Identifying potential evolutionary consequences of climate-driven phenological shifts

Climate change is shifting the phenology of many species throughout the world. While the interspecific consequences of these phenological shifts have been well documented, the intraspecific shifts and their resultant evolutionary consequences remain relatively unexplored. Here, we present a conceptual framework and overview of how phenological shifts within species can drive evolutionary change. We suggest that because the impacts of climate change are likely to vary across the range of a species and differentially impact individuals, phenological shifts may often be highly variable both within and among populations. Together these changes have the potential to alter existing patterns of gene flow and influence evolutionary trajectories by increasing phenological isolation and connectivity. Recent research examining the response of species to contemporary climate change suggests that both phenological isolation and connectivity may be likely responses to future climate change. However, recent studies also show mixed results on whether adaptive responses to climate change are likely to occur, as some populations have already shown adaptive responses to changing climate, while others have not despite fitness costs. While predicting the exact consequences of intraspecific phenological shifts may be difficult, identifying the evolutionary implications of these shifts will allow a better understanding of the effects of future climate change on species persistence and adaptation.     

A perspective on match/mismatch of phenology in community contexts

Climate change has significant impacts on phenology of various organisms in a species‐specific manner. Facing this problem, the match/mismatch hypothesis that phenological (a)synchrony with resource availability strongly influences recruitment success of a consumer population has recently received much attention. In this article, we discuss extending the conventional pairwise concept and demonstrate a community module‐based approach as an initial step for exploring community consequences of species‐specific phenological shifts caused by climate change. Our multispecies match/mismatch perspective leads to the prediction that phenological (a)synchrony among interacting species critically affects not only population recruitment of species but also key dynamical features of ecological communities such as trophic cascades, competitive hierarchies, and species coexistence. Explicit identification and consideration of species relationships is therefore desirable for a better understanding of seasonal community dynamics and thus community consequences of climate change‐induced phenological shifts.     

Phenological indices of avian reproduction: cryptic shifts and prediction across large spatial and temporal scales

Climate change‐induced shifts in phenology have important demographic consequences, and are frequently used to assess species' sensitivity to climate change. Therefore, developing accurate phenological predictions is an important step in modeling species' responses to climate change. The ability of such phenological models to predict effects at larger spatial and temporal scales has rarely been assessed. It is also not clear whether the most frequently used phenological index, namely the average date of a phenological event across a population, adequately captures phenological shifts in the distribution of events across the season. We use the long‐tailed tit Aegithalos caudatus (Fig. 1) as a case study to explore these issues. We use an intensive 17‐year local study to model mean breeding date and test the capacity of this local model to predict phenology at larger spatial and temporal scales. We assess whether local models of breeding initiation, termination, and renesting reveal phenological shifts and responses to climate not detected by a standard phenological index, that is, population average lay date. These models take predation timing/intensity into account. The locally‐derived model performs well at predicting phenology at the national scale over several decades, at both high and low temperatures. In the local model, a trend toward warmer Aprils is associated with a significant advance in termination dates, probably in response to phenological shifts in food supply. This results in a 33% reduction in breeding season length over 17 years – a substantial loss of reproductive opportunity that is not detected by the index of population average lay date. We show that standard phenological indices can fail to detect patterns indicative of negative climatic effects, potentially biasing assessments of species' vulnerability to climate change. More positively, we demonstrate the potential of detailed local studies for developing broader‐scale predictive models of future phenological shifts.     

The eco‐evolutionary consequences of interspecific phenological asynchrony – a theoretical perspective

The timing of biological events (phenology) is an important aspect of both a species’ life cycle and how it interacts with other species and its environment. Patterns of phenological change have been given much scientific attention, particularly recently in relation to climate change. For pairs of interacting species, if their rates of phenological change differ, then this may lead to asynchrony between them and disruption of their ecological interactions. However it is often difficult to interpret differential rates of phenological change and to predict their ecological and evolutionary consequences. We review theoretical results regarding this topic, with special emphasis on those arising from life history theory, evolutionary game theory and population dynamic models. Much ecological research on phenological change builds upon the concept of match/mismatch, so we start by putting forward a simple but general model that captures essential elements of this concept. We then systematically compare the predictions of this baseline model with expectations from theory in which additional ecological mechanisms and features of species life cycles are taken into account. We discuss the ways in which the fitness consequences of interspecific phenological asynchrony may be weak, strong, or idiosyncratic. We discuss theory showing that synchrony is not necessarily an expected evolutionary outcome, and how population densities are not necessarily maximized by adaptation, and the implications of these findings. By bringing together theoretical developments regarding the eco‐evolutionary consequences of phenological asynchrony, we provide an overview of available alternative hypotheses for interpreting empirical patterns as well as the starting point for the next generation of theory in this field.     

