Quantifying thermal extremes and biological variation to predict evolutionary responses to changing climate

Central ideas from thermal biology, including thermal performance curves and tolerances, have been widely used to evaluate how changes in environmental means and variances generate changes in fitness, selection and microevolution in response to climate change. We summarize the opportunities and challenges for extending this approach to understanding the consequences of extreme climatic events. Using statistical tools from extreme value theory, we show how distributions of thermal extremes vary with latitude, time scale and climate change. Second, we review how performance curves and tolerances have been used to predict the fitness and evolutionary responses to climate change and climate gradients. Performance curves and tolerances change with prior thermal history and with time scale, complicating their use for predicting responses to thermal extremes. Third, we describe several recent case studies showing how infrequent extreme events can have outsized effects on the evolution of performance curves and heat tolerance. A key issue is whether thermal extremes affect reproduction or survival, and how these combine to determine overall fitness. We argue that a greater focus on tails-in the distribution of environmental extremes, and in the upper ends of performance curves-is needed to understand the consequences of extreme events.This article is part of the themed issue 'Behavioural, ecological and evolutionary responses to extreme climatic events'

The Well‐Temperatured Biologist: (American Society of Naturalists Presidential Address)

Abstract: Temperature provides a powerful theme for exploring environmental adaptation at all levels of biological organization, from molecular kinetics to organismal fitness to global biogeography. First, the thermodynamic properties that underlie biochemical kinetics and protein stability determine the overall thermal sensitivity of rate processes. Consequently, a single quantitative framework can assess variation in thermal sensitivity of ectotherms in terms of single amino acid substitutions, quantitative genetics, and interspecific differences. Thermodynamic considerations predict that higher optimal temperatures will result in greater maximal fitness at the optimum, a pattern seen both in interspecific comparisons and in withinpopulation genotypic variation. Second, the temperaturesize rule (increased developmental temperature causes decreased adult body size) is a common pattern of phenotypic plasticity in ectotherms. Mechanistic models can correctly predict the rule in some taxa, but lab and field studies show that rapid evolution can weaken or even break the rule. Third, phenotypic and evolutionary models for thermal sensitivity can be combined to explore potential fitness consequences of climate warming for terrestrial ectotherms. Recent analyses suggest that climate change will have greater negative fitness consequences for tropical than for temperate ectotherms, because many tropical species have relatively narrow thermal breadths and smaller thermal safety margins

Historical changes in thermoregulatory traits of alpine butterflies reveal complex ecological and evolutionary responses to recent climate change

Abstract Background Trait evolution and plasticity are expected to interactively influence responses to climate change, but rapid changes in and increased variability of temperature may limit evolutionary responses. We use historical specimens to document changes in the size and thermoregulatory traits of a montane butterfly, Colias meadii, in Colorado, USA over the past 60 years (1953–2012). We quantify forewing wing length, ventral wing melanin that increases solar absorption, and the length of thorax setae that reduces convective heat loss. Results The mean of all three traits has increased during this time period despite climate warming. Phenological shifts may have extended the active season earlier at low elevations and later at high elevations, increasing exposure to cool temperatures and selecting for increases in thermoregulatory traits. Fitness increases at higher elevations due to warming could also increase thermoregulatory traits. Warmer temperatures during pupal development and later flight dates in the season are associated with decreased wing melanin, indicating a role of phenotypic plasticity in historical trait changes. Conclusions Phenotypic shifts result from a complex interplay of ecological and evolutionary responses to climate change. Environmental variability within and across seasons can limit the evolutionary responses of populations to increasing mean temperatures during climate change

Hotter Is Better and Broader: Thermal Sensitivity of Fitness in a Population of Bacteriophages

Hotter is better is a hypothesis of thermal adaptation that posits that the rate-depressing effects of low temperature on biochemical reactions cannot be overcome by physiological plasticity or genetic adaptation. If so, then genotypes or populations adapted to warmer temperatures will have higher maximum growth rates than those adapted to low temperatures. Here we test hotter is better by measuring thermal reaction norms for intrinsic rate of population growth among an intraspecific collection of bacteriophages recently isolated from nature. Consistent with hotter is better, we find that phage genotypes with higher optimal temperatures have higher maximum growth rates. Unexpectedly, we also found that hotter is broader, meaning that the phages with the highest optimal temperatures also have the greatest temperature ranges. We found that the temperature sensitivity of fitness for phages is similar to that for insects

Variation in Continuous Reaction Norms: Quantifying Directions of Biological Interest

Abstract: Thermal performance curves are an example of continuous reaction norm curves of common shape. Three modes of variation in these curvesvertical shift, horizontal shift, and generalistspecialist tradeoffsare of special interest to evolutionary biologists. Since two of these modes are nonlinear, traditional methods such as principal components analysis fail to decompose the variation into biological modes and to quantify the variation associated with each mode. Here we present the results of a new method, template mode of variation (TMV), that decomposes the variation into predetermined modes of variation for a particular set of thermal performance curves. We illustrate the method using data on thermal sensitivity of growth rate in Pieris rapae caterpillars. The TMV model explains 67% of the variation in thermal performance curves among families; generalistspecialist tradeoffs account for 38% of the total betweenfamily variation. The TMV method implemented here is applicable to both differences in mean and patterns of variation, and it can be used with either phenotypic or quantitative genetic data for thermal performance curves or other continuous reaction norms that have a template shape with a single maximum. The TMV approach may also apply to growth trajectories, agespecific lifehistory traits, and other functionvalued traits

