Temperature Sensitivity of Fitness Components across Life Cycles Drives Insect Responses to Climate Change.

AbstractThermal performance curves (TPCs) are increasingly used as a convenient approach to predict climate change impacts on ectotherms that accounts for organismal thermal sensitivity; however, directly applying TPCs to temperature data to estimate fitness has yielded contrasting predictions depending on assumptions regarding climate variability. We compare direct application of TPCs to an approach integrating TPCs for different fitness components (e.g., per capita birth rate, adult life span) across ectotherm life cycles into a population dynamic model, which we independently validated with census data and applied to hemipteran insect populations across latitude. The population model predicted that climate change will reduce insect fitness more at higher latitudes due to its effects on survival but will reduce net reproductive rate more at lower latitudes due to its effects on fecundity. Directly applying TPCs underestimated climate change impacts on fitness relative to incorporating the TPCs into the population model due to simplifying survival dynamics across the life cycle. The population model predicted that climate change will reduce mean insect density and increase population variability at higher latitudes via reduced survival, despite faster development and a longer activity period. Our study highlights the importance of considering how multiple fitness components respond to climate variability across the life cycle to better understand and anticipate the ecological consequence of climate change.

Mechanistic forecasts of species responses to climate change: The promise of biophysical ecology.

A core challenge in global change biology is to predict how species will respond to future environmental change and to manage these responses. To make such predictions and management actions robust to novel futures, we need to accurately characterize how organisms experience their environments and the biological mechanisms by which they respond. All organisms are thermodynamically connected to their environments through the exchange of heat and water at fine spatial and temporal scales and this exchange can be captured with biophysical models. Although mechanistic models based on biophysical ecology have a long history of development and application, their use in global change biology remains limited despite their enormous promise and increasingly accessible software. We contend that greater understanding and training in the theory and methods of biophysical ecology is vital to expand their application. Our review shows how biophysical models can be implemented to understand and predict climate change impacts on species' behavior, phenology, survival, distribution, and abundance. It also illustrates the types of outputs that can be generated, and the data inputs required for different implementations. Examples range from simple calculations of body temperature at a particular site and time, to more complex analyses of species' distribution limits based on projected energy and water balances, accounting for behavior and phenology. We outline challenges that currently limit the widespread application of biophysical models relating to data availability, training, and the lack of common software ecosystems. We also discuss progress and future developments that could allow these models to be applied to many species across large spatial extents and timeframes. Finally, we highlight how biophysical models are uniquely suited to solve global change biology problems that involve predicting and interpreting responses to environmental variability and extremes, multiple or shifting constraints, and novel abiotic or biotic environments.

Shifts in the relative fitness contributions of fecundity and survival in variable and changing environments.

Organisms respond to shifts in climate means and variability via distinct mechanisms. Accounting for these differential responses and appropriately aggregating them is central to understanding and predicting responses to climate variability and change. Separately considering fitness components can clarify organismal responses: fecundity is primarily an integrated, additive response to chronic environmental conditions over time via mechanisms such as energy use and acquisition, whereas survival can be strongly influenced by short-term, extreme environmental conditions. In many systems, the relative importance of fecundity and survival constraints changes systematically along climate gradients, with fecundity constraints dominating at high latitudes or altitudes (i.e. leading range edges as climate warms), and survival constraints dominating at trailing range edges. Incorporating these systematic differences in models may improve predictions of responses to recent climate change over models that assume similar processes along environmental gradients. We explore how detecting and predicting shifts in fitness constraints can improve our ability to forecast responses to climate gradients and change.

Grasshopper species' seasonal timing underlies shifts in phenological overlap in response to climate gradients, variability and change.

