The value of long-term ecological research for evolutionary insights.

Scientists must have an integrative understanding of ecology and evolution across spatial and temporal scales to predict how species will respond to global change. Although comprehensively investigating these processes in nature is challenging, the infrastructure and data from long-term ecological research networks can support cross-disciplinary investigations. We propose using these networks to advance our understanding of fundamental evolutionary processes and responses to global change. For ecologists, we outline how long-term ecological experiments can be expanded for evolutionary inquiry, and for evolutionary biologists, we illustrate how observed long-term ecological patterns may motivate new evolutionary questions. We advocate for collaborative, multi-site investigations and discuss barriers to conducting evolutionary work at network sites. Ultimately, these networks offer valuable information and opportunities to improve predictions of species' responses to global change.

Defining fitness in evolutionary ecology.

An understanding of biological fitness is central to theory and practice in ecology and evolution, yet fitness remains an elusive concept to define and challenging to measure accurately. Fitness reflects an individual's ability to pass its alleles on to subsequent generations. Researchers often quantify proxies for fitness, such as survival, growth or reproductive success. However, it can be difficult to determine lifetime fitness, especially for species with long lifespans. The abiotic and biotic environment strongly affects the expression of fitness, which means that fitness components can vary through both space and time. This spatial and temporal heterogeneity results in the impressive range of adaptations that we see in nature. Here, we review definitions of fitness and approaches to measuring fitness at the level of genes, individuals, genotypes, and populations and highlight that fitness is a key concept linking ecological and evolutionary thought.

Academic publishing requires linguistically inclusive policies.

Scientific knowledge is produced in multiple languages but is predominantly published in English. This practice creates a language barrier to generate and transfer scientific knowledge between communities with diverse linguistic backgrounds, hindering the ability of scholars and communities to address global challenges and achieve diversity and equity in science, technology, engineering and mathematics (STEM). To overcome those barriers, publishers and journals should provide a fair system that supports non-native English speakers and disseminates knowledge across the globe. We surveyed policies of 736 journals in biological sciences to assess their linguistic inclusivity, identify predictors of inclusivity, and propose actions to overcome language barriers in academic publishing. Our assessment revealed a grim landscape where most journals were making minimal efforts to overcome language barriers. The impact factor of journals was negatively associated with adopting a number of inclusive policies whereas ownership by a scientific society tended to have a positive association. Contrary to our expectations, the proportion of both open access articles and editors based in non-English speaking countries did not have a major positive association with the adoption of linguistically inclusive policies. We proposed a set of actions to overcome language barriers in academic publishing, including the renegotiation of power dynamics between publishers and editorial boards.

Local adaptation: Causal agents of selection and adaptive trait divergence.

Divergent selection across the landscape can favor the evolution of local adaptation in populations experiencing contrasting conditions. Local adaptation is widely observed in a diversity of taxa, yet we have a surprisingly limited understanding of the mechanisms that give rise to it. For instance, few have experimentally confirmed the biotic and abiotic variables that promote local adaptation, and fewer yet have identified the phenotypic targets of selection that mediate local adaptation. Here, we highlight critical gaps in our understanding of the process of local adaptation and discuss insights emerging from in-depth investigations of the agents of selection that drive local adaptation, the phenotypes they target, and the genetic basis of these phenotypes. We review historical and contemporary methods for assessing local adaptation, explore whether local adaptation manifests differently across life history, and evaluate constraints on local adaptation.

Costs of reproduction under experimental climate change across elevations in the perennial forb Boechera stricta.

Investment in current reproduction can reduce future fitness by depleting resources needed for maintenance, particularly under environmental stress. These trade-offs influence life-history evolution. We tested whether climate change alters the future-fitness costs of current reproduction in a large-scale field experiment of Boechera stricta (Brassicaceae). Over 6 years, we simulated climate change along an elevational gradient in the Rocky Mountains through snow removal, which accelerates snowmelt and reduces soil water availability. Costs of reproduction were greatest in arid, lower elevations, where high initial reproductive effort depressed future fitness. At mid-elevations, initial reproduction augmented subsequent fitness in benign conditions, but pronounced costs emerged under snow removal. At high elevation, snow removal dampened costs of reproduction by prolonging the growing season. In most scenarios, failed reproduction in response to resource limitation depressed lifetime fecundity. Indeed, fruit abortion only benefited high-fitness individuals under benign conditions. We propose that climate change could shift life-history trade-offs in an environment-dependent fashion, possibly favouring early reproduction and short lifespans in stressful conditions.

Climate change disrupts local adaptation and favours upslope migration.

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.

Transgenerational and Within-Generation Plasticity in Response to Climate Change: Insights from a Manipulative Field Experiment across an Elevational Gradient.

Parental environmental effects-or transgenerational plasticity-can influence an individual's phenotype or fitness yet remain underexplored in the context of global change. Using the perennial self-pollinating plant Boechera stricta, we explored the effects of climate change on transgenerational and within-generation plasticity in dormancy, germination, growth, and survival. We first conducted a snow removal experiment in the field, in which we transplanted 16 families of known origin into three common gardens at different elevations and exposed half of the siblings to contemporary snow dynamics and half to early snow removal. We planted the offspring of these individuals in a factorial manipulation of temperature and water level in the growth chamber and reciprocally transplanted them across all parental environments in the field. The growth chamber experiment revealed that the effects of transgenerational plasticity persist in traits expressed after establishment, even when accounting for parental effects on seed mass. The field experiment showed that transgenerational and within-generation plasticity can interact and that plasticity varies clinally in populations distributed across elevations. These findings demonstrate that transgenerational plasticity can influence fitness-related traits and should be incorporated in studies of biological responses to climate change.

