Overwintering energetics and life-history trade-offs in insects: the interplay between stochastic and seasonal variation

Seasonality shapes major life-history strategies and adaptations across the tree of life. The alternating nature of seasons for growth and reproduction and seasons of adverse conditions can put conflicting selective pressures on energy use. Growing seasons often drive evolution of fast-paced processes and activity, while adverse seasons like winter drive evolution of dormancy and energy conservation. Thus, energy use strategies in seasonal environments have profound impacts on fitness. Integrating fitness across seasons and organismal responses to environmental change is key to understanding how populations will respond to ongoing global climate change. Energetics can play two essential roles in mediating organismal fitness in seasonal environments: energy reserves can determine winter survival, and energy at the end of winter can determine reproductive success. Survival and reproduction are both critical components of fitness, and thus energy allocation strategies may favor one over the other, revealing potential trade-offs when energy is limited. However, we do not know how environmental variation and predictability affect energy allocation strategies. Understanding the impacts of environmental change in seasonal environments will help us make better predictions of population responses and vulnerability to climate change.My dissertation aims to expand our understanding of overwintering energy use strategies, then explore how variable environments affect energy allocation strategies under a trade-off between maintenance and future reproduction. Finally, I test my predictions of energy allocation strategies under realistic winter conditions. Winter performance can determine summer performance, linking life cycles in seasonal environments. This work reveals the extent to which stochastic and predictable variation in seasonal environments can affect selective pressures and thus fitness in overwintering organisms. The carry-over effects of winter fitness into the growing season and vice versa expand our understanding of population responses to variable and changing environments. Chapter 1 explores the role of group behavior on energy conservation in overwintering aggregations, a potential energy use strategy that remains widely underexplored. The convergent ladybeetle (Hippodamia convergens) overwinters in massive aggregations, making it an ideal system for testing the effect of aggregation size on metabolic rates in overwintering insects. I measured energy use and thermal sensitivity of beetle aggregations across two ecologically relevant temperatures, and measured locomotor activity as one possible driver of group effects on energy use. Metabolic rates per beetle decreased with increasing aggregation size and scaled hypometrically with mass at both temperatures tested, with responses more pronounced at low temperatures. Activity decreased with aggregation size, but only at low temperatures. These results suggest that individuals within aggregations enter a deeper metabolically inactive state that single individual beetles cannot achieve, which is partly but not completely explained by a reduction in locomotor activity. This behavioral strategy for energy conservation may provide an additional selective advantage for the evolution of large overwintering aggregations. Chapter 2 explores the impact that variation in predictable and stochastic environments has on an energy allocation trade-off between somatic maintenance and future reproduction. Seasonality can modulate selection of energy use strategies, but we currently lack a theoretical framework to generate predictions on energy allocation strategies under changing stochastic conditions. Stochastic extreme events, like heat waves or cold snaps, are increasing in frequency and can have major impacts on population fitness. Overwintering organisms can prepare for harsh conditions by investing energy into stress tolerance (somatic maintenance). However, energy reserves at the end of winter can also influence future reproductive fitness, depending on the relative importance of stored versus recently acquired reserves for reproduction across the capital to income breeding continuum. In this chapter, I develop a general theoretical model that assesses fitness under increasing probability of stochastic lethal events, temporal variation in probability of stochastic events through winter, and how a stochastic end of winter affects optimal allocation strategies in income and capital breeders. Increasing probability of extreme events modulates allocation strategies in capital breeders. Temporal variation in extreme events and stochastic end of the season can alter optimal timing of investments, offering insights on the mismatch costs that changing environments may impose on overwintering organisms. These results highlight the role of end reserves in seasonal transitions and identify capital breeders to be especially susceptible to climate change. Chapter 3 tests the predictions from Chapter 2 by applying it to a case study of a capital breeder, the beetle Chrysomela aeneicollis, and answering how variation in snow cover can affect a trade-off between winter survival and future reproduction in realistic scenarios. Variation in snow cover modulates stochastic cold events and baseline energetic costs for organisms overwintering underground. Winters with deep snow cover have high baseline winter costs while having a low risk of lethal cold events. On the other hand, winters with little or no snow cover have low baseline winter costs but organisms are exposed to a high risk of lethal cold. In this chapter, I build on Chapter 2 by incorporating organism-specific parameters for energy reserves, rates of energy use, and microclimate conditions. I develop a model to systematically explore how cold risk, baseline winter costs, and their interaction under realistic winter scenarios affect energy use, survival, and allocation strategies of the willow leaf beetle (Chrysomela aeneicollis). My results support conclusions from Chapter 2, as increased cold risk and baseline costs can drive allocation strategies, but the response is strongly dependent on starting reserves. Increased cold risk affects future reproduction of beetles starting winter with high reserves, while increased baseline costs affect both reproduction and survival for lean beetles. Under realistic winter conditions, snow cover can modulate the trade-off between winter survival and future reproduction. Overwintering organisms under deep snow cover show high survival at the cost of reproduction, while winters with low snow favored reproduction at the cost of survival. These results show that both starting reserves and winter conditions, in the form of cold risk and baseline costs, drive distinct energy allocation strategies, and offer new insights into population dynamics and predictions under climate change.

Advisor: Williams, Caroline M