Species with different life histories and communities that vary in their seasonal constraints tend to shift their phenology (seasonal timing) differentially in response to climate warming. We investigate how these variable phenological shifts aggregate to influence phenological overlap within communities. Phenological advancements of later season species and extended durations of early season species may increase phenological overlap, with implications for species' interactions such as resource competition. We leverage extensive historic (1958-1960) and recent (2006-2015) weekly survey data for communities of grasshoppers along a montane elevation gradient to assess the impact of climate on shifts in the phenology and abundance distributions of species. We then examine how these responses are influenced by the seasonal timing of species and elevation, and how in aggregate they influence degrees of phenological overlap within communities. In warmer years, abundance distributions shift earlier in the season and become broader. Total abundance responds variably among species and we do not detect a significant response across species. Shifts in abundance distributions are not strongly shaped by species' seasonal timing or sites of variable elevations. The area of phenological overlap increases in warmer years due to shifts in the relative seasonal timing of compared species. Species that overwinter as nymphs increasingly overlap with later season species that advance their phenology. The days of phenological overlap also increase in warm years but the response varies across sites of variable elevation. Our phenological overlap metric based on comparing single events-the dates of peak abundance-does not shift significantly with warming. Phenological shifts are more complex than shifts in single dates such as first occurrence. As abundance distributions shift earlier and become broader in warm years, phenological overlap increases. Our analysis suggests that overall grasshopper abundance is relatively robust to climate and associated phenological shifts but we find that increased overlap can decrease abundance, potentially by strengthening species interactions such as resource competition.

Geographical limits to species-range shifts are suggested by climate velocity.

The reorganization of patterns of species diversity driven by anthropogenic climate change, and the consequences for humans, are not yet fully understood or appreciated. Nevertheless, changes in climate conditions are useful for predicting shifts in species distributions at global and local scales. Here we use the velocity of climate change to derive spatial trajectories for climatic niches from 1960 to 2009 (ref. 7) and from 2006 to 2100, and use the properties of these trajectories to infer changes in species distributions. Coastlines act as barriers and locally cooler areas act as attractors for trajectories, creating source and sink areas for local climatic conditions. Climate source areas indicate where locally novel conditions are not connected to areas where similar climates previously occurred, and are thereby inaccessible to climate migrants tracking isotherms: 16% of global surface area for 1960 to 2009, and 34% of ocean for the 'business as usual' climate scenario (representative concentration pathway (RCP) 8.5) representing continued use of fossil fuels without mitigation. Climate sink areas are where climate conditions locally disappear, potentially blocking the movement of climate migrants. Sink areas comprise 1.0% of ocean area and 3.6% of land and are prevalent on coasts and high ground. Using this approach to infer shifts in species distributions gives global and regional maps of the expected direction and rate of shifts of climate migrants, and suggests areas of potential loss of species richness.

Evolution of plasticity and adaptive responses to climate change along climate gradients.

The relative contributions of phenotypic plasticity and adaptive evolution to the responses of species to recent and future climate change are poorly understood. We combine recent (1960-2010) climate and phenotypic data with microclimate, heat balance, demographic and evolutionary models to address this issue for a montane butterfly, Colias eriphyle, along an elevational gradient. Our focal phenotype, wing solar absorptivity, responds plastically to developmental (pupal) temperatures and plays a central role in thermoregulatory adaptation in adults. Here, we show that both the phenotypic and adaptive consequences of plasticity vary with elevation. Seasonal changes in weather generate seasonal variation in phenotypic selection on mean and plasticity of absorptivity, especially at lower elevations. In response to climate change in the past 60 years, our models predict evolutionary declines in mean absorptivity (but little change in plasticity) at high elevations, and evolutionary increases in plasticity (but little change in mean) at low elevation. The importance of plasticity depends on the magnitude of seasonal variation in climate relative to interannual variation. Our results suggest that selection and evolution of both trait means and plasticity can contribute to adaptive response to climate change in this system. They also illustrate how plasticity can facilitate rather than retard adaptive evolutionary responses to directional climate change in seasonal environments.

Diminishing returns limit energetic costs of climate change.