Community‐wide changes in intertaxonomic temporal co‐occurrence resulting from phenological shifts

Global climate change is known to affect the assembly of ecological communities by altering species' spatial distribution patterns, but little is known about how climate change may affect community assembly by changing species' temporal co‐occurrence patterns, which is highly likely given the widely observed phenological shifts associated with climate change. Here, we analyzed a 29‐year phenological data set comprising community‐level information on the timing and span of temporal occurrence in 11 seasonally occurring animal taxon groups from 329 local meteorological observatories across China. We show that widespread shifts in phenology have resulted in community‐wide changes in the temporal overlap between taxa that are dominated by extensions, and that these changes are largely due to taxa's altered span of temporal occurrence rather than the degree of synchrony in phenological shifts. Importantly, our findings also suggest that climate change may have led to less phenological mismatch than generally presumed, and that the context under which to discuss the ecological consequences of phenological shifts should be expanded beyond asynchronous shifts.     

Phenological plasticity is a poor predictor of subalpine plant population performance following experimental climate change

Phenological shifts, changes in the seasonal timing of life cycle events, are among the best documented responses of species to climate change. However, the consequences of these phenological shifts for population dynamics remain unclear. Population growth could be enhanced if species that advance their phenology benefit from longer growing seasons and gain a pre-emptive advantage in resource competition. However, it might also be reduced if phenological advances increase exposure to stresses, such as herbivores and, in colder climates, harsh abiotic conditions early in the growing season. We exposed subalpine grasslands to ~3 K of warming by transplanting intact turfs from 2000 m to 1400 m elevation in the eastern Swiss Alps, with turfs transplanted within the 2000 m site acting as a control. In the first growing season after transplantation, we recorded species’ flowering phenology at both elevations. We also measured species’ cover change for three consecutive years as a measure of plant performance. We used models to estimate species’ phenological plasticity (the response of flowering time to the change in climate) and analysed its relationship with cover changes following climate change. The phenological plasticity of the 18 species in our study varied widely but was unrelated to their changes in cover. Moreover, early- and late-flowering species did not differ in their cover response to warming, nor in the relationship between cover changes and phenological plasticity. These results were replicated in a similar transplant experiment within the same subalpine community, established one year earlier and using larger turfs. We discuss the various ecological processes that can be affected by phenological shifts, and argue why the population-level consequences of these shifts are likely to be species- and context-specific. Our results highlight the importance of testing assumptions about how warming-induced changes in phenotypic traits, like phenology, impact population dynamics.     

Earlier Migration Timing,Decreasing Phenotypic Variation,and Biocomplexity in Multiple Salmonid Species

Climate-induced phenological shifts can influence population, evolutionary, and ecological dynamics, but our understanding of these phenomena is hampered by a lack of long-term demographic data. We use a multi-decade census of 5 salmonid species representing 14 life histories in a warming Alaskan stream to address the following key questions about climate change and phenology: How consistent are temporal patterns and drivers of phenology for similar species and alternative life histories? Are shifts in phenology associated with changes in phenotypic variation? How do phenological changes influence the availability of resource subsidies? For most salmonid species, life stages, and life histories, freshwater temperature influences migration timing – migration events are occurring earlier in time (mean = 1.7 days earlier per decade over the 3–5 decades), and the number of days over which migration events occur is decreasing (mean = 1.5 days per decade). Temporal trends in migration timing were not correlated with changes in intra-annual phenotypic variation, suggesting that these components of the phenotypic distribution have responded to environmental change independently. Despite commonalities across species and life histories, there was important biocomplexity in the form of disparate shifts in migration timing and variation in the environmental factors influencing migration timing for alternative life history strategies in the same population. Overall, adult populations have been stable during these phenotypic and environmental changes (λ ≈1.0), but the temporal availability of salmon as a resource in freshwater has decreased by nearly 30 days since 1971 due to changes in the median date of migration timing and decreases in intra-annual variation in migration timing. These novel observations advance our understanding of phenological change in response to climate warming, and indicate that climate change has influenced the ecology of salmon populations, which will have important consequences for the numerous species that depend on this resource.     

