Integrated metabolic strategy: A framework for predicting the evolution of carbon‐water tradeoffs within plant clades

Abstract

The fundamental tradeoff between carbon gain and water loss has long been predicted as an evolutionary driver of plant strategies across environments. Nonetheless, challenges in measuring carbon gain and water loss in ways that integrate over leaf lifetime have limited our understanding of the variation in and mechanistic bases of this tradeoff. Furthermore, the microevolution of plant traits within species versus the macroevolution of strategies among closely related species may not be the same, and accordingly, the latter must be addressed using comparative phylogenetic analyses. Here we introduce the concept of ‘integrated metabolic strategy’ (IMS) to describe the ratio between carbon isotope composition (δ¹³C) and oxygen isotope composition above source water (Δ¹⁸O) of leaf cellulose. IMS is a measure of leaf‐level conditions that integrate several mechanisms contributing to carbon gain (δ¹³C) and water loss (Δ¹⁸O) over leaf lifespan, with larger values reflecting higher metabolic efficiency and hence less of a tradeoff. We tested how IMS evolves among closely related yet ecologically diverse milkweed species, and subsequently addressed phenotypic plasticity in response to water availability in species with divergent IMS. Integrated metabolic strategy varied strongly among 20 Asclepias species when grown under controlled conditions, and phylogenetic analyses demonstrate species‐specific tradeoffs between carbon gain and water loss. Larger IMS values were associated with species from dry habitats, with larger carboxylation capacity, smaller stomatal conductance and smaller leaves; smaller IMS was associated with wet habitats, smaller carboxylation capacity, larger stomatal conductance and larger leaves. The evolution of IMS was dominated by changes in species’ demand for carbon (δ¹³C) more so than water conservation (Δ¹⁸O). Although some individual physiological traits showed phylogenetic signal, IMS did not. In response to experimental decreases in soil moisture, three species maintained similar IMS across levels of water availability because of proportional increases in δ¹³C and Δ¹⁸O (or little change in either), while one species increased IMS due to disproportional changes in δ¹³C relative to Δ¹⁸O. Synthesis. IMS is a broadly applicable mechanistic tool; IMS variation among and within species may shed light on unresolved questions relating to the evolution and ecology of plant ecophysiological strategies.

Plant phenotyping relevance

葉の同位体組成を統合して炭素獲得・水損失という植物生理状態を定量するIMS指標を新たに導入し、複数種で適用・評価しているため、単なる生物学的測定ではなく方法開発を含む実質的な植物フェノタイピング研究である。

Code and data availability

The article states its phenotype/trait data are deposited on Dryad (doi 10.5061/dryad.203pf67), but that URL is not among the allowed_urls, so no actionable paper-specific asset can be cited. No author analysis code or public repository URL within the allowed set is mentioned.

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