Evolutionary Divergence in Thermal Sensitivity and Diapause of Field and Laboratory Populations of Manduca sexta

The tobacco hornworm Manduca sexta has been an important model system in insect biology for more than half a century. Here we report the evolutionary divergence in thermal sensitivity and diapause initiation between field and laboratory populations that were separated for more than 35 yr (>240 laboratory generations) and that are descendants from the same field populations in central North Carolina. At intermediate rearing temperatures (20 degrees-25 degrees C), mean body size was significantly larger and development time significantly faster in the laboratory than in the field populations. At higher temperatures (30 degrees -35 degrees C), these mean differences between populations were reduced or eliminated, and larval survival at 35 degrees C was significantly lower in the laboratory population than in the field population. F(1) crosses had survival and development time to wandering similar to the field population times at both 25 degrees and 35 degrees C; body mass at wandering for F(1) crosses was intermediate compared with that of the field and laboratory populations. Comparisons with earlier field and laboratory studies suggest evolutionary reductions in thermal tolerance and performance at high temperatures in the laboratory population. The critical photoperiod initiating diapause in field populations in North Carolina did not change detectably between the 1960s and 2005. In contrast, the laboratory population has evolved a reduced tendency to diapause under short-day conditions, relative to the field population

Host plant quality, selection history and trade-offs shape immune responses ofManduca sexta.

Immune defences are an important component of fitness. Yet susceptibility to pathogens is common, suggesting the presence of ecological and evolutionary limitations on immune defences. Here, we use structural equation modelling to quantify the direct effects of resource quality and selection history, and their indirect effects mediated via body condition prior to an immune challenge on encapsulation and melanization immune defences in the tobacco hornworm, Manduca sexta. We also investigate allocation trade-offs among immune defences and growth rate following an immune challenge. We found considerable variation in the magnitude and direction of the direct effects of resource quality and selection history on immune defences and their indirect effects mediated via body condition and allocation trade-offs. Greater resource quality and evolutionary exposure to pathogens had positive direct effects on encapsulation and melanization. The indirect effect of resource quality on encapsulation mediated via body condition was substantial, whereas indirect effects on melanization were negligible. Individuals in better condition prior to the immune challenge had greater encapsulation; however, following the immune challenge, greater encapsulation traded off with slower growth rate. Our study demonstrates the importance of experimentally and analytically disentangling the relative contributions of direct and indirect effects to understand variation in immune defences

Erroneous Arrhenius: Modified Arrhenius Model Best Explains the Temperature Dependence of Ectotherm Fitness

The initial rise of fitness that occurs with increasing temperature is attributed to Arrhenius kinetics, in which rates of reaction increase exponentially with increasing temperature. Models based on Arrhenius typically assume single rate-limiting reaction(s) over some physiological temperature range for which all the rate-limiting enzymes are in 100% active conformation. We test this assumption using datasets for microbes that have measurements of fitness (intrinsic rate of population growth) at many temperatures and over a broad temperature range, and for diverse ectotherms that have measurements at fewer temperatures. When measurements are available at many temperatures, strictly Arrhenius kinetics is rejected over the physiological temperature range. However, over a narrower temperature range, we cannot reject strictly Arrhenius kinetics. The temperature range also affects estimates of the temperature dependence of fitness. These results indicate that Arrhenius kinetics only apply over a narrow range of temperatures for ectotherms, complicating attempts to identify general patterns of temperature dependence

Host plant quality, selection history and trade-offs shape immune responses ofManduca sexta.

Immune defences are an important component of fitness. Yet susceptibility to pathogens is common, suggesting the presence of ecological and evolutionary limitations on immune defences. Here, we use structural equation modelling to quantify the direct effects of resource quality and selection history, and their indirect effects mediated via body condition prior to an immune challenge on encapsulation and melanization immune defences in the tobacco hornworm, Manduca sexta. We also investigate allocation trade-offs among immune defences and growth rate following an immune challenge. We found considerable variation in the magnitude and direction of the direct effects of resource quality and selection history on immune defences and their indirect effects mediated via body condition and allocation trade-offs. Greater resource quality and evolutionary exposure to pathogens had positive direct effects on encapsulation and melanization. The indirect effect of resource quality on encapsulation mediated via body condition was substantial, whereas indirect effects on melanization were negligible. Individuals in better condition prior to the immune challenge had greater encapsulation; however, following the immune challenge, greater encapsulation traded off with slower growth rate. Our study demonstrates the importance of experimentally and analytically disentangling the relative contributions of direct and indirect effects to understand variation in immune defences

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