Predicting population consequences of ocean climate change for an ecosystem sentinel,the seabird Cassin's auklet

Forecasting the ecological effects of climate change on marine species is critical for informing greenhouse gas mitigation targets and developing marine conservation strategies that remain effective and increase species' resilience under changing climate conditions. Highly productive coastal upwelling systems are predicted to experience substantial effects from climate change, making them priorities for ecological forecasting. We used a population modeling approach to examine the consequences of ocean climate change in the California Current upwelling ecosystem on the population growth rate of the planktivorous seabird Cassin's auklet (Ptychoramphus aleuticus), a demographically sensitive indicator of marine climate change. We use future climate projections for sea surface temperature and upwelling intensity from a regional climate model to forecast changes in the population growth rate of the auklet population at the important Farallon Island colony in central California. Our study projected that the auklet population growth rate will experience an absolute decline of 11–45% by the end of the century, placing this population on a trajectory toward extinction. In addition, future changes in upwelling intensity and timing of peak upwelling are likely to vary across auklet foraging regions in the California Current Ecosystem (CCE), producing a mosaic of climate conditions and ecological impacts across the auklet range. Overall, the Farallon Island Cassin's auklet population has been declining during recent decades, and ocean climate change in this century under a mid‐level emissions scenario is projected to accelerate this decline, leading toward population extinction. Because our study species has proven to be a sensitive indicator of oceanographic conditions in the CCE and a powerful predictor of the abundance of other important predators (i.e. salmon), the significant impacts we predicted for the Cassin's auklet provide insights into the consequences that ocean climate change may have for other plankton predators in this system.     

How will global climate change affect parasite–host assemblages?

Parasites are integral components of the biosphere. Host switching correlated with events of episodic climate change is ubiquitous in evolutionary and ecological time. Global climate change produces ecological perturbations, which cause geographical and phenological shifts, and alteration in the dynamics of parasite transmission, increasing the potential for host switching. The intersection of climate change with evolutionary conservative aspects of host specificity and transmission dynamics, called ecological fitting, permits emergence of parasites and diseases without evolutionary changes in their capacity for host utilization.     

Mismatch managed? Phenological phase extension as a strategy to manage phenological asynchrony in plant–animal mutualisms

Species‐specific shifts in phenology (timing of periodic life cycle events) are occurring with climate change and are already disrupting interactions within and among trophic levels. Phenological phase duration (e.g. beginning to end of flowering) and complementarity (patterns of nonoverlap), and their responses to changing conditions, will be important determinants of species' adaptive capacity to these shifts. Evidence indicates that extension of phenological duration of mutualistic partners could buffer negative impacts that occur with phenological shifts. Therefore, we suggest that techniques to extend the length of phenological duration will contribute to management of systems experiencing phenological asynchrony. Techniques of phenological phase extension discussed include the role of abiotic heterogeneity, genetic and species diversity, and alteration of population timing. We explore these approaches with the goal of creating a framework to build adaptive capacity and address phenological asynchrony in plant–animal mutualisms under climate change.     

Marine biological shifts and climate

Phenological, biogeographic and community shifts are among the reported responses of marine ecosystems and their species to climate change. However, despite both the profound consequences for ecosystem functioning and services, our understanding of the root causes underlying these biological changes remains rudimentary. Here, we show that a significant proportion of the responses of species and communities to climate change are deterministic at some emergent spatio-temporal scales, enabling testable predictions and more accurate projections of future changes. We propose a theory based on the concept of the ecological niche to connect phenological, biogeographic and long-term community shifts. The theory explains approximately 70% of the phenological and biogeographic shifts of a key zooplankton Calanus finmarchicus in the North Atlantic and approximately 56% of the long-term shifts in copepods observed in the North Sea during the period 1958–2009.     

Toward a synthetic understanding of the role of phenology in ecology and evolution

Phenology affects nearly all aspects of ecology and evolution. Virtually all biological phenomena—from individual physiology to interspecific relationships to global nutrient fluxes—have annual cycles and are influenced by the timing of abiotic events. Recent years have seen a surge of interest in this topic, as an increasing number of studies document phenological responses to climate change. Much recent research has addressed the genetic controls on phenology, modelling techniques and ecosystem-level and evolutionary consequences of phenological change. To date, however, these efforts have tended to proceed independently. Here, we bring together some of these disparate lines of inquiry to clarify vocabulary, facilitate comparisons among habitat types and promote the integration of ideas and methodologies across different disciplines and scales. We discuss the relationship between phenology and life history, the distinction between organismal- and population-level perspectives on phenology and the influence of phenology on evolutionary processes, communities and ecosystems. Future work should focus on linking ecological and physiological aspects of phenology, understanding the demographic effects of phenological change and explicitly accounting for seasonality and phenology in forecasts of ecological and evolutionary responses to climate change.     

