Contemporary climate change is proceeding at an unprecedented rate. The question remains whether populations adapted to historical conditions can persist under rapid environmental change. We tested whether climate change will disrupt local adaptation and reduce population growth rates using the perennial plant Boechera stricta (Brassicaceae). In a large‐scale field experiment conducted over five years, we exposed > 106 000 transplants to historical, current, or future climates and quantified fitness components. Low‐elevation populations outperformed local populations under simulated climate change (snow removal) across all five experimental gardens. Local maladaptation also emerged in control treatments, but it was less pronounced than under snow removal. We recovered local adaptation under snow addition treatments, which reflect historical conditions. Our results revealed that low elevation populations risk rapid decline, whereas upslope migration could enable population persistence and expansion at higher elevation locales. Local adaptation to historical conditions could increase vulnerability to climate change, even for geographically widespread species.
Genetically based trait variation across environmental gradients can reflect adaptation to local environments. However, natural populations that appear well-adapted often exhibit directional, not stabilizing, selection on ecologically relevant traits. Temporal variation in the direction of selection could lead to stabilizing selection across multiple episodes of selection, which might be overlooked in short-term studies that evaluate relationships of traits and fitness under only one set of conditions. Furthermore, nonrandom mortality prior to trait expression can bias inferences about trait evolution if viability selection opposes fecundity selection. Here, we leveraged fitness and trait data to test whether phenotypic clines are genetically based and adaptive, whether temporal variation in climate imposes stabilizing selection, and whether viability selection acts on adult phenotypes. We monitored transplants of the subalpine perennial forb, Boechera stricta (Brassicaceae), in common gardens at two elevations over 2-3 years that differed in drought intensity. We quantified viability, and fecundity fitness components for four heritable traits: specific leaf area, integrated water-use efficiency, height at first flower, and flowering phenology. Our results indicate that genetic clines are maintained by selection, but their expression is context dependent, as they do not emerge in all environments. Moreover, selection varied spatially and temporally. Stabilizing selection was most pronounced when we integrated data across years. Finally, viability selection prior to trait expression targeted adult phenotypes (age and size at flowering). Indeed, viability selection for delayed flowering opposed fecundity selection for accelerated flowering; this result demonstrates that neglecting to account for viability selection could lead to inaccurate conclusions that populations are maladapted. Our results suggest that reconciling clinal trait variation with selection requires data collected across multiple spatial scales, time frames, and life-history stages. K E Y W O R D S :Elevational gradient, flowering phenology, invisible fraction, stabilizing selection, specific leaf area, water-use efficiency. Impact SummaryNatural selection has produced extraordinary diversity in adaptations to natural environments. Many species are distributed broadly across climatic gradients, such as elevation or latitude. Natural populations of these species often exhibit continuous clines in morphology and physiology in response to environmental variation. Clines provide supurb opportunities to study natural selection and adaptation. We performed a field experiment replicated across space and over time to evaluate the environmental context of clinal trait variation and natural selection in the perennial montane plant Boechera stricta. We transplanted N = 4510 individuals derived from N = 24 maternal families into natural communities in two experimental gardens. Over 2-3 growing seasons, we measured survival, flowering success, fruit production...
Summary Extensive empirical work has demonstrated local adaptation to discrete environments, yet few studies have elucidated the genetic and environment mechanisms that generate it. Here, we advocate for research that broadens our understanding of local adaptation beyond pattern and towards process. We discuss how studies of local adaptation can be designed to address two unresolved questions in evolutionary ecology: Does local adaptation result from fitness trade‐offs at individual loci across habitats? How do agents of selection interact to generate local adaptation to discrete contrasting habitats types and continuous environmental gradients? To inform future investigations of the genetic basis of local adaptation, we conducted a literature review of studies that mapped quantitative trait loci (QTL) for fitness in native field environments using reciprocal transplant experiments with hybrid mapping populations or Genome‐wide Association Study (GWAS) panels. We then reviewed the literature for field experiments that disentangle the contributions of various agents of selection to local adaptation. For each question, we suggest future lines of inquiry and discuss implications for climate change and agriculture research. (i) Studies in the native habitats of five biological systems revealed that local adaptation is more often caused by conditional neutrality than genetic trade‐offs at the level of the QTL. We consider the ramifications of this result and discuss knowledge gaps in our current understanding of the genetic basis of local adaptation. (ii) We uncovered only five studies that identified the agents of selection that contribute to local adaptation, and nearly all were conducted in discrete habitats rather than across the continuous environmental gradients that many species inhabit. We introduce a novel experimental framework for illuminating the processes underlying local adaptation. A holistic view of local adaptation is critical for predicting the responses of organisms to climate change, enhancing conservation efforts, and developing strategies to improve crop resilience to environmental stress. Experiments that manipulate agents of selection in native field environments using pedigreed populations or GWAS panels offer unique opportunities for detecting the genetic and environmental mechanisms that generate local adaptation.
Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.
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