Evolutionary context for understanding and manipulating plant responses to past, present and future atmospheric [CO ₂ ]

Abstract

Variation in atmospheric [CO 2 ] is a prominent feature of the environmental history over which vascular plants have evolved. Periods of falling and low [CO 2 ] in the palaeo-record appear to have created selective pressure for important adaptations in modern plants. Today, rising [CO 2 ] is a key component of anthropogenic global environmental change that will impact plants and the ecosystem goods and services they deliver. Currently, there is limited evidence that natural plant populations have evolved in response to contemporary increases in [CO 2 ] in ways that increase plant productivity or fitness, and no evidence for incidental breeding of crop varieties to achieve greater yield enhancement from rising [CO 2 ]. Evolutionary responses to elevated [CO 2 ] have been studied by applying selection in controlled environments, quantitative genetics and traitbased approaches. Findings to date suggest that adaptive changes in plant traits in response to future [CO 2 ] will not be consistently observed across species or environments and will not be large in magnitude compared with physiological and ecological responses to future [CO 2 ]. This lack of evidence for strong evolutionary effects of elevated [CO 2 ] is surprising, given the large effects of elevated [CO 2 ] on plant phenotypes. New studies under more stressful, complex environmental conditions associated with climate change may revise this view. Efforts are underway to engineer plants to: (i) overcome the limitations to photosynthesis from today's [CO 2 ] and (ii) benefit maximally from future, greater [CO 2 ]. Targets range in scale from manipulating the function of a single enzyme (e.g. Rubisco) to adding metabolic pathways from bacteria as well as engineering the structural and functional components necessary for C 4 photosynthesis into C 3 leaves. Successfully improving plant performance will depend on combining the knowledge of the evolutionary context, cellular basis and physiological integration of plant responses to varying [CO 2 ].

Evolution of C 4 plants: a new hypothesis for an interaction of CO 2 and water relations mediated by plant hydraulics

“…Our hypothesis adds the evolution of C 4 photosynthesis to the list of exceptional innovations based on the plant hydraulic system that arose during periods of low CO 2 that have impacted on plant life history, biogeography and the distribution of ecosystems in the deep past, present and future [107]. Previously hypothesized modifications of the water transport system and associated plant features driven by low CO 2 include the evolution of xylem vessels and stomata [108], and the planate leaf [109,110] with high vein density [78].…”

Evolutionary and Ecological Responses to Anthropogenic Climate Change

“…We may be able to draw from the paleoecological literature to understand extinction risks, migration rates, and potential adaptive responses to climate change (Davis and Shaw, 2001;Leakey and Lau, 2012), especially by focusing on the few geological intervals during which the rate and magnitude of naturally induced climate change were similar to contemporary climate change driven by anthropogenic processes (Willis and MacDonald, 2011). During four geological periods of rapid climate change, macrofossil and pollen records document extensive changes in species' distribution patterns, but species likely also adapted to novel climates (for review, see Willis and MacDonald, 2011).…”

“…Manipulative experiments that include replicated genotypes of known origin, collected from multiple populations across the range of a species, can test all of the hypotheses in Table I (Leakey and Lau, 2012), especially when combined with provenance trials or longitudinal studies. Comparisons of ancestral (pretreatment) and descendant (posttreatment) genotypes in artificial selection experiments can also be used to evaluate whether adaptation to climate change is likely, and if so, how many generations will be needed (Kelly et al, 2012).…”

“…Experiments run in controlled environmental facilities can model past, present, and future climatic conditions to test adaptation to climate in isolation from other environmental factors. However, controlled environments do not reflect the complexity of abiotic and biotic conditions that species experience in nature (Leakey and Lau, 2012). Laboratory studies often overestimate heritabilities (Etterson, 2008), thereby inflating the perceived rate of evolution.…”

“…Although few evolutionary genetic studies have manipulated climatic variables in the field, results to date suggest that the predominant response to elevated CO 2 concentration is physiological, not genetic (for review, see Leakey and Lau, 2012); there is a great need for additional research that exposes replicated genotypes to different climatic treatments for multiple generations. Evolutionary biologists should capitalize on long-term ongoing experiments, such as the warming meadow at the Rocky Mountain Biological Laboratory (Dunne et al, 2003), to investigate the evolutionary implications of climate change (A.M. Panetta, M. Stanton, and J. Harte, unpublished data).…”