Long‐term changes in autumn migration dates at the Strait of Gibraltar reflect population trends of soaring birds

A growing body of work shows that climate change is the cause of a number of directional shifts in the spring phenology of migratory birds. However, changes in autumn phenology are well studied and their consistency across species, as well as their link with population trends, remains uncertain. We investigate changes in the autumn migration dates of 11 species of soaring birds over the Strait of Gibraltar over a 16‐year period. Using models corrected for phylogeny, we assessed whether ecological and morphological characteristics, as well as population trends, account for interspecific shifts in migration times. We recorded different phenological changes in different periods of the migration season and suggest that these differences are due to age‐dependent responses. The variable best predicting advances in migration dates was population trend: species that did not advance their autumn migration dates were those showing a decline in their European breeding populations. We repeated our tests on a dataset representing the migration date of soaring birds across the Pyrenees Mountains and found that population trends at this site also predicted phenological shifts. Our results suggest that flexibility in migratory strategy and population trends may be related, such that different adaptive capacity in migration timing may be more relevant than other ecological traits in determining the conservation status of migratory birds in Europe and perhaps other regions.     

Game theory sheds new light on ecological responses to current climate change when phenology is historically mismatched

Phenological changes are well documented biological effects of current climate change but their adaptive value and demographic consequences are poorly known. Game theoretical models have shown that deviating from the fitness-maximising phenology can be evolutionary stable under frequency-dependent selection. We study eco-evolutionary responses to climate change when the historical phenology is mismatched in this way. For illustration we model adaptation of arrival dates in migratory birds that compete for territories at their breeding grounds. We simulate climate change by shifting the timing and the length of the favourable season for breeding. We show that initial trends in changes of population densities can be either reinforced or counteracted during the ensuing evolutionary adaptation. We find in total seven qualitatively different population trajectories during the transition to a new evolutionary equilibrium. This surprising diversity of eco-evolutionary responses provides adaptive explanations to the observed variation in phenological responses to recent climate change.     

The importance of phylogeny to the study of phenological response to global climate change

Climate change has resulted in major changes in the phenology—i.e. the timing of seasonal activities, such as flowering and bird migration—of some species but not others. These differential responses have been shown to result in ecological mismatches that can have negative fitness consequences. However, the ways in which climate change has shaped changes in biodiversity within and across communities are not well understood. Here, we build on our previous results that established a link between plant species'' phenological response to climate change and a phylogenetic bias in species'' decline in the eastern United States. We extend a similar approach to plant and bird communities in the United States and the UK that further demonstrates that climate change has differentially impacted species based on their phylogenetic relatedness and shared phenological responses. In plants, phenological responses to climate change are often shared among closely related species (i.e. clades), even between geographically disjunct communities. And in some cases, this has resulted in a phylogenetically biased pattern of non-native species success. In birds, the pattern of decline is phylogenetically biased but is not solely explained by phenological response, which suggests that other traits may better explain this pattern. These results illustrate the ways in which phylogenetic thinking can aid in making generalizations of practical importance and enhance efforts to predict species'' responses to future climate change.     

Global warming and the disruption of plant-pollinator interactions

Anthropogenic climate change is widely expected to drive species extinct by hampering individual survival and reproduction, by reducing the amount and accessibility of suitable habitat, or by eliminating other organisms that are essential to the species in question. Less well appreciated is the likelihood that climate change will directly disrupt or eliminate mutually beneficial (mutualistic) ecological interactions between species even before extinctions occur. We explored the potential disruption of a ubiquitous mutualistic interaction of terrestrial habitats, that between plants and their animal pollinators, via climate change. We used a highly resolved empirical network of interactions between 1420 pollinator and 429 plant species to simulate consequences of the phenological shifts that can be expected with a doubling of atmospheric CO₂. Depending on model assumptions, phenological shifts reduced the floral resources available to 17–50% of all pollinator species, causing as much as half of the ancestral activity period of the animals to fall at times when no food plants were available. Reduced overlap between plants and pollinators also decreased diet breadth of the pollinators. The predicted result of these disruptions is the extinction of pollinators, plants and their crucial interactions.     

