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'

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

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

Plasticity of upper thermal limits to acute and chronic temperature variation in Manduca sexta larvae

ABSTRACT In many ectotherms, exposure to high temperatures can improve subsequent tolerance to higher temperatures. However, the differential effects of single, repeated or continuous exposure to high temperatures are less clear. We measured the effects of single heat shocks and of diurnally fluctuating or constant rearing temperatures on the critical thermal maximum (CTmax) for final instar larvae of Manduca sexta. Brief (2 h) heat shocks at temperatures of 35°C and above significantly increased CTmax relative to control temperatures (25°C). Increasing mean temperatures (from 25 to 30°C) or greater diurnal fluctuations (from constant to ±10°C) during larval development also significantly increased CTmax. Combining these data showed that repeated or continuous temperature exposure during development improved heat tolerance beyond the effects of a single exposure to the same maximum temperature. These results suggest that both acute and chronic temperature exposure can result in adaptive plasticity of upper thermal limits

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

How has the environment shaped geographical patterns of insect body sizes? A test of hypotheses using sphingid moths

Aim: We mapped the geographical pattern of body sizes in sphingid moths and investigated latitudinal clines. We tested hypotheses concerning their possible environmental control, that is, effects of temperature (negative: temperature size rule or Bergmann's rule; positive: converse Bergmann rule), food availability, robustness to starvation during extreme weather and seasonality. Location: Old World and Australia/Pacific region. Methods: Body size data of 950 sphingid species were compiled and related to their distribution maps. Focusing on body length, we mapped the median and maximum size of all species occurring in 100 km grid cells. In a comparative approach, we tested the predictions from explanatory hypotheses by correlating species' size to the average environmental conditions encountered throughout their range, under univariate and multivariate models. We accounted for phylogeny by stepwise inclusion of phylogenetically informed taxonomic classifications into hierarchical random‐intercept mixed models. Results: Median body sizes showed a distinctive geographical pattern, with large species in the Middle East and the Asian tropics, and smaller species in temperate regions and the Afrotropics. Absolute latitude explained very little body size variation, but there was a latitudinal cline of maximum size. Species' median size was correlated with net primary productivity, supporting the food availability hypothesis, whereas support for other hypotheses was weak. Environmental correlations contributed much less (i.e. <10%) to explaining overall size variation than phylogeny (inclusion of which led to models explaining >70% of variability). Main conclusion: The intuitive impression of larger species in the tropics is shaped by larger size maxima. Median body sizes are only very weakly related to latitude. Most of the geographical variation in body size in sphingid moths is explained by their phylogenetic past. NPP and forest cover correlate positively with the body size, which supports the idea that food availability allowed the evolution of larger sizes.The attached document is the author(’s’) final accepted/submitted version of the journal article. You are advised to consult the publisher’s version if you wish to cite from i

Variation in pre- and post-copulatory sexual selection on male genital size in two species of lygaeid bug

This study was funded by the Natural Environmental Research Council (DTG studentship 1109354 to LRD).Sexual selection has been shown to be the driving force behind the evolution of the sometimes extreme and elaborate genitalia of many species. Sexual selection may arise before and/or after mating, or vary according to other factors such as the social environment. However, bouts of selection are typically considered in isolation. We measured the strength and pattern of selection acting on the length of the male intromittent organ (or processus) in two closely related species of lygaeid seed bug: Lygaeus equestris and Lygaeus simulans. In both species, we measured both pre- and post-copulatory selection. For L. equestris, we also varied the experimental choice design used in mating trials. We found contrasting pre- and post-copulatory selection on processus length in L. equestris. Furthermore, significant pre-copulatory selection was only seen in mating trials in which two males were present. This selection likely arises indirectly due to selection on a correlated trait, as the processus does not interact with the female prior to copulation. In contrast, we were unable to detect significant pre- or post-copulatory selection on processus length in L. simulans. However, a formal meta-analysis of previous estimates of post-copulatory selection on processus length in L. simulans suggests that there is significant stabilising selection across studies, but the strength of selection varies between experiments. Our results emphasise that the strength and direction of sexual selection on genital traits may be multifaceted and can vary across studies, social contexts and different stages of reproduction.Publisher PDFPeer reviewe