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

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

Environmental Dependence of Thermal Reaction Norms: Host Plant Quality Can Reverse the Temperature‐Size Rule

Abstract: The temperaturesize rule, a form of phenotypic plasticity in which decreased temperature increases final size, is one of the most widespread patterns in biology, particularly for ectotherms. Identifying the environmental conditions in which this pattern is reversed is key to understanding the generality of the rule. We use wild and domesticated populations of the tobacco hornworm Manduca sexta and the natural host plants of this species to explore the consequences of resource quality for the temperaturesize rule. Manduca sexta reared on a highquality host, tobacco (Nicotiana tabacum), followed the temperaturesize rule, with larger final sizes at lower temperatures. In contrast, M. sexta reared on a lowquality host, devils claw (Proboscidea louisianica), showed the reverse response. Wild and domesticated M. sexta exhibited qualitatively similar responses. Survival, growth and development rates, fecundity, and final size decreased with decreasing temperature in M. sexta reared on devils claw. We propose that the reversal of the temperaturesize rule results from the stressful combination of low temperatures and low dietary quality. Such reversals may impact seasonal and geographic patterns of host use in Manduca and other systems. Our results suggest that the temperaturesize rule occurs for a restricted range of nonstressful environmental conditions, limiting the robustness of this widespread pattern of phenotypic plasticity

Morphological and physiological determinants of local adaptation to climate in Rocky Mountain butterflies

Flight is a central determinant of fitness in butterflies and other insects, but it is restricted to a limited range of body temperatures. To achieve these body temperatures, butterflies use a combination of morphological, behavioural and physiological mechanisms. Here, we used common garden (without direct solar radiation) and reciprocal transplant (full solar radiation) experiments in the field to determine the thermal sensitivity of flight initiation for two species of Colias butterflies along an elevation gradient in the southwestern Rocky Mountains. The mean body temperature for flight initiation in the field was lower (24–26°C) than indicated by previous studies (28–30°C) in these species. There were small but significant differences in thermal sensitivity of flight initiation between species; high-elevation Colias meadii initiated flight at a lower mean body temperature than lower-elevation Colias eriphyle. Morphological differences (in wing melanin and thoracic setae) drive body temperature differences between species and contributed strongly to differences in the time and probability of flight and air temperatures at flight initiation. Our results suggest that differences both in thermal sensitivity (15% contribution) and in morphology (85% contribution) contribute to the differences in flight initiation between the two species in the field. Understanding these differences, which influence flight performance and fitness, aids in forecasting responses to climate change