Disentangling climate change effects on species interactions: effects of temperature, phenological shifts, and body size

Climate-mediated shifts in species’ phenologies are expected to alter species interactions, but predicting the consequences of this is difficult because phenological shifts may be driven by different climate factors that may or may not be correlated. Temperature could be an important factor determining effects of phenological shifts by altering species’ growth rates and thereby the relative size ratios of interacting species. We tested this hypothesis by independently manipulating temperature and the relative hatching phenologies of two competing amphibian species. Relative shifts in hatching time generally altered the strength of competition, but the presence and magnitude of this effect was temperature dependent and joint effects of temperature and hatching phenology were non-additive. Species that hatched relatively early or late performed significantly better or worse, respectively, but only at higher temperatures and not at lower temperatures. As a consequence, climate-mediated shifts in hatching phenology or temperature resulted in stronger or weaker effects than expected when both factors acted in concert. Furthermore, consequences of phenological shifts were asymmetric; arriving relatively early had disproportional stronger (or weaker) effects than arriving relatively late, and this varied with species identity. However, consistent with recent theory, these seemingly idiosyncratic effects of phenological shifts could be explained by species-specific differences in growth rates across temperatures and concordant shifts in relative body size of interacting species. Our results emphasize the need to account for environmental conditions when predicting the effects of phenological shifts, and suggest that shifts in size-structured interactions can mediate the impact of climate change on natural communities.     

Modeling plant diseases under climate change: evolutionary perspectives

Infectious plant diseases are a major threat to global agricultural productivity, economic development, and ecological integrity. There is widespread concern that these social and natural disasters caused by infectious plant diseases may escalate with climate change and computer modeling offers a unique opportunity to address this concern. Here, we analyze the intrinsic problems associated with current modeling strategies and highlight the need to integrate evolutionary principles into polytrophic, eco-evolutionary frameworks to improve predictions. We particularly discuss how evolutionary shifts in functional trade-offs, relative adaptability between plants and pathogens, ecosystems, and climate preferences induced by climate change may feedback to future plant disease epidemics and how technological advances can facilitate the generation and integration of this relevant knowledge for better modeling predictions.     

Forecasting phenology: from species variability to community patterns

Shifts in species' phenology in response to climate change have wide-ranging consequences for ecological systems. However, significant variability in species' responses, together with limited data, frustrates efforts to forecast the consequences of ongoing phenological changes. Herein, we use a case study of three North American plant communities to explore the implications of variability across levels of organisation (within and among species, and among communities) for forecasting responses to climate change. We show how despite significant variation among species in sensitivities to climate, comparable patterns emerge at the community level once regional climate drivers are accounted for. However, communities differ with respect to projected patterns of divergence and overlap among their species' phenological distributions in response to climate change. These analyses and a review of hypotheses suggest how explicit consideration of spatial scale and levels of biological organisation may help to understand and forecast phenological responses to climate change.     

Phenological overlap of interacting species in a changing climate: an assessment of available approaches

Concern regarding the biological effects of climate change has led to a recent surge in research to understand the consequences of phenological change for species interactions. This rapidly expanding research program is centered on three lines of inquiry: (1) how the phenological overlap of interacting species is changing, (2) why the phenological overlap of interacting species is changing, and (3) how the phenological overlap of interacting species will change under future climate scenarios. We synthesize the widely disparate approaches currently being used to investigate these questions: (1) interpretation of long‐term phenological data, (2) field observations, (3) experimental manipulations, (4) simulations and nonmechanistic models, and (5) mechanistic models. We present a conceptual framework for selecting approaches that are best matched to the question of interest. We weigh the merits and limitations of each approach, survey the recent literature from diverse systems to quantify their use, and characterize the types of interactions being studied by each of them. We highlight the value of combining approaches and the importance of long‐term data for establishing a baseline of phenological synchrony. Future work that scales up from pairwise species interactions to communities and ecosystems, emphasizing the use of predictive approaches, will be particularly valuable for reaching a broader understanding of the complex effects of climate change on the phenological overlap of interacting species. It will also be important to study a broader range of interactions: to date, most of the research on climate‐induced phenological shifts has focused on terrestrial pairwise resource–consumer interactions, especially those between plants and insects.