Research

Selection of Current Projects

Winter in a changing world: the critical importance of snow

Collaborators: Elizabeth DahlhoffNathan RankJonathon StillmanIrja RatikainenØystein VarpeDoris Bachtrog, Kevin Roberts, Andre Szejner Sigal, Christina Lee, Elliott Smeds, Joanna Elmore.

Snow determines soil microclimate and responses to climate change. When snow is covering the soil it is protected from cold and variable temperatures, and loss of snow can, counterintuitively, lead to colder soils (Kearney 2020, Fitzpatrick et al. 2020, Zhu et al. 2019). Moving up a mountain, air temperatures decrease but snow buffering increases. The combined influences of air temperature and snow cover on organismal stress exposure along an elevational gradient is unknown, and this gap in knowledge limits our ability to predict impacts of declining snowpack due to climate warming. We determine how snow cover variation over the past decade in the Sierra Nevada mountains impacts cold and energy stress of willow leaf beetles, as a model for other ectotherms that overwinter in the soil in snowy habitats. We consider the whole life cycle, from growing season to growing season, to develop a theoretical and empirical understanding of how snow impacts physiology, ecology and evolution of these winter-adapted beetles. This work is currently led by PhD students Kevin Roberts and Andre Szejner Sigal, supported by research technician Christina Lee.

Sierra Nevada populations of the willow leaf beetle Chrysomela aeneicollis overwinter beneath snow in the soil as dormant adults for most of their lives (8 out of 12 months). Snow cover is highly variable in the Eastern Sierra Nevada mountain ranges these beetles call home, and environmental gradients in temperature and oxygen strongly influence beetle genetic structure and population dynamics (read about previous research in this system in this illustrated case study: https://evolution.berkeley.edu/evolibrary/article/dahlhoff_rank_01). We study the winter side of the story.

We have found that winter snow cover strongly modifies elevational gradients in two key fitness components for overwintering ectotherms: cold stress and energy stress; with cold stress peaking at mid-elevations (Roberts et al., in prep). Loss of snow cover due to climate change will most strongly impact stress exposure for mid-elevation populations, which will counterintuitively experience colder soils. Untangling the complex interactions between snow, air temperature, and soil temperature across the landscape is critical to predicting the impacts of climate change in snowy environments.

Funding:

NSF 1558159 (2014-present); co-PIs Elizabeth DahlhoffNathan Rank, and Jonathon Stillman (https://www.nsf.gov/awardsearch/showAward?AWD_ID=1558159)

Peder Sather Center; co-PIs Irja Ratikainen (NTNU) and Øystein Varpe (Bergen).

California Conservation Genomics Grant; co-PIs Elizabeth DahlhoffNathan Rank, and Doris Bachtrog.

Evolutionary physiology of a life history trade-off in Gryllus field crickets

In collaboration with Lisa Treidel, Anthony Zera, Kristi Montooth, Colin Meikeljohn, Ibrahim El Shesheny, David Gray, and David Weissman

Life history polymorphisms, wherein one genome produces two or more very different phenotypes, are widespread across animals and plants and are maintained by life history trade-offs, wherein there is no one “best” strategy across all environments. An example of a life history polymorphism is flight capability in insects. Flight is a key evolutionary innovation that enabled the huge diversification of insects, but is frequently lost because it is costly, and reduces investments in other fitness-relevant traits such as reproduction. This has led to widespread flight polymorphisms across many insect taxa. However, the evolutionary and physiological mechanisms by which flight is lost and gained across insect phylogenies are still unknown.

North American Gryllus field crickets show evidence for repeated evolutionary transitions to flight polymorphisms, with 35 species ranging from fully flight capable, through species that have both flight-capable and -incapable morphs (polymorphic), to fully flightless. This provides an ideal system to investigate the genetic and developmental processes underlying parallel losses and gains of flight capability through evolutionary time. PhD student Lisa Treidel is leading this project.

