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Review Tansley insight Plant fitness in a rapidly changing world Author for correspondence: Jill T. Anderson Tel: +1 706 542 0853 Email: [email protected] Jill T. Anderson1,2 1 Department Genetics, University of Georgia, Athens, GA 30602, USA; 2Odum School of Ecology, University of Georgia, Athens, GA 30602, USA Received: 17 June 2015 Accepted: 25 August 2015 Contents Summary 81 IV. Evolutionary consequences 84 I. Introduction 81 V. Conclusions 85 II. Fitness landscapes 82 Acknowledgements 85 III. Recommendations for future studies 84 References 85 Summary New Phytologist (2016) 210: 81–87 doi: 10.1111/nph.13693 Key words: climate change, climatic manipulation, evolution, fecundity, fitness, germination, meta-analysis, migration. Modern reliance on fossil fuels has ushered in extreme temperatures globally and abnormal precipitation patterns in many regions. Although the climate is changing rapidly, other agents of natural selection such as photoperiod remain constant. This decoupling of previously reliable environmental cues shifts adaptive landscapes, favors novel suites of traits and likely increases the extinction risk of local populations. Here, I examine the fitness consequences of changing climates. Meta-analyses demonstrate that simulated future climates depress viability and fecundity components of fitness for native plant species in the short term, which could reduce population growth rates. Contracting populations that cannot adapt or adjust plastically to new climates might not be capable of producing sufficient migrants to track changing conditions. I. Introduction Climate change brings to the forefront a long-standing question at the interface of ecology and evolution: what are the evolutionary consequences of rapid environmental change? The answer will shape conservation priorities, shed light on the genetic and phenotypic fates of communities, and enhance our understanding of evolution. Climate change has already disrupted phenology and physiology, and altered community dynamics (Elmendorf et al., 2012; Leonardi et al., 2012; CaraDonna et al., 2014). Species as diverse as plants, arthropods, birds and fish have experienced recent range contractions and expansions (Chen et al., 2011). However, distributional Jill Anderson was a finalist for the 2015 New Phytologist Tansley Medal for excellence in plant science, which recognises an outstanding contribution to research in plant science by an individual in the early stages of their career; see the Editorial by Lennon & Dolan, 210: 5 Ó 2015 The Author New Phytologist Ó 2015 New Phytologist Trust shifts do not always occur in the predicted direction of higher elevations or poleward latitudes (VanDerWal et al., 2013; Rapacciuolo et al., 2014). Additionally, the ranges of some species are contracting on both cooler and warmer edges, as evinced by narrower latitudinal distributions of seedlings than adult trees in contemporary landscapes (Zhu et al., 2012). Many species will not be able to disperse fast enough to track rapidly changing climates (Loarie et al., 2009), and extensive habitat fragmentation will obstruct migration (Kremer et al., 2012). Adaptive evolution, gene flow and phenotypic plasticity could buffer populations from climate change (Nicotra et al., 2010; Gonzalez et al., 2013; Carlson et al., 2014). High fecundity, large population sizes, broad geographic distributions, spatially extensive dispersal, plasticity and rapid generation times could enable population persistence (Aitken et al., 2008; Alsos et al., 2012). A burgeoning literature explores ecoevolution in the context of climate change, the genetic basis of climatic adaptation, and conservation in a changing world New Phytologist (2016) 210: 81–87 81 www.newphytologist.com New Phytologist Tansley insight (Gienapp et al., 2008; Hoffmann & Sgro, 2011; Shaw & Etterson, 2012; Aitken & Whitlock, 2013; Alberto et al., 2013; Franks et al., 2014). Yet we lack a comprehensive analysis of how changing climates influence fitness in natural populations. If climate change diminishes fitness, it could reduce the adaptive and migratory potential of populations. As shifting range dynamics have been discussed in depth (Valladares et al., 2014), my objectives are to evaluate shifting fitness landscapes in native plant populations in the core portions of their ranges, to discuss methods that could improve the predictive power of climate change experiments and to examine the evolutionary significance of novel selective regimes. Mid-elevation common garden B A Fitness 82 Review II. Fitness landscapes Climate change decouples agents of selection Natural populations evolve in response to complex suites of abiotic and biotic conditions. Climatic factors such as temperature and precipitation shape evolution (Kim & Donohue, 2013), influence population growth rates (Dalgleish et al., 2011) and govern species distributions (Chen et al., 2011). Plants also adapt locally to variation in nonclimatic factors, including herbivores (Garrido et al., 2012), pollinators (Boberg et al., 2014), mycorrhizal fungi (Johnson et al., 2010), edaphic conditions (Gould et al., 2014) and photoperiod (Friedman & Willis, 2013). Human activities are simultaneously modifying multiple abiotic and biotic agents