Changes in the time available for organisms to maintain physiologically preferred temperatures (thermal opportunity) is a primary mechanism by which climate change impacts the fitness and population dynamics of organisms. Yet, it is unclear whether losses or gains in thermal opportunity result in proportional changes in rates of energy procurement and use. We experimentally quantified lizard food consumption and energy assimilation at different durations of thermal opportunity. We incorporated these data in an individual-based model of foraging and digestion in lizards to explore the implications of nonlinear responses to shifts in thermal opportunity across a wide geographic range. Our model predicts that shifts in thermal opportunities resulting from climate change alter energy intake primarily through digestion rather than feeding, because simulated lizards were able to fill their gut faster than they can digest their food. Moreover, since rates of energy assimilation decelerate with increasing thermal opportunity, shifts in daily energetic assimilation would depend on the previous opportunity for thermoregulation. In particular, the same changes in thermal opportunity will have little impact on lizards from warm locations, while having a large impact on lizards from cold locations where thermoregulation is possible for only a few hours each day. Energy expenditure followed spatial patterns in thermal opportunity, with greater annual energy expenditure occurring at warmer locations. Our model predicts that lizards will spend more energy under climate change by maintaining higher body temperatures and remaining active longer. However, the predicted changes in energy assimilation following climate change greatly exceeded the predicted increases in energy expenditure. Simple models, which assume constant rates of energy gain during activity, will potentially mislead efforts to understand and predict the biological impacts of climate change.

Lizards fail to plastically adjust nesting behavior or thermal tolerance as needed to buffer populations from climate warming.

Although observations suggest the potential for phenotypic plasticity to allow adaptive responses to climate change, few experiments have assessed that potential. Modeling suggests that Sceloporus tristichus lizards will need increased nest depth, shade cover, or embryonic thermal tolerance to avoid reproductive failure resulting from climate change. To test for such plasticity, we experimentally examined how maternal temperatures affect nesting behavior and embryonic thermal sensitivity. The temperature regime that females experienced while gravid did not affect nesting behavior, but warmer temperatures at the time of nesting reduced nest depth. Additionally, embryos from heat-stressed mothers displayed increased sensitivity to high-temperature exposure. Simulations suggest that critically low temperatures, rather than high temperatures, historically limit development of our study population. Thus, the plasticity needed to buffer this population has not been under selection. Plasticity will likely fail to compensate for ongoing climate change when such change results in novel stressors.

Ontogeny constrains phenology: opportunities for activity and reproduction interact to dictate potential phenologies in a changing climate.

As global warming has lengthened the active seasons of many species, we need a framework for predicting how advances in phenology shape the life history and the resulting fitness of organisms. Using an individual-based model, we show how warming differently affects annual cycles of development, growth, reproduction and activity in a group of North American lizards. Populations in cold regions can grow and reproduce more when warming lengthens their active season. However, future warming of currently warm regions advances the reproductive season but reduces the survival of embryos and juveniles. Hence, stressful temperatures during summer can offset predicted gains from extended growth seasons and select for lizards that reproduce after the warm summer months. Understanding these cascading effects of climate change may be crucial to predict shifts in the life history and demography of species.

Temperature extremes: geographic patterns, recent changes, and implications for organismal vulnerabilities.

Extreme temperatures can injure or kill organisms and can drive evolutionary patterns. Many indices of extremes have been proposed, but few attempts have been made to establish geographic patterns of extremes and to evaluate whether they align with geographic patterns in biological vulnerability and diversity. To examine these issues, we adopt the CLIMDEX indices of thermal extremes. We compute scores for each index on a geographic grid during a baseline period (1961-1990) and separately for the recent period (1991-2010). Heat extremes (temperatures above the 90th percentile during the baseline period) have become substantially more common during the recent period, particularly in the tropics. Importantly, the various indices show weak geographic concordance, implying that organisms in different regions will face different forms of thermal stress. The magnitude of recent shifts in indices is largely uncorrelated with baseline scores in those indices, suggesting that organisms are likely to face novel thermal stresses. Organismal tolerances correlate roughly with absolute metrics (mainly for cold), but poorly with metrics defined relative to local conditions. Regions with high extreme scores do not correlate closely with regions with high species diversity, human population density, or agricultural production. Even though frequency and intensity of extreme temperature events have - and are likely to have - major impacts on organisms, the impacts are likely to be geographically and taxonomically idiosyncratic and difficult to predict.