Detecting and predicting the relative contributions of fecundity and survival to fitness in changing environments

NSF IOS 1951396 (2020-2023) to Lauren Buckley (PI), Caroline Williams (co-PI) and Sean Schoville (co-PI).

We will use a system of montane grasshoppers distributed along an elevational gradient to understand how constraints on survival and fecundity (reproduction) will shift over time as a result of climate change. The project goal is to develop a general modeling approach that can bridge levels of biological organization, space and time to predict shifts in survival and reproduction constraints and thus improve our ability to forecast responses to environmental gradients and change.

For trainee-led research projects, see People tab. 

Past projects

Biochemical and physiological architecture of cold hardiness in Drosophila melanogaster (postdoctoral research, University of Florida, 2012- 2014)

In collaboration with Daniel Hahn (advisor), Ted Morgan, Art Edison, and David Allison (PIs, NSF grant 1051890), as well as Arezue Boroujerdi, Maria-Brigida Ferraro, Mario Guarracino, Brittany Lee, Marshall McCue, James Rocca, Nishanth Sunny, Andre Szejner (undergraduate researcher), Glenn Walter, and Miki Watanabe.

Bioenergetics, or energy flow within organisms, interacts with temperature to constrain species distributions and influence global patterns in species abundance. Normal physiological function requires organisms to precisely and dynamically balance energy supply and demand, but fluctuating temperatures make this difficult by changing rates of biochemical reactions within cells. Species distributions can thus be driven not only directly by exposure to lethal temperatures, but also indirectly through repeated or long-term exposures to sub-lethal temperatures that lead to energetic failures.

At low temperatures, insects enter into a cold-induced coma (chill-coma), during which mating and foraging is precluded and predators cannot be avoided. The rate of recovery from chill coma is a commonly used metric of cold tolerance and corresponds to the environment that the insect inhabits (insects from colder locations tend to recover more quickly. This suggests an adaptive response, but the mechanisms underlying variation in chill-coma recovery times are largely unknown. Differences in ionic regulation in the cold are clearly important at the proximate level (MacMillan and Sinclair 2011, Andersen et al. 2013, Findsen et al 2013), but the mechanisms underpinning evolutionary variation in ionic homeostasis are less clear. We hypothesized that evolutionary variation in chill-coma recovery times are driven by differences in the ability to maintain key catabolic processes in the cold, resulting from alterations to intermediary metabolism.

We addressed this hypothesis at the whole organism, pathway flux, and metabolite level using respirometry, growth rate assays, in vivo nuclear magnetic resonance spectroscopy, kinetic studies using stable isotope tracers, and metabolomics. We used a combination of experimental evolution lines and natural isolates with variation in chill coma recovery times (Drosophila genetic reference panel). We demonstrated that cold tolerant flies had higher whole-organism metabolic and growth rates, better maintenance of metabolic homeostasis and more robust metabolic networks in the cold (Williams et al. in press Evolution), and higher rates of glycolysis before and during cold exposure. This supports our hypothesis that remodelling of metabolic pathways underpins cold adaptation, leading to an improved ability to maintain metabolic homeostasis in the cold. Moreover, the metabolic changes were associated with changes in other important life-history traits (such as larval growth rate), suggesting that selection on recovery time from acute low temperature exposure can fundamentally reshape organismal life-histories.

Overwintering energetics in Lepidoptera (PhD research, University of Western Ontario, 2007-2012)

In collaboration with Brent Sinclair (supervisor), Wesley Chick (undergraduate researcher), Jason Dzurisin, Jessica Hellmann, Heath MacMillan, Katie Marshall, Shannon Pelini, and Raymond Thomas.