of selection, and decoupling linked cues including photoperiod and temperature that trigger phenological transitions (Bradshaw & Holzapfel, 2008), resulting in growing discrepancies between current and optimal phenotypes (Etterson, 2004). By altering selection on genetically correlated traits (Etterson & Shaw, 2001), climate change could depress fitness (Kingsolver et al., 2013) and cause widespread local maladaptation in the short term (Fig. 1) (Wilczek et al., 2014). Even species that migrate rapidly will encounter biotic and abiotic conditions in their expanded ranges to which they are not currently adapted (Brown & Vellend, 2014). The question remains whether adaptation can keep pace with rapid climate change (Gonzalez et al., 2013) or whether declining fitness could lead to extinction of local populations (Valladares et al., 2014). Individual plant performance links demography and evolution: fitness components and vital rates include germination success, survival, flowering success and fecundity (Morris et al., 2008). If climate change reduces the average fitness of individuals, population growth rates may decline (Clark et al., 2012), leading to lower effective population sizes. Contracting populations are susceptible to demographic stochasticity, loss of genetic diversity and adaptive potential, and further reductions in fitness from inbreeding depression (Bijlsma & Loeschcke, 2012; Gossmann et al., 2012). Importantly, even if the proportion of seeds and pollen that disperse out of a local population remains constant, fewer seeds and pollen grains will emigrate from shrinking populations. Simulations demonstrate that low abundance can inhibit emigration (Nabel et al., 2013). Small populations attract fewer pollinators (Duffy et al., 2013), reducing plant fecundity and the extent of gene flow via pollen. Long-distance dispersal is typically considered to be rare (Nathan, 2006), and could become even less frequent if climate change decreases seed production. Reductions in New Phytologist (2016) 210: 81–87 www.newphytologist.com Contemporary climate Future climate Elevation of origin (m) Fig. 1 Climate change could disrupt local adaptation. Climate change exposes natural populations to novel combinations of climatic and nonclimatic conditions, which likely causes fitness landscapes to shift. Migrants that disperse to upslope elevations or poleward latitudes could remain within their historical climatic niche, but will likely confront nonclimatic factors to which they are not adapted. Researchers can transplant seeds and seedlings of genotypes from across the range of a species into common gardens to evaluate the extent of local adaptation to climate in a forestry approach known as provenance trials (e.g. Wang et al., 2010). By pairing this approach with climatic manipulations, researchers can assay fitness not only in current conditions, but also in response to simulated climate change to test whether climate change disrupts local adaptation by favoring genotypes that evolved under warmer and drier conditions. This hypothetical example assesses fitness as a function of provenance elevation (a proxy for climate) for genotypes transplanted into a mid-elevation common garden (indicated with a star) in a species that has populations distributed across a broad elevational gradient. The full experiment would be conducted simultaneously in multiple common gardens. In contemporary conditions, genotypes that evolved in climates similar to that of the common garden have optimal fitness. In simulated future climates, individuals experience a combination of new climatic conditions plus historical nonclimatic environments. Global change could depress short-term fitness because of the decoupling of climatic and nonclimatic agents of selection (arrow A), favoring genotypes from warmer regions over local ecotypes (arrow B). This shift would lead to local maladaptation, as genotypes would no longer occur where they have the greatest fitness. These experiments can be conducted in gardens across any relevant climatic gradients, including latitude, longitude and elevation. To generate realistic fitness curves, seeds and seedlings would be planted with minimal disturbance to the natural community, and would not be supplemented with water or other resources after the risk of transplant shock subsides. fitness caused by climate change could diminish the potential for populations to migrate to areas with favorable climates, and could underlie recent observations that distributions are not simply shifting poleward or upslope (Zhu et al., 2012). Short-term fitness consequences of climate change To test the hypothesis that climate change depresses plant fitness in the short-term, I conducted a phylogenetically controlled metaanalysis of field studies that manipulated one or more climatic Ó 2015 The Author New Phytologist Ó 2015 New Phytologist Trust New Phytologist Ó 2015 The Author New Phytologist Ó 2015 New Phytologist Trust Review 83 (a) Binary fitness components Log odds ratio 3 2 [CO2]: 2 studies 13 species Passive warming Reduced water Snow removal Infrared heating Warming + drought 9 studies 21 species 5 studies 6 species 5 studies 19 species 5 studies 38 species 2 studies 7 species 1 0 –1 –2 –3 (b) Fecundity fitness components: individual level Log