Ecological and methodological drivers of species' distribution and phenology responses to climate change.

Climate change is shifting species' distribution and phenology. Ecological traits, such as mobility or reproductive mode, explain variation in observed rates of shift for some taxa. However, estimates of relationships between traits and climate responses could be influenced by how responses are measured. We compiled a global data set of 651 published marine species' responses to climate change, from 47 papers on distribution shifts and 32 papers on phenology change. We assessed the relative importance of two classes of predictors of the rate of change, ecological traits of the responding taxa and methodological approaches for quantifying biological responses. Methodological differences explained 22% of the variation in range shifts, more than the 7.8% of the variation explained by ecological traits. For phenology change, methodological approaches accounted for 4% of the variation in measurements, whereas 8% of the variation was explained by ecological traits. Our ability to predict responses from traits was hindered by poor representation of species from the tropics, where temperature isotherms are moving most rapidly. Thus, the mean rate of distribution change may be underestimated by this and other global syntheses. Our analyses indicate that methodological approaches should be explicitly considered when designing, analysing and comparing results among studies. To improve climate impact studies, we recommend that (1) reanalyses of existing time series state how the existing data sets may limit the inferences about possible climate responses; (2) qualitative comparisons of species' responses across different studies be limited to studies with similar methodological approaches; (3) meta-analyses of climate responses include methodological attributes as covariates; and (4) that new time series be designed to include the detection of early warnings of change or ecologically relevant change. Greater consideration of methodological attributes will improve the accuracy of analyses that seek to quantify the role of climate change in species' distribution and phenology changes.

Geographic divergence in upper thermal limits across insect life stages: does behavior matter?

Insects with complex life cycles vary in size, mobility, and thermal ecology across life stages. We examine how differences in the capacity for thermoregulatory behavior influence geographic differences in physiological heat tolerance among egg and adult Colias butterflies. Colias adults exhibit differences in morphology (wing melanin and thoracic setal length) along spatial gradients, whereas eggs are morphologically indistinguishable. Here we compare Colias eriphyle eggs and adults from two elevations and Colias meadii from a high elevation. Hatching success and egg development time of C. eriphyle eggs did not differ significantly with the elevation of origin. Egg survival declined in response to heat-shock temperatures above 38-40 °C and egg development time was shortest at intermediate heat-shock temperatures of 33-38 °C. Laboratory experiments with adults showed survival in response to heat shock was significantly greater for Colias from higher than from lower elevation sites. Common-garden experiments at the low-elevation field site showed that C. meadii adults initiated heat-avoidance and over-heating behaviors significantly earlier in the day than C. eriphyle. Our study demonstrates the importance of examining thermal tolerances across life stages. Our findings are inconsistent with the hypothesis that thermoregulatory behavior inhibits the geographic divergence of physiological traits in mobile stages, and suggest that sessile stages may evolve similar heat tolerances in different environments due to microclimatic variability or evolutionary constraints.

Climate variability slows evolutionary responses of Colias butterflies to recent climate change.