Phenological responses to multiple environmental drivers under climate change: insights from a long-term observational study and a manipulative field experiment.

Climate change has induced pronounced shifts in the reproductive phenology of plants, yet we know little about which environmental factors contribute to interspecific variation in responses and their effects on fitness. We integrate data from a 43 yr record of first flowering for six species in subalpine Colorado meadows with a 3 yr snow manipulation experiment on the perennial forb Boechera stricta (Brassicaceae) from the same site. We analyze shifts in the onset of flowering in relation to environmental drivers known to influence phenology: the timing of snowmelt, the accumulation of growing degree days, and photoperiod. Variation in responses to climate change depended on the sequence in which species flowered, with early-flowering species reproducing faster, at a lower heat sum, and under increasingly disparate photoperiods relative to later-flowering species. Early snow-removal treatments confirm that the timing of snowmelt governs observed trends in flowering phenology of B. stricta and that climate change can reduce the probability of flowering, thereby depressing fitness. Our findings suggest that climate change is decoupling historical combinations of photoperiod and temperature and outpacing phenological changes for our focal species. Accurate predictions of biological responses to climate change require a thorough understanding of the factors driving shifts in phenology.

Phenological mismatch and the effectiveness of assisted gene flow.

The persistence of narrowly adapted species under climate change will depend on their ability to migrate apace with their historical climatic envelope or to adapt in place to maintain fitness. This second path to persistence can only occur if there is sufficient genetic variance for response to new selection regimes. Inadequate levels of genetic variation can be remedied through assisted gene flow (AGF), that is the intentional introduction of individuals genetically adapted to localities with historic climates similar to the current or future climate experienced by the resident population. However, the timing of reproduction is frequently adapted to local conditions. Phenological mismatch between residents and migrants can reduce resident × migrant mating frequencies, slowing the introgression of migrant alleles into the resident genetic background and impeding evolutionary rescue efforts. Focusing on plants, we devised a method to estimate the frequency of resident × migrant matings based on flowering schedules and applied it in an experiment that mimicked the first generation of an AGF program with Chamaecrista fasciculata, a prairie annual, under current and expected future temperature regimes. Phenological mismatch reduced the potential for resident × migrant matings by 40-90%, regardless of thermal treatment. The most successful migrant sires were the most resident like in their flowering time, further biasing the genetic admixture between resident and migrant populations. Other loci contributing to local adaptation-heat-tolerance genes, for instance-may be in linkage disequilibrium with phenology when residents and migrants are combined into a single mating pool. Thus, introgression of potentially adaptive migrant alleles into the resident genetic background is slowed when selection acts against migrant phenology. Successful AGF programs may require sustained high immigration rates or preliminary breeding programs when phenologically matched migrant source populations are unavailable.

Integrating viability and fecundity selection to illuminate the adaptive nature of genetic clines.

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.

The success of assisted colonization and assisted gene flow depends on phenology.

Global warming will jeopardize the persistence and genetic diversity of many species. Assisted colonization, or the movement of species beyond their current range boundary, is a conservation strategy proposed for species with limited dispersal abilities or adaptive potential. However, species that rely on photoperiodic and thermal cues for development may experience conflicting signals if transported across latitudes. Relocating multiple, distinct populations may remedy this quandary by expanding genetic variation and promoting evolutionary responses in the receiving habitat--a strategy known as assisted gene flow. To better inform these policies, we planted seeds from latitudinally distinct populations of the annual legume, Chamaecrista fasciculata, in a potential future colonization site north of its current range boundary. Plants were exposed to ambient or elevated temperatures via infrared heating. We monitored several life history traits and estimated patterns of natural selection to determine the adaptive value of plastic responses. To assess the feasibility of assisted gene flow between phenologically distinct populations, we counted flowers each day and estimated the degree of temporal isolation between populations. Increased temperatures advanced each successive phenological trait more than the last, resulting in a compressed life cycle for all but the southern-most population. Warming altered patterns of selection on flowering onset and vegetative biomass. Population performance was dependent on latitude of origin, with the northern-most population performing best under ambient conditions and the southern-most performing most poorly, even under elevated temperatures. Among-population differences in flowering phenology limited the potential for genetic exchange among the northern- and southern-most populations. All plastic responses to warming were neutral or adaptive; however, photoperiodic constraints will likely necessitate evolutionary responses for long-term persistence, especially when involving populations from disparate latitudes. With strategic planning, our results suggest that assisted colonization and assisted gene flow may be feasible options for preservation.

Hard and soft selection on phenology through seasonal shifts in the general and social environments: A study on plant emergence time.

The timing of transition out of one life-history phase determines where in the seasonal succession of environments the next phase is spent. Shifts in the general environment (e.g., seasonal climate) affect the expected fitness for particular transition dates. Variation in transition date also leads to temporal variation in the social environment. For instance, early transition may confer a competitive advantage over later individuals. If so, the social environment will impose frequency- and density-dependent selection components. In effect, the general environment imposes hard selection, whereas the social environment imposes soft selection on phenology. We examined hard and soft selection on seedling emergence time in an experiment on Brassica rapa. In monoculture (uniform social environment), early emergence results in up to a 1.5-fold increase in seed production. In bicultures (heterogeneous social environment), early-emerging plants capitalized on their head start, suppressing their late neighbors and increasing their fitness advantage to as much as 38-fold, depending on density. We devised a novel adaptation of contextual analysis to partition total selection (i.e., cov(ω, z)) into the hard and soft components. Hard and soft components had similar strengths at low density, whereas soft selection was five times stronger than hard at high density.