response ratio [CO2]: 4 1 study 1 species Passive warming Reduced water Infrared heating [CO2] + warming 12 studies 30 species 8 studies 12 species 3 studies 11 species 1 study 1 species 2 0 –2 –4 (c) Fecundity fitness components: population level [CO2]: Log response ratio factors (see Supporting Information Methods S1 for details on methods, results and diagnostics, and Notes S1–S5 for datasets). The meta-analysis focused on 157 native plant species in core populations in 60 studies that quantified fitness for at least one life history stage, from germination to survival to fecundity. The most recent metaanalysis on this topic suggested that warming may enhance reproductive success for tundra plants, but did not present viability data or include studies from other ecosystems (Arft et al., 1999). Field studies test fitness responses in plants exposed to novel climates and historical nonclimatic agents of selection; these experiments more realistically reflect the decoupling of environmental signals that natural populations will confront than do studies in controlled conditions. Experiments included in the metaanalyses simulated climates projected to occur within the next century (Methods S1). For many systems, manipulations fall within the range of current climatic variability, such as 0.32–4.0°C increase in growing season temperature, or 15–50% reduction in precipitation. Several studies in Mediterranean climates simulated historical conditions via supplemental watering, documenting declines in plant fitness in response to increasing drought frequency (Matesanz et al., 2009; Pratt & Mooney, 2013). Three manipulations depressed viability (germination, seedling establishment, and juvenile and adult survival): warming via infrared heaters (z = 2.28, P = 0.023), snow removal (z = 2.44, P = 0.015) and warming plus drought (z = 2.64, P = 0.0084); however, there was no effect of elevated CO2 concentration, drought or warming via open top chambers (Fig. 2a). The fecundity meta-analysis revealed that infrared heaters reduced individual-level fitness (number of reproductive structures per individual plant, z = 2.53, P = 0.011, Fig. 2b) and that drought stress reduced population-level fitness (number of reproductive structures per unit area, z = 2.01, P = 0.045, Fig. 2c). Infrared heating lamps mimic climatic projections for many regions over the next century (Dunne et al., 2003; Pfeifer-Meister et al., 2013). The key result is that germination and survival are particularly susceptible to multiple climate change factors, and that studies focused entirely on fecundity will underestimate fitness consequences of climate change. Similarly, a recent meta-analysis indicated that intense and frequent floods projected under climate change reduced survival of riparian plants during intense and frequent floods projected under climate change (Garssen et al., 2015). In concert, these results suggest that novel climatic regimes could depress recruitment even in established populations (Pe~ nuelas et al., 2004), and that conservation efforts should be aimed at increasing viability. Future studies should aim to quantify vital rates across multiple life history stages to project population growth under various climate scenarios. Experiments in the meta-analysis occurred within natural communities: changes in fitness resulted from direct and indirect effects of altered climates. Indirect effects of global change on species interactions have profound consequences for eco-evolutionary dynamics (Lau et al., 2014). For example, drought-adapted soil microbial communities attenuated reductions in fecundity in response to drought in Brassica rapa (Lau & Lennon, 2012). By contrast, drought stress increased floral herbivory on Hypericum perforatum, depressing fecundity (Fox et al., 1999). Direct and Tansley insight 2 1 3 studies 3 species Passive warming Reduced water Infrared heating 5 studies 8 species 2 studies 3 species 1 study 7 species 0 –1 –2 –3 Fig. 2 Results of two separate meta-analyses examining the fitness consequences of climatic manipulations under field conditions for native plant species. I initially screened titles and abstracts of 546 papers, of which 28 studies (92 species total) contained suitable data for binary fitness components (germination, seedling establishment, juvenile survival and adult survival; Table S1a within Supporting Information Methods S1) and 37 studies (86 species total) contained data on reproductive components of fitness (Table S1b within Methods S1). Manipulations included reduced water availability (generally via rainout shelters), passive warming (typically controlled via open-top chambers), active warming (infrared heaters), snow removal, elevated [CO2], and warming + reduced water availability. In snow-dominated regions (high elevation and high latitude), warming winters reduce snowpack, and warming springs cause snow to melt early (Hewitson et al., 2014); snow removal efficiently simulates these changing dynamics (Anderson & Gezon, 2015). Effect sizes are reported as the natural log of odds ratios for binary fitness components (a) and natural log of response ratios for continuous fecundity variables (b, c) in treatment relative to control groups. Values < 0 indicate that fitness was lower under simulated climate change (treatment) than contemporary conditions (control) in the field. Symbols represent mean effect sizes and bars are 95% confidence intervals. (a) Meta-analysis of binary fitness components showed that snow removal, infrared heating lamps, and warming plus drought depressed germination success, seedling establishment, and juvenile and adult survival. (b, c) Fecundity data were available at the level of the individual plant (e.g. number of flowers, fruits or seeds per individual) for 55 records (species by study combinations). For the remaining 40 records, fecundity data were presented on a population level, either per unit area (e.g. number of seeds or seed biomass per m2) or per plot (e.g. fecundity per experimental block). The fecundity meta-analysis revealed a significant interaction (P = 0.0015) between climatic factor and the level of the data (individual or population). (b) Infrared heating lamps depressed fecundity, but other climatic manipulations had no overall effect on flower, fruit or seed production on individual plants. (c) Drought stressed reduced population-level fecundity. Population data integrate across survival and fecundity, and provide a more nuanced perspective on population-level consequences of specific climatic manipulations. New Phytologist (2016) 210: 81–87 www.newphytologist.com 84 Review New Phytologist Tansley insight indirect effects can be either positive or negative, and remain to be examined explicitly in most systems. Intense precipitation events have been linked to expansion of woody plants into semi-arid ecosystems (Kulmatiski & Beard, 2013), and shrubs have encroached into alpine, tundra, grassland and savannah habitats (Eldridge et al., 2011; Formica et al., 2014). Climate change could induce temporal or spatial mismatches with pollinators or other mutualists (Gordo & Sanz, 2005), and increased prevalence of herbivory or disease (de Sassi & Tylianakis, 2012) beyond what is seen in the spatiotemporal scale of climate change experiments. Nonanalog climates will likely reshape biotic interactions. Climatic experiments have been concentrated in alpine, arctic, polar and temperate regions. Species in tropical ecosystems have a much more restricted climatic tolerance (Kingsolver et al., 2013) and lower climatic plasticity, yet there is a dearth of climate-change studies of tropical plant species (Cavaleri et al., 2015). I found no studies assessing plant fitness in tropical climate change experiments, even though species with restricted climatic tolerances and limited distributions could be particularly vulnerable to changing climates. Field experiments mimic abrupt changes in climate and extreme events that are projected to increase in frequency (Hansen et al., 2012; Reyer et al., 2013); however, they might not capture responses to gradually changing climates. Nevertheless, these manipulations are relevant to population dynamics in an increasingly variable climate. In a study of vital rates in 36 plant and animal species, Morris et al. (2008) found that increased interannual variability in survival and reproduction depressed long-term population growth, especially for short-lived species. Even if the climate returns to baseline conditions following perturbation, extreme events could reduce long-term population growth (but see Koons et al., 2009). Finally, short-term manipulations can reflect longer-term responses of natural communities to climate change (Harte et al., 2015). fitness consequences of global change (Shaw & Etterson, 2012; Kim & Donohue, 2013). The provenance trial approach (Fig. 1) often reveals that fitness declines with increasing climatic distance between the source population and the experimental garden (Wang et al., 2010; Wilczek et al., 2014). However, nonclimatic agents of selection vary spatially and distort inferences about adaptation to climate change. Combining transplant experiments with climatic manipulations increases realism and predictive power (PfeiferMeister et al., 2013), enabling researchers to address the implications of climate change for fitness, adaptation and selection in local populations, and the performance of (transplanted) migrants in contemporary and simulated future climates. Studies designed to estimate genetic variance in fitness under various climates could examine the adaptive potential of populations (Shaw & Shaw, 2014). Evolutionary field studies can test whether climate change will outpace adaptation (Wilczek et al., 2014), and dissect the factors that constrain migration (Brown & Vellend, 2014). Few published field studies simultaneously manipulate multiple global change factors (but see Matesanz et al., 2009). Multifactorial studies impose treatments that more closely resemble climate change scenarios than single factor studies (Beier et al., 2012). Additionally, regression-based manipulations enable researchers to examine fitness across multiple levels of climatic factors to achieve a more precise estimate of how climate affects fitness (Marchin et al., 2014). Researchers have begun to simulate extreme events, exposing experimental individuals to fluctuations in the severity of warming or drought stress (Jentsch et al., 2007). Furthermore, by recreating historical climates in the field through manipulations such as supplemental precipitation (Matesanz