Towards Integrating Evolution, Metabolism, and Climate Change Studies of Marine Ecosystems
Authors: Federico Baltar, Barbara Bayer, Nina Bednarsek, Stacy Deppeler, Ruben Escribano, Carolina E. Gonzalez, Roberta L. Hansman, Rajani Kanta Mishra, Mary Ann Moran, Daniel J. Repeta, Carol Robinson, Eva Sintes, Christian Tamburini, Luis E. Valentin, Gerhard J. Herndl
Journal: Trends in Ecology & Evolution (2019)

Marine ecosystems are changing and the services they provide are threatened by global environmental changes.Environmental changes can provoke evolution of species, affecting both the realized and fundamental niches of species.Environmental change can drive evolution, but evolution can also affect environmental conditions.There is a need for a unifying framework that combines studies of evolution, metabolism, and climate change.That framework should be based on ecological theory, on the study of the realized and fundamental niche dynamics, their spatial and temporal dynamics, and their potential response to environmental changes. Global environmental changes are challenging the structure and functioning of ecosystems. However, a mechanistic understanding of how global environmental changes will affect ecosystems is still lacking. The complex and interacting biological and physical processes spanning vast temporal and spatial scales that constitute an ecosystem make this a formidable problem. A unifying framework based on ecological theory, that considers fundamental and realized niches, combined with metabolic, evolutionary, and climate change studies, is needed to provide the mechanistic understanding required to evaluate and forecast the future of marine communities, ecosystems, and their services. Global environmental changes are challenging the structure and functioning of ecosystems. However, a mechanistic understanding of how global environmental changes will affect ecosystems is still lacking. The complex and interacting biological and physical processes spanning vast temporal and spatial scales that constitute an ecosystem make this a formidable problem. A unifying framework based on ecological theory, that considers fundamental and realized niches, combined with metabolic, evolutionary, and climate change studies, is needed to provide the mechanistic understanding required to evaluate and forecast the future of marine communities, ecosystems, and their services. The ocean absorbs most (∼93%) of the heat generated by greenhouse gas emissions, resulting in a predicted increase in the sea surface temperature of 1–10°C over the next 100 years [1IPCC Climate Change 2013: The Physical Science Basis: Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, 2013Google Scholar]. The ocean also absorbs CO2 released to the atmosphere from anthropogenic sources (currently ∼1/3 of this CO2), resulting in a profound change in the carbonate chemistry and predicted increased acidity of seawater [1IPCC Climate Change 2013: The Physical Science Basis: Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, 2013Google Scholar] to 100–150% above pre-industrial era values [1IPCC Climate Change 2013: The Physical Science Basis: Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, 2013Google Scholar]. 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We advocate the need to combine the study of evolution, together with metabolism and climate change, since a more realistic representation of the future of marine ecosystems and biogeochemical cycles can only be obtained at the intersection of these three fields. To study these interactions, a framework based on theoretical ecology that considers fundamental and realized niches, including their spatial dynamics and potential alterations in response to environmental changes, appears to be a promising approach. In the following sections we will first consider the intersection between evolution and climate change, then how microbial metabolism might interact with climate change, before commenting on the interaction of all three processes. The ecological niche concept considers how abiotic and biotic factors constrain the distribution of species and, consequently, is more informative than just focusing on geographic distribution patterns of populations [24Scheele B.C. et al.Niche contractions in declining species: mechanisms and consequences.Trends Ecol. Evol. 2017; 32: 346-355Abstract Full Text Full Text PDF PubMed Scopus (81) Google Scholar]. The fundamental niche is the multidimensional environmental space under which a species can potentially persist in the absence of biotic interactions and dispersal barriers [25Hutchinson G. Concluding Remarks: Population Studies, Animal Ecology and Demography. Cold Spring Harbor Symposium of Quantitative Biology, 1957: 415-427Google Scholar]. 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The rate of adaptation is determined by the genetic variation, individual fecundity, effective population size, environmental stochasticity, and strength of selection. If that threshold is surpassed, the rate of adaptation cannot compensate for the rate of environmental change, causing a decrease in fitness, adaptational lag, and, potentially, extirpation [32Lynch M. Lande R. Evolution and extinction in response to environmental change.in: Kareiva P.K. Biotic Interactions and Global Change. Sinauer Associates, 1993: 234-250Google Scholar]. In the Bürger and Lynch model, a stronger fitness loss (or greater extinction risk) in response to a changing trait has been related to small effective population sizes [33Bürger R. Lynch M. Evolution and extinction in a changing environment: a quantitative-genetic analysis.Evolution. 1995; 49: 151-163Crossref PubMed Google Scholar]. 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MTE provides a mechanistic, quantitative, synthetic framework to determine the effect of individual organisms on the pools and flow of energy and matter in populations, communities, and ecosystems [48Brown J.H. et al.Toward a metabolic theory of ecology.Ecology. 