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.

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.

Fluctuating temperatures and ectotherm growth: distinguishing non-linear and time-dependent effects.

Most terrestrial ectotherms experience diurnal and seasonal variation in temperature. Because thermal performance curves are non-linear, mean performance can differ in fluctuating and constant thermal environments. However, time-dependent effects--effects of the order and duration of exposure to temperature--can also influence mean performance. We quantified the non-linear and time-dependent effects of diurnally fluctuating temperatures for larval growth rates in the tobacco hornworm, Manduca sexta L., with four main results. First, the shape of the thermal performance curve for growth rate depended on the duration of exposure: for example, optimal temperature and thermal breadth were greater for growth rates measured over short (24 h during the last instar) compared with long (the entire period of larval growth) time periods. Second, larvae reared in diurnally fluctuating temperatures had significantly higher optimal temperatures and maximal growth rates than larvae reared in constant temperatures. Third, for larvae maintained at three mean temperatures (20, 25 and 30°C) and three diurnal temperature ranges (±0, ±5 and ±10°C), diurnal fluctuations had opposite effects on mean growth rates at low versus high mean temperature. Fourth, both short- and long-term thermal performance curves yielded poor predictions of the non-linear effects of fluctuating temperature on mean growth rates (compared with our experimental results) at higher mean temperatures. Our results suggest caution in using constant temperature studies to model the consequences of variable thermal environments.

Gene expression in closely related species mirrors local adaptation: consequences for responses to a warming world.

Local adaptation of populations could preclude or slow range expansions in response to changing climate, particularly when dispersal is limited. To investigate the differential responses of populations to changing climatic conditions, we exposed poleward peripheral and central populations of two Lepidoptera to reciprocal, common-garden climatic conditions and compared their whole-transcriptome expression. We found evidence of simple population differentiation in both species, and in the species with previously identified population structure and phenotypic local adaptation, we found several hundred genes that responded in a synchronized and localized fashion. These genes were primarily involved in energy metabolism and oxidative stress, and expression levels were most divergent between populations in the same environment in which we previously detected divergence for metabolism. We found no localized genes in the species with less population structure and for which no local adaptation was previously detected. These results challenge the assumption that species are functionally similar across their ranges and poleward peripheral populations are preadapted to warmer conditions. Rather, some taxa deserve population-level consideration when predicting the effects of climate change because they respond in genetically based, distinctive ways to changing conditions.

Complex life cycles and the responses of insects to climate change.

Many organisms have complex life cycles with distinct life stages that experience different environmental conditions. How does the complexity of life cycles affect the ecological and evolutionary responses of organisms to climate change? We address this question by exploring several recent case studies and synthetic analyses of insects. First, different life stages may inhabit different microhabitats, and may differ in their thermal sensitivities and other traits that are important for responses to climate. For example, the life stages of Manduca experience different patterns of thermal and hydric variability, and differ in tolerance to high temperatures. Second, life stages may differ in their mechanisms for adaptation to local climatic conditions. For example, in Colias, larvae in different geographic populations and species adapt to local climate via differences in optimal and maximal temperatures for feeding and growth, whereas adults adapt via differences in melanin of the wings and in other morphological traits. Third, we extend a recent analysis of the temperature-dependence of insect population growth to demonstrate how changes in temperature can differently impact juvenile survival and adult reproduction. In both temperate and tropical regions, high rates of adult reproduction in a given environment may not be realized if occasional, high temperatures prevent survival to maturity. This suggests that considering the differing responses of multiple life stages is essential to understand the ecological and evolutionary consequences of climate change.