Winter temperatures are changing both in mean (a generally increasing trend), and in thermal variability (Williams et al. in press Biological Reviews). Although the intuitive outcome of increases in mean temperature are a release from cold-induced stress and mortality, increased temperature also increases the rate of use of stored energy reserves. Many insects that overwinter in temperate environments do so in a state of dormancy, so energy reserves with which they start the winter must see them through to spring and also sometimes fuel reproduction and post-winter performance. Thus, any increase in temperature during the winter can exacerbate energetic stress and decrease performance in winter and subsequent seasons. Negative fitness consequences of increases in winter temperature had been demonstrated for a few insects but not in others (Irwin and Lee 2003, Williams et al. 2003, Mercader and Scriber 2008), so we did not know how widespread these negative effects might be across species, nor whether insects had mechanisms to compensate for energy drain resulting for winter warming. These gaps in knowledge seriously impeded our ability to predict whether negative effects of winter warming were likely to be widespread.

During my doctoral work, I employed a comparative approach to address two main questions: 1) what are the impacts of winter warming or changes in thermal variability on insects at the biochemical, physiological and ecological levels, and 2) can insects modify their metabolism to mitigate any negative effects, either through phenotypic plasticity or genetic adaptation. I found that moderate degrees of winter warming (4 degC) reduced energy reserves in a skipper butterfly that overwinters as a larva and has a restricted distribution, but did not reduce energy reserves in two species of swallowtail butterflies that overwintered as pupae and were widely distributed (Williams et al. 2012 Climate Research). The skipper butterfly, Erynnis propertius, lives along the west coast of North America along a strong thermal variability gradient (the center of its range in Oregon has high daily thermal variability, while the northern range edge populations on Vancouver Island experience little daily variability). Thermal variability can also increase energy use, due to the non-linear shapes of biological rate functions (go here for an excellent explanation of Jensen’s inequality). Therefore I hypothesized that  thermally variable environments would be more energy-demanding, and that populations that had evolved in such environments would have been under strong selective pressure to dampen the thermal sensitivity of their metabolism. By rearing larvae in the lab from hatching under conditions designed to mimic Oregon and Vanvcouver Island, I discovered that larvae from Oregon had a suppressed thermal sensitivity of metabolic rate relative to those from Oregon (Williams et al. 2012 PLoS ONE). Interestingly, when the larvae from each population were raised at the opposite to their natal temperature, I found that Vancouver Island larvae could plastically suppress their thermal sensitivity to the same degree as the Oregon population, but that the Oregon population were canalised in their suppression (they did not become more thermally sensitive when raised under less variable conditions). I combined my empirical metabolic rate data with historical climate data to estimate the energetic consequences of the suppression of thermal sensitivity, and found that larvae would save ~20% of their energy use overwinter in a variable environment by suppressing their thermal sensitivity. This was the first evidence for thermal variability driving metabolic suppression, and suggested that changes in thermal variability over winter will be important selective agents.

Finally, I turned to a different system to study the cross-seasonal consequences of changes in the winter thermal environment. Using a lab-based simulated reciprocal transplant, I found that populations of a widespread thermal generalist moth were locally adapted to their winter environment such that the northern range edge population performed better under cooler, northern conditions, while a population from the center of the range performed better under warmer central conditions (Williams et al. in press Functional Ecology). This was mediated through alterations to energy storage that allowed each population to retain energy stores and size better in their natal environment. Both populations suppressed their metabolic rates in warm winter conditions; a pattern I have also observed in a swallowtail (Papilio zelicaon, unpublished data) and which thus appears to be widespread among the Lepidoptera.

Thus, my doctoral research uncovered a large amount of variation in the responses to Lepidopteran species to winter warming. Some species were unaffected, some suffered performance decreases, and for some species the responses were population-specific and depended on the thermal history. I uncovered several systems in which Lepidopteran insects modify their metabolism to compensate for winter warming – a phenomenon that was previously unknown. In the future, I want to delve further into the mechanisms by which metabolism can be modified, including the pathways and enzymes that are modulated and the genetic changes that occur to bring them about.