2004; 85: 1771-1789Crossref Scopus (4900) Google Scholar]. The MTE predicts that photosynthesis and respiration, two of the most important metabolic processes, respond very differently to temperature [48Brown J.H. et al.Toward a metabolic theory of ecology.Ecology. 2004; 85: 1771-1789Crossref Scopus (4900) Google Scholar, 49Allen A. et al.Linking the global carbon cycle to individual metabolism.Funct. Ecol. 2005; 19: 202-213Crossref Scopus (370) Google Scholar, 50Chen B. et al.Does warming enhance the effect of microzooplankton grazing on marine phytoplankton in the ocean?.Limnol. 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This MTE prediction on the differential response of respiration and photosynthesis to temperature is conserved among heterotrophic and autotrophic taxa and scales to community levels [48Brown J.H. et al.Toward a metabolic theory of ecology.Ecology. 2004; 85: 1771-1789Crossref Scopus (4900) Google Scholar, 49Allen A. et al.Linking the global carbon cycle to individual metabolism.Funct. Ecol. 2005; 19: 202-213Crossref Scopus (370) Google Scholar, 51López-Urrutia Á. et al.Scaling the metabolic balance of the oceans.Proc. Natl. Acad. Sci. U. S. A. 2006; 103: 8739-8744Crossref PubMed Scopus (405) Google Scholar]. Based on that, the MTE predicts that ocean warming will impact the efficiency of the ocean to act as a carbon sink by changing the balance between autotrophic and heterotrophic metabolism, which might have a critical feedback on marine community and ecosystem structure and global climate [52Boscolo-Galazzo F. et al.Temperature dependency of metabolic rates in the upper ocean: a positive feedback to global climate change?.Glob. Planet. Chang. 2018; 170: 201-212Crossref Scopus (45) Google Scholar]. Growth in heterotrophic organisms also seems to respond differently to temperature when compared with metabolic rates in fish, which could affect both the efficiency of energy transfer as well as the shape of trophic pyramids [53Barneche D.R. Allen A.P. The energetics of fish growth and how it constrains food-web trophic structure.Ecol. Lett. 2018; 21: 836-844Crossref PubMed Scopus (39) Google Scholar]. This seems to be also manifested in how fisheries' catches respond to changes in temperature [54Carozza D.A. et al.Metabolic impacts of climate change on marine ecosystems: implications for fish communities and fisheries.Glob. Ecol. Biogeogr. 2019; 28: 158-169Crossref Scopus (39) Google Scholar]. In laboratory experiments, however, phytoplankton cultures have been shown to increase their carbon use efficiency within ≈100 generations in response to elevated temperatures [55Padfield D. et al.Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton.Ecol. Lett. 2016; 19: 133-142Crossref PubMed Scopus (175) Google Scholar], which might dampen the decrease in C sequestration predicted by the MTE in response to warming [49Allen A. et al.Linking the global carbon cycle to individual metabolism.Funct. 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These responses to temperature in carbon use efficiency and photosynthetic traits also serve as examples of how adaptation in marine microbes (in this case thermal adaptation) might impact biogeochemical cycles and ecosystem structure and function in response to climate change. Although experiments indicate the potential for evolutionary change to mitigate effects of warming on carbon-use efficiency, we still lack evidence on whether this evolutionary change also happens within a food web where multiple intra- and interspecific interactions (not yet accounted for experimentally) are in play. The application of ecological theory to the response of populations and ecosystems to environmental changes can shed light on the response of marine ecosystems to global climate change. Below, we describe some specific outcomes that can be derived from the application of theoretical ecology to marine ecosystems (Figure 1, Figure 2, Figure 3, Figure 4, Figure 5).Figure 2Example 2 of Specific Relevant Points/Outcomes That Can Be Derived from the Application of Theoretical Ecology to Marine Ecosystems: Selection Events Caused by Extreme Weather Events.Show full captionClimate-related events (e.g., ocean warming or de-oxygenation) take place over long temporal scales and in addition extreme weather-related events can occur and cause sudden drastic changes in key communities or ecosystem engineers, decreasing ecosystem maturity and causing a resetting of ecological succession that, on the way to resuming higher ecosystem maturity, might give rise to a different ecosystem structure and different temporal response to long-scale climate-related processes.View Large Image Figure ViewerDownload Hi-res image Download (PPT)Figure 3Example 3 of Specific Relevant Points/Outcomes That Can Be Derived from the Application of Theoretical Ecology to Marine Ecosystems: Peripheral Populations as Sentinels of Change of Evolutionary, Metabolic, and Ecological Changes of Niches and Ecosystems.Show full captionPeripheral populations located at the edges of niches are predicted to present higher interspecific competition and environmental stress and lower population densities and local adaptability. We made a distinction between peripheral populations of nekton (i.e., organisms that can swim) and plankton (i.e., organisms that cannot swim faster than currents), because the inability of plankton to swim suggests that frequently fronts (where the edges of different water masses meet) will delimit the location of planktonic peripheral populations, and frontal zones can result in nutritional alleviation of limiting resources, which might counteract the predicted lower fitness and adaptability of peripheral populations of plankton. In contrast, the ability of nekton to swim allows them to more easily respond to different environmental factors via migration, but, being peripheral populations, they are probably more affected (unless they are also in fronts, where higher primary production will also potentially increase their fitness) than the planktonic counterparts.View Large