Heidi J. MacLean

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.

Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity

Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity’s key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits.

Evolutionary Change in Continuous Reaction Norms

Understanding the evolution of reaction norms remains a major challenge in ecology and evolution. Investigating evolutionary divergence in reaction norm shapes between populations and closely related species is one approach to providing insights. Here we use a meta-analytic approach to compare divergence in reaction norms of closely related species or populations of animals and plants across types of traits and environments. We quantified mean-standardized differences in overall trait means (Offset) and reaction norm shape (including both Slope and Curvature). These analyses revealed that differences in shape (Slope and Curvature together) were generally greater than differences in Offset. Additionally, differences in Curvature were generally greater than differences in Slope. The type of taxon contrast (species vs. population), trait, organism, and the type and novelty of environments all contributed to the best-fitting models, especially for Offset, Curvature, and the total differences (Total) between reaction norms. Congeneric species had greater differences in reaction norms than populations, and novel environmental conditions increased the differences in reaction norms between populations or species. These results show that evolutionary divergence of curvature is common and should be considered an important aspect of plasticity, together with slope. Biological details about traits and environments, including cryptic variation expressed in novel environmental conditions, may be critical to understanding how reaction norms evolve in novel and rapidly changing environments.

Common garden experiments reveal uncommon responses across temperatures, locations, and species of ants

Population changes and shifts in geographic range boundaries induced by climate change have been documented for many insect species. On the basis of such studies, ecological forecasting models predict that, in the absence of dispersal and resource barriers, many species will exhibit large shifts in abundance and geographic range in response to warming. However, species are composed of individual populations, which may be subject to different selection pressures and therefore may be differentially responsive to environmental change. Asystematic responses across populations and species to warming will alter ecological communities differently across space. Common garden experiments can provide a more mechanistic understanding of the causes of compositional and spatial variation in responses to warming. Such experiments are useful for determining if geographically separated populations and co-occurring species respond differently to warming, and they provide the opportunity to compare effects of warming on fitness (survivorship and reproduction). We exposed colonies of two common ant species in the eastern United States, Aphaenogaster rudis and Temnothorax curvispinosus, collected along a latitudinal gradient from Massachusetts to North Carolina, to growth chamber treatments that simulated current and projected temperatures in central Massachusetts and central North Carolina within the next century. Regardless of source location, colonies of A. rudis, a keystone seed disperser, experienced high mortality and low brood production in the warmest temperature treatment. Colonies of T. curvispinosus from cooler locations experienced increased mortality in the warmest rearing temperatures, but colonies from the warmest locales did not. Our results suggest that populations of some common species may exhibit uniform declines in response to warming across their geographic ranges, whereas other species will respond differently to warming in different parts of their geographic ranges. Our results suggest that differential responses of populations and species must be incorporated into projections of range shifts in a changing climate.

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. Summary: Heat tolerance in Manduca sexta larvae is affected by both the magnitude and the temporal pattern of previous exposure to high temperatures.

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

We use field experiments to examine how butterflies achieve the flight required to forage, mate, and lay eggs in cool, montane environments. Potential adaptations include thermoregulatory traits that elevate body temperatures, basking behaviors, or shifts in the thermal sensitivity of flight. By comparing populations and species along an elevation gradient, we find that they use a combination of morphological, physiological, and behavioral adaptations to achieve flight.

Growth, developmental and stress responses of larvae of the clouded sulphur butterfly Colias eriphyle to repeated exposure to high, sub-lethal temperatures

The optimal temperature at which an organism grows and develops is commonly correlated with latitude and elevation; however, the maximum temperature for physiological performance often is not. This makes performance at temperatures between the optimum and the maximum of particular interest. Temperature can influence long‐term performance (growth and development), as well as short‐term performance (heat shock protein) responses differentially. In the present study, two populations of the clouded sulphur butterfly Colias eriphyle Edwards that differ in elevation, thermal regime and optimal and maximum temperatures are studied to quantify their responses to repeated, sub‐lethal heat treatments early in development (second instar). Heat treatments accelerate development during the second to fourth instars in both populations initially, although this effect disappears by pupation. Heat treatment decreases pupal mass in the lower elevation population, suggesting that repeated exposure to high temperatures early in development may reduce final size and fecundity in this population. Heat shock protein gene (hsp70) expression levels in the lower elevation (1633 m a.s.l.) population are highest 24 h after the start of the heat treatment and then the fall to pre‐exposure levels by 36–72 h, suggesting a rapid response to stressful temperatures. By contrast, heat treatment has no significant effect on pupal mass in the higher elevation (2347 m a.s.l.) population. This population has higher levels of hsp70 expression overall but constant expression levels, suggesting that the temperature treatments used are insufficient to elicit a heat stress response. Overall, the effects of repeated exposure to sub‐lethal high temperatures early in development on growth, final size and gene expression differ between populations that differ in thermal sensitivity.