How do variable environments drive the evolution of metabolic physiology in ectotherms?

An organism’s central task is to obtain nutrients from the environment, and divide those nutrients among competing demands in the way that best enhances the passing on of its genes. This task is complicated enormously by the fact that environments vary widely in concentrations of nutrients, and in abiotic factors such as temperature and oxygen that profoundly impact the acquisition and processing of those nutrients. Fluctuations in these abiotic factors can push organisms outside tolerance limits, inducing stress responses that in turn alter resource allocation strategies. My research aims to uncover drivers, mechanisms and consequences of adaptive evolutionary change in pathways of energy metabolism, in response to environmental variability. My current research focuses on four inter-related themes: 1) Evolutionary impacts of seasonality; 2) Mechanisms and consequences of stress responses; and 3) Mechanisms of life history evolution; and 4) Methods development in metabolic physiology and biochemistry. I use a diverse array of small ectotherms in my research, mostly insects (although now I have students working on tardigrades and aquatic snails!). Small ectotherms frequently have body temperatures close to environmental temperatures, comprise many important herbivores that are an integral link in terrestrial food webs, and are extremely sensitive to changes in the environment.

My research combines field-based natural history and experiments with laboratory-based biochemistry and physiology. I use the UC Natural Reserves extensively for empirical work. One of the hallmarks of research in my lab is a focus on linking detailed biochemical and physiological measurements to their life history and fitness consequences. Biochemical and physiological techniques are often low-throughput, limiting their application in ecological and evolutionary studies that frequently require large sample sizes and multiple treatment groups. We overcome this challenge by first doing the careful and slow biochemistry and physiology across multiple levels of the biological hierarchy (from molecules, cells and organs to tissues and whole organisms), and then using the results to develop and validate high-throughput assays that recapitulate the phenotype of interest. This approach has enabled me to discover links between genotype and physiological phenotype, and understand how those links are mediated through the biochemistry of metabolic pathways. Another hallmark of my research approach is the analysis of evolutionary change in the plasticity of physiological traits. Unlike morphological traits that are frequently fixed during development, physiological traits are labile over the entire lifetime of an organism, responding almost instantly to changes in environmental conditions with changes in their rates and intensities. Thus, most physiological traits are best described as curves or functions that describe their environmental sensitivity. Joel Kingsolver and Ray Huey, among others, have pioneered this “curve-thinking”, and this approach is revealing that much of physiological evolution occurs in the shape of these curves. My research incorporates these powerful theoretical advances to understand how environmental variability on a range of timescales, ranging from a fraction of an organism’s lifetime to multiple generations, reshapes the sensitivity of physiological traits to environmental variation.

Evolutionary Impacts of Winter

Climate change research historically focused on summer, and winter climate change was considered mostly beneficial due to amelioration of damaging cold. My research is shifting this paradigm, and illustrating how sub-lethal performance consequences of variation in winter conditions drive responses of terrestrial organisms to climate change.  I have shown that winter warming negatively impacts many insects by increasing metabolic rates and energy drain, which can reduce subsequent reproduction. Selective pressures imposed by warm winters can lead to changes in the thermal sensitivity of metabolism, leading to better performance over winter and in the subsequent growing season. Using field- and lab-based reciprocal transplant experiments, I demonstrated that winter conditions drive local adaptation of insect populations, suggesting that changes in winter conditions may cause population declines across the range. I have shown that cold adaptation increases metabolic costs due to increased flux through central metabolic pathways, allowing cold hardy flies to synthesize protective molecules more rapidly. This suggests a mechanism through which cold stress shapes evolution of metabolic pathways, possibly contributing to large-scale biogeographic patterns in life histories previously attributed to selection on growing season performance. Together, this work illustrates how profoundly winter conditions shape ecology and evolution of ectothermic animals.

Current research

I am currently investigating how snow drives ecology and evolution of insects. In collaboration with Nathan Rank, Elizabeth Dahlhoff and Jonathon Stillman, we are using Sierra Nevada willow leaf beetles, which live in highly seasonal montane environments, to understand physiological and genetic responses to snow. We aim to understand how inter-annual fluctuation in snowpack and air temperature interact to determine performance and evolution, towards my long-term goal of understanding how variation in winter conditions maintains genetic variation in natural populations. My second major research direction seeks to understand biochemical and metabolic origin of resource-based trade-offs. Why do we see such striking variation in the capacity for energy generation across individuals and species with divergent life history demands? What constrains evolution of metabolic systems? We are collaborating with Tony Zera using wing polymorphic Gryllus crickets to understand how metabolic physiology diverges during life history evolution, and how these metabolic processes constrain the evolution of life histories.