How does recent climate warming and climate variability alter fitness, phenotypic selection and evolution in natural populations? We combine biophysical, demographic and evolutionary models with recent climate data to address this question for the subalpine and alpine butterfly, Colias meadii, in the southern Rocky Mountains. We focus on predicting patterns of selection and evolution for a key thermoregulatory trait, melanin (solar absorptivity) on the posterior ventral hindwings, which affects patterns of body temperature, flight activity, adult and egg survival, and reproductive success in Colias. Both mean annual summer temperatures and thermal variability within summers have increased during the past 60 years at subalpine and alpine sites. At the subalpine site, predicted directional selection on wing absorptivity has shifted from generally positive (favouring increased wing melanin) to generally negative during the past 60 years, but there is substantial variation among years in the predicted magnitude and direction of selection and the optimal absorptivity. The predicted magnitude of directional selection at the alpine site declined during the past 60 years and varies substantially among years, but selection has generally been positive at this site. Predicted evolutionary responses to mean climate warming at the subalpine site since 1980 is small, because of the variability in selection and asymmetry of the fitness function. At both sites, the predicted effects of adaptive evolution on mean population fitness are much smaller than the fluctuations in mean fitness due to climate variability among years. Our analyses suggest that variation in climate within and among years may strongly limit evolutionary responses of ectotherms to mean climate warming in these habitats.

Elevational differences in developmental plasticity determine phenological responses of grasshoppers to recent climate warming.

Annual species may increase reproduction by increasing adult body size through extended development, but risk being unable to complete development in seasonally limited environments. Synthetic reviews indicate that most, but not all, species have responded to recent climate warming by advancing the seasonal timing of adult emergence or reproduction. Here, we show that 50 years of climate change have delayed development in high-elevation, season-limited grasshopper populations, but advanced development in populations at lower elevations. Developmental delays are most pronounced for early-season species, which might benefit most from delaying development when released from seasonal time constraints. Rearing experiments confirm that population, elevation and temperature interact to determine development time. Population differences in developmental plasticity may account for variability in phenological shifts among adults. An integrated consideration of the full life cycle that considers local adaptation and plasticity may be essential for understanding and predicting responses to climate change.

Resolving the life cycle alters expected impacts of climate change.

Recent models predict contrasting impacts of climate change on tropical and temperate species, but these models ignore how environmental stress and organismal tolerance change during the life cycle. For example, geographical ranges and extinction risks have been inferred from thermal constraints on activity during the adult stage. Yet, most animals pass through a sessile embryonic stage before reaching adulthood, making them more susceptible to warming climates than current models would suggest. By projecting microclimates at high spatio-temporal resolution and measuring thermal tolerances of embryos, we developed a life cycle model of population dynamics for North American lizards. Our analyses show that previous models dramatically underestimate the demographic impacts of climate change. A predicted loss of fitness in 2% of the USA by 2100 became 35% when considering embryonic performance in response to hourly fluctuations in soil temperature. Most lethal events would have been overlooked if we had ignored thermal stress during embryonic development or had averaged temperatures over time. Therefore, accurate forecasts require detailed knowledge of environmental conditions and thermal tolerances throughout the life cycle.

Phenotypic clines, energy balances and ecological responses to climate change.

The Metabolic Theory of Ecology has renewed interest in using energetics to scale across levels of ecological organization. Can scaling from individual phenotypes to population dynamics provides insight into why species have shifted their phenologies, abundances and distributions idiosyncratically in response to recent climate change? We consider how the energetic implications of phenotypes may scale to understand population and species level responses to climate change using four focal grasshopper species along an elevation gradient in Colorado. We use a biophysical model to translate phenotypes and environmental conditions into estimates of body temperatures. We measure thermal tolerances and preferences and metabolic rates to assess rates of energy use and acquisition. Body mass declines along the elevation gradient for all species, but mass-specific metabolic rates increases only modestly. We find interspecific differences in both overall thermal tolerances and preferences and in the variation of these metrics along the elevation gradient. The more dispersive species exhibit significantly higher thermal tolerance and preference consistent with much of their range spanning hot, low elevation areas. When integrating these metrics to consider metabolic constraints, we find that energetic costs decrease along the elevation gradient due to decreasing body size and temperature. Opportunities for energy acquisition, as reflected by the proportion of time that falls within a grasshopper's thermal tolerance range, peak at mid elevations. We discuss methods for translating these energetic metrics into population dynamics. Quantifying energy balances and allocation offers a viable approach for predicting how populations will respond to climate change and the consequences for species composed of populations that may be locally adapted.

