Seasonal energetics: are insects constrained by energy during dormancy?

In seasonal environments, many animals, including insects, enter dormancy, where they are limited to a fixed energy budget. The inability to replenish energetic stores during these periods suggests insects should be constrained by pre-dormancy energy stores. Over the last century, the community of researchers working on survival during dormancy has operated under the strong assumption that energy limitation is a key fitness trait driving the evolution of seasonal strategies. That is, energy use has to be minimized during dormancy because insects otherwise run out of energy and die during dormancy, or are left with too little energy to complete development, reproductive maturation or other costly post-dormancy processes such as dispersal or nest building. But if energy is so strongly constrained during dormancy, how can some insects - even within the same species and population - be dormant in very warm environments or show prolonged dormancy for many successive years? In this Commentary, we discuss major assumptions regarding dormancy energetics and outline cases where insects appear to align with our assumptions and where they do not. We then highlight several research directions that could help link organismal energy use with landscape-level changes. Overall, the optimal energetic strategy during dormancy might not be to simply minimize metabolic rate, but instead to maintain a level that matches the demands of the specific life-history strategy. Given the influence of temperature on energy use rates of insects in winter, understanding dormancy energetic strategies is critical in order to determine the potential impacts of climate change on insects in seasonal environments.

Aggregations reduce winter metabolic rates in the diapausing ladybeetle Hippodamia convergens.

Energy conservation is linked to survival and fitness of overwintering ectotherms, and is particularly critical in winter. Although many insects overwinter individually, some form aggregations with conspecifics. Aggregations cause metabolic suppression in some insects, but the effect of aggregations on metabolic rates and energy use in overwintering aggregations remains 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. We measured metabolic rates of beetle aggregations of 1, 10, 25, and 50 individuals using stop-flow respirometry across two ecologically relevant temperatures, and measured locomotor activity as one possible driver of group effects on metabolic rate. Metabolic rates per beetle decreased with increasing aggregation size at both temperatures, but was more pronounced at low temperatures. Metabolic rates scaled hypometrically with mass, with deeper response at cool 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 group strategy for energy conservation may provide an additional selective advantage for the evolution of large overwintering aggregations.

Movement of a Heliconius hybrid zone over 30 years: A Bayesian approach.

Hybrid zones have long been of interest to biologists as natural laboratories where we can gain insight into the processes of adaptation and speciation. Repeated sampling of individual hybrid zones has been particularly useful in elucidating the dynamic balance between selection and dispersal that maintains most hybrid zones. Here, we revisit a hybrid zone between Heliconius erato butterflies in Panamá for a third time over more than 30 years. We combine a novel Bayesian extension of stepped-cline hybrid zone models with environmental data to understand the genetic and environmental causes of cline dynamics in this species. The cline has continued to move west, likely due to dominance drive, but has slowed and broadened. Environmental analyses suggest that widespread deforestation in Panamá could be leading to decreased avian predation and relaxed selection, causing the observed changes in cline dynamics.

Cold adaptation increases rates of nutrient flow and metabolic plasticity during cold exposure in Drosophila melanogaster.

Metabolic flexibility is an important component of adaptation to stressful environments, including thermal stress and latitudinal adaptation. A long history of population genetic studies suggest that selection on core metabolic enzymes may shape life histories by altering metabolic flux. However, the direct relationship between selection on thermal stress hardiness and metabolic flux has not previously been tested. We investigated flexibility of nutrient catabolism during cold stress in Drosophila melanogaster artificially selected for fast or slow recovery from chill coma (i.e. cold-hardy or -susceptible), specifically testing the hypothesis that stress adaptation increases metabolic turnover. Using (13)C-labelled glucose, we first showed that cold-hardy flies more rapidly incorporate ingested carbon into amino acids and newly synthesized glucose, permitting rapid synthesis of proline, a compound shown elsewhere to improve survival of cold stress. Second, using glucose and leucine tracers we showed that cold-hardy flies had higher oxidation rates than cold-susceptible flies before cold exposure, similar oxidation rates during cold exposure, and returned to higher oxidation rates during recovery. Additionally, cold-hardy flies transferred compounds among body pools more rapidly during cold exposure and recovery. Increased metabolic turnover may allow cold-adapted flies to better prepare for, resist and repair/tolerate cold damage. This work illustrates for the first time differences in nutrient fluxes associated with cold adaptation, suggesting that metabolic costs associated with cold hardiness could invoke resource-based trade-offs that shape life histories.

Adaptation to Low Temperature Exposure Increases Metabolic Rates Independently of Growth Rates.

Metabolic cold adaptation is a pattern where ectotherms from cold, high-latitude, or -altitude habitats have higher metabolic rates than ectotherms from warmer habitats. When found, metabolic cold adaptation is often attributed to countergradient selection, wherein short, cool growing seasons select for a compensatory increase in growth rates and development times of ectotherms. Yet, ectotherms in high-latitude and -altitude environments face many challenges in addition to thermal and time constraints on lifecycles. In addition to short, cool growing seasons, high-latitude and - altitude environments are characterized by regular exposure to extreme low temperatures, which cause ectotherms to enter a transient state of immobility termed chill coma. The ability to resume activity quickly after chill coma increases with latitude and altitude in patterns consistent with local adaptation to cold conditions. We show that artificial selection for fast and slow chill coma recovery among lines of the fly Drosophila melanogaster also affects rates of respiratory metabolism. Cold-hardy fly lines, with fast recovery from chill coma, had higher respiratory metabolic rates than control lines, with cold-susceptible slow-recovering lines having the lowest metabolic rates. Fast chill coma recovery was also associated with higher respiratory metabolism in a set of lines derived from a natural population. Although their metabolic rates were higher than control lines, fast-recovering cold-hardy lines did not have faster growth rates or development times than control lines. This suggests that raised metabolic rates in high-latitude and -altitude species may be driven by adaptation to extreme low temperatures, illustrating the importance of moving "Beyond the Mean".