Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures

Abstract Background Climate change is expected to lead to warming in ocean surface temperatures which will have unequal effects on the rates of photosynthesis and heterotrophy. As a result of this changing metabolic landscape, directional phenotypic evolution will occur, with implications that casca...

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Main Authors: Logan M. Gonzalez, Stephen R. Proulx, Holly V. Moeller
Format: Article
Language:English
Published: BMC 2022-11-01
Series:BMC Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1186/s12862-022-02092-9
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author Logan M. Gonzalez
Stephen R. Proulx
Holly V. Moeller
author_facet Logan M. Gonzalez
Stephen R. Proulx
Holly V. Moeller
author_sort Logan M. Gonzalez
collection DOAJ
description Abstract Background Climate change is expected to lead to warming in ocean surface temperatures which will have unequal effects on the rates of photosynthesis and heterotrophy. As a result of this changing metabolic landscape, directional phenotypic evolution will occur, with implications that cascade up to the ecosystem level. While mixotrophic phytoplankton, organisms that combine photosynthesis and heterotrophy to meet their energetic and nutritional needs, are expected to become more heterotrophic with warmer temperatures due to heterotrophy increasing at a faster rate than photosynthesis, it is unclear how evolution will influence how these organisms respond to warmer temperatures. In this study, we used adaptive dynamics to model the consequences of temperature-mediated increases in metabolic rates for the evolution of mixotrophic phytoplankton, focusing specifically on phagotrophic mixotrophs. Results We find that mixotrophs tend to evolve to become more reliant on phagotrophy as temperatures rise, leading to reduced prey abundance through higher grazing rates. However, if prey abundance becomes too low, evolution favors greater reliance on photosynthesis. These responses depend upon the trade-off that mixotrophs experience between investing in photosynthesis and phagotrophy. Mixotrophs with a convex trade-off maintain mixotrophy over the greatest range of temperatures; evolution in these “generalist” mixotrophs was found to exacerbate carbon cycle impacts, with evolving mixotrophs exhibiting increased sensitivity to rising temperature. Conclusions Our results show that mixotrophs may respond more strongly to climate change than predicted by phenotypic plasticity alone due to evolutionary shifts in metabolic investment. However, the type of metabolic trade-off experienced by mixotrophs as well as ecological feedback on prey abundance may ultimately limit the extent of evolutionary change along the heterotrophy-phototrophy spectrum.
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spelling doaj.art-cb97db6d23404306afd5e695871201a22022-12-22T03:43:02ZengBMCBMC Ecology and Evolution2730-71822022-11-0122111310.1186/s12862-022-02092-9Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperaturesLogan M. Gonzalez0Stephen R. Proulx1Holly V. Moeller2Biogeochemical Sciences Branch, Cold Regions Research and Engineering Laboratory, US Army Corps of EngineersDepartment of Ecology, Evolution, and Marine Biology, University of California-Santa BarbaraDepartment of Ecology, Evolution, and Marine Biology, University of California-Santa BarbaraAbstract Background Climate change is expected to lead to warming in ocean surface temperatures which will have unequal effects on the rates of photosynthesis and heterotrophy. As a result of this changing metabolic landscape, directional phenotypic evolution will occur, with implications that cascade up to the ecosystem level. While mixotrophic phytoplankton, organisms that combine photosynthesis and heterotrophy to meet their energetic and nutritional needs, are expected to become more heterotrophic with warmer temperatures due to heterotrophy increasing at a faster rate than photosynthesis, it is unclear how evolution will influence how these organisms respond to warmer temperatures. In this study, we used adaptive dynamics to model the consequences of temperature-mediated increases in metabolic rates for the evolution of mixotrophic phytoplankton, focusing specifically on phagotrophic mixotrophs. Results We find that mixotrophs tend to evolve to become more reliant on phagotrophy as temperatures rise, leading to reduced prey abundance through higher grazing rates. However, if prey abundance becomes too low, evolution favors greater reliance on photosynthesis. These responses depend upon the trade-off that mixotrophs experience between investing in photosynthesis and phagotrophy. Mixotrophs with a convex trade-off maintain mixotrophy over the greatest range of temperatures; evolution in these “generalist” mixotrophs was found to exacerbate carbon cycle impacts, with evolving mixotrophs exhibiting increased sensitivity to rising temperature. Conclusions Our results show that mixotrophs may respond more strongly to climate change than predicted by phenotypic plasticity alone due to evolutionary shifts in metabolic investment. However, the type of metabolic trade-off experienced by mixotrophs as well as ecological feedback on prey abundance may ultimately limit the extent of evolutionary change along the heterotrophy-phototrophy spectrum.https://doi.org/10.1186/s12862-022-02092-9MixoplanktonAdaptive dynamicsMetabolic scalingCarbon cycleEco-evolutionary feedback
spellingShingle Logan M. Gonzalez
Stephen R. Proulx
Holly V. Moeller
Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
BMC Ecology and Evolution
Mixoplankton
Adaptive dynamics
Metabolic scaling
Carbon cycle
Eco-evolutionary feedback
title Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title_full Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title_fullStr Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title_full_unstemmed Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title_short Modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
title_sort modeling the metabolic evolution of mixotrophic phytoplankton in response to rising ocean surface temperatures
topic Mixoplankton
Adaptive dynamics
Metabolic scaling
Carbon cycle
Eco-evolutionary feedback
url https://doi.org/10.1186/s12862-022-02092-9
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