Interconnecting global threats: climate change, biodiversity loss, and infectious diseases.

The concurrent pressures of rising global temperatures, rates and incidence of species decline, and emergence of infectious diseases represent an unprecedented planetary crisis. Intergovernmental reports have drawn focus to the escalating climate and biodiversity crises and the connections between them, but interactions among all three pressures have been largely overlooked. Non-linearities and dampening and reinforcing interactions among pressures make considering interconnections essential to anticipating planetary challenges. In this Review, we define and exemplify the causal pathways that link the three global pressures of climate change, biodiversity loss, and infectious disease. A literature assessment and case studies show that the mechanisms between certain pairs of pressures are better understood than others and that the full triad of interactions is rarely considered. Although challenges to evaluating these interactions-including a mismatch in scales, data availability, and methods-are substantial, current approaches would benefit from expanding scientific cultures to embrace interdisciplinarity and from integrating animal, human, and environmental perspectives. Considering the full suite of connections would be transformative for planetary health by identifying potential for co-benefits and mutually beneficial scenarios, and highlighting where a narrow focus on solutions to one pressure might aggravate another.

Can terrestrial ectotherms escape the heat of climate change by moving?

Whether movement will enable organisms to alleviate thermal stress is central to the biodiversity implications of climate change. We use the temperature-dependence of ectotherm performance to investigate the fitness consequences of movement. Movement to an optimal location within a 50 km radius will only offset the fitness impacts of climate change by 2100 in 5 per cent of locations globally. Random movement carries an 87 per cent risk of further fitness detriment. Mountainous regions with high temperature seasonality (i.e. temperate areas) not only offer the greatest benefit from optimal movement but also the most severe fitness consequences if an organism moves to the wrong location. Doubling dispersal capacity would provide modest benefit exclusively to directed dispersers in topographically diverse areas. The benefits of movement for escaping climate change are particularly limited in the tropics, where fitness impacts will be most severe. The potential of movement to lessen climate change impacts may have been overestimated.

Conservatism of lizard thermal tolerances and body temperatures across evolutionary history and geography.

Species may exhibit similar thermal tolerances via either common ancestry or environmental filtering and local adaptation, if the species inhabit similar environments. We ask whether upper and lower thermal limits (critical thermal maxima and minima) and body temperatures are more strongly conserved across evolutionary history or geography for lizard populations distributed globally. We find that critical thermal maxima are highly conserved with location accounting for a higher proportion of the variation than phylogeny. Notably, thermal tolerance breadth is conserved across the phylogeny despite critical thermal minima showing little niche conservatism. Body temperatures observed during activity in the field show the greatest degree of conservatism, with phylogeny accounting for most of the variation. This suggests that propensities for thermoregulatory behaviour, which can buffer body temperatures from environmental variation, are similar within lineages. Phylogeny and geography constrain thermal tolerances similarly within continents, but variably within clades. Conservatism of thermal tolerances across lineages suggests that the potential for local adaptation to alleviate the impacts of climate change on lizards may be limited.

Fire-driven animal evolution in the Pyrocene.

Fire regimes are a major agent of evolution in terrestrial animals. Changing fire regimes and the capacity for rapid evolution in wild animal populations suggests the potential for rapid, fire-driven adaptive animal evolution in the Pyrocene. Fire drives multiple modes of evolutionary change, including stabilizing, directional, disruptive, and fluctuating selection, and can strongly influence gene flow and genetic drift. Ongoing and future research in fire-driven animal evolution will benefit from further development of generalizable hypotheses, studies conducted in highly responsive taxa, and linking fire-adapted phenotypes to their underlying genetic basis. A better understanding of evolutionary responses to fire has the potential to positively influence conservation strategies that embrace evolutionary resilience to fire in the Pyrocene.