thermal acclimatization capacity, the tropical species is likely to have increased vulnerability to climate change.

INSTRUMENT(S): Gas Chromatography MS -

SUBMITTER: Hongxin xieylw@foxmail.com

PROVIDER: MTBLS3627 | MetaboLights | 2022-01-20

REPOSITORIES: MetaboLights

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Project description:We used custom Nimblegen microarrays representing whole-larval transcriptomes for two species (Erynnis propertius [this submission] and Papilio zelicaon [submitted seperately]) to assess gene expression differences affecting tolerance to climatic regimes. Many individuals were sourced from populations from the northern periphery and center of the species' (shared) range; these were each divided into groups treated under peripheral and central climate regimes, resulting in 4 experimental groups for each species (Peripheral Source, Peripheral treatment; Peripheral Source, Central Treatment; Central Source, Peripheral Treatment; Central Source, Central Treatment). Using technical microarray replicates allowed us to use ANOVA to identify genes whose expression may underlie local adaptation to climate (i.e., those showing an interaction term between source and population). Abstract: Population differences may determine geographic range shifts and adaptive evolution under climate change. Local adaptation in peripheral populations could preclude or slow range expansions, and populations with different genetic make-up could have distinct trajectories that produce complex spatial patterns of population change. To investigate the genetic extent of local responses to climate change, we exposed poleward-periphery and central populations of two Lepidoptera to reciprocal, common-garden climatic conditions and compared whole-transcriptome expression. We found significant expression differences between populations in both species. In addition, several hundred genes including genes involved in energy metabolism and oxidative stress responded in a localized fashion in the species that exhibits greater population structure and local adaptation. Expression levels of these genes are most divergent in the same environment in which we previously detected phenotypic divergence in metabolism. By contrast, we found no localized genes in the species with higher gene flow, reflecting the lack of previously observed local adaptation. These results suggest that population differences do not generalize easily, even for related species living in the same climate, but some taxa deserve population-level consideration when predicting the effects of climate change.

Project description:We used custom Nimblegen microarrays representing whole-larval transcriptomes for two species (Papilio zelicaon [this submission] and Erynnis propertius [submitted seperately]) to assess gene expression differences affecting tolerance to climatic regimes. Many individuals were sourced from populations from the northern periphery and center of the species' (shared) range; these were each divided into groups treated under peripheral and central climate regimes, resulting in 4 experimental groups for each species (Peripheral Source, Peripheral treatment; Peripheral Source, Central Treatment; Central Source, Peripheral Treatment; Central Source, Central Treatment). Using technical microarray replicates allowed us to use ANOVA to identify genes whose expression may underlie local adaptation to climate (i.e., those showing an interaction term between source and population). Abstract: Population differences may determine geographic range shifts and adaptive evolution under climate change. Local adaptation in peripheral populations could preclude or slow range expansions, and populations with different genetic make-up could have distinct trajectories that produce complex spatial patterns of population change. To investigate the genetic extent of local responses to climate change, we exposed poleward-periphery and central populations of two Lepidoptera to reciprocal, common-garden climatic conditions and compared whole-transcriptome expression. We found significant expression differences between populations in both species. In addition, several hundred genes including genes involved in energy metabolism and oxidative stress responded in a localized fashion in the species that exhibits greater population structure and local adaptation. Expression levels of these genes are most divergent in the same environment in which we previously detected phenotypic divergence in metabolism. By contrast, we found no localized genes in the species with higher gene flow, reflecting the lack of previously observed local adaptation. These results suggest that population differences do not generalize easily, even for related species living in the same climate, but some taxa deserve population-level consideration when predicting the effects of climate change.

			Action	DRS
	MTBLS3627	Other
	FILES	Other
	a_MTBLS3627_GC-MS___metabolite_profiling.txt	Txt
	files-all.json	Other
	i_Investigation.txt	Txt

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Metabolic plasticity confers increased resilience to climate variability in temperate compared to tropical lizards

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