et al., 2009), studies could illuminate the extent to which climate change has already altered eco-evolutionary dynamics. Results of these studies will highlight when intervention, such as assisted migration/gene flow (Aitken & Whitlock, 2013), is needed to conserve species. Plant fitness through time IV. Evolutionary consequences Longitudinal studies that assess vital rates in relation to temporal variation in climate (Clark et al., 2011) can identify responses to gradually changing climates. Such studies have documented droughtinduced mortality in adult trees over the past century (Bigler et al., 2007), and found that increasingly prevalent water stress diminishes juvenile recruitment (Pe~ nuelas et al., 2004). Plant populations could be particularly susceptible in regions where drought frequency and intensity are projected to increase. Furthermore, Willis et al. (2008) found that species that did not adjust their flowering phenology to changing climates declined in abundance from the 1850s to the 2000s. Such studies require a long time horizon, historical data or archived seeds (Franks et al., 2008). Funding cycles might not support the lengthy periods of data collection required to detect longitudinal trends. Field experiments increase our ability to identify species and regions vulnerable to climate change. If natural populations do not have sufficient genetic variation to adapt to changing local conditions or to a new habitat in a shifted geographic range, the average fitness of populations could decline rapidly, depressing emigration rates and increasing extinction risk. If climate change-mediated selection drives genetically correlated traits in antagonistic directions, evolutionary response could be negligible or even maladaptive (Etterson & Shaw, 2001), and adaptive evolution could lag far behind global change (Wilczek et al., 2014). Adaptational lag could be especially pronounced for species with small effective population sizes subject to abruptly changing conditions (Gonzalez et al., 2013), which are likely to occur more frequently under increased climatic variability (Hansen et al., 2012). If reductions in fitness coincide with reductions in genetic variance in fitness, climate change could exacerbate adaptational lags. Adaptation and plasticity could counteract the negative shortterm effects of global change. Phenotypic plasticity may enable populations to persist in situ or establish in new habitats (Chevin et al., 2013; Anderson & Gezon, 2015), and increased climatic variation could selectively favor plasticity (Nicotra et al., 2010). Micro-environmental variation within sites could also buffer local III. Recommendations for future studies Transplanting propagules into sites that mirror climatic projections (e.g. lower elevations) could provide insight into the long-term New Phytologist (2016) 210: 81–87 www.newphytologist.com Ó 2015 The Author New Phytologist Ó 2015 New Phytologist Trust New Phytologist populations from immediate fitness reductions (De Frenne et al., 2013). If selection is strong and genetic constraints minimal, adaptive evolution could track climate change in species that maintain high genetic variation and effective population sizes (Franks et al., 2014; Gould et al., 2014; Ravenscroft et al., 2014). For example, Thompson et al. (2013) demonstrated an adaptive reduction in winter freezing tolerance of wild thyme populations in response to warming from the 1970s to 2010. Gene flow could promote adaptation to novel suites of environments if alleles adapted to elevated temperatures, drought, reduced snowpack or other conditions associated with climate change become introgressed into locally adapted populations in upslope or poleward locations (Aitken & Whitlock, 2013). If natural populations rapidly adapt to novel climates, global change models might overestimate extinction risks and generate unreliable future distribution maps. V. Conclusions Climate change has already altered selection on traits in natural populations. Novel suites of climatic and nonclimatic conditions may reduce viability and fecundity components of fitness, and hinder the adaptive and migratory potential of local populations. Species that cannot keep pace with environmental change risk extinction (Willis et al., 2008). However, some plants are capable of rapid adaptation to novel climates (Franks et al., 2007; Nevo et al., 2012; Thompson et al., 2013) and some populations could adjust plastically (Anderson & Gezon, 2015). Future studies should combine data on fitness under climate change scenarios with estimates of the spatial extent of seed and pollen dispersal. Emerging modeling techniques can incorporate population dynamics and plasticity into global change models to forecast extinction risks (Fordham et al., 2012; Valladares et al., 2014). Ultimately, population persistence could be greatest for those species capable of tracking shifting adaptive landscapes via a combination of migration of propagules, gene flow, adaptation and plasticity. Acknowledgements I thank Thomas Pendergast and Monica Geber for discussion and comments on a previous version, Craig Osenberg for advice on meta-analysis, and three anonymous reviewers for critiques. References Aitken SN, Whitlock MC. 2013. 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