Developmental plasticity in metabolism but not in energy reserve accumulation in a seasonally polyphenic butterfly

Abstract

The evolution of seasonal polyphenisms (discrete phenotypes in different annual generations) associated with alternative developmental pathways of diapause (overwintering) and direct development is favoured in temperate insects. Seasonal life history polyphenisms are common and include faster growth and development under direct development than diapause. However, the physiological underpinnings of this difference remain poorly known despite its significance for understanding the evolution of polyphenisms. We measured respiration and metabolic rates through the penultimate and final larval instars in the butterfly Pieris napi and show that directly developing larvae grew and developed faster and had a higher metabolic rate than larvae entering pupal diapause. The metabolic divergence appeared only in the final instar, that is, after the induction of developmental pathway that takes place in the penultimate instar in P. napi. The accumulation of fat reserves during the final larval instar was similar under diapause and direct development, which was unexpected as diapause is predicted to select for exaggerated reserve accumulation. This suggests that overwinter survival may be more dependent on metabolic suppression during diapause than the size of energy reserves. The results, nevertheless, demonstrate that physiological changes coincide with the divergence of life histories between the alternative developmental pathways, thus elucidating the proximate basis of seasonal life history polyphenisms.Summary statementThe switch between diapause and direct development results in developmental pre-diapause plasticity in life history and metabolism but not in reserve accumulation in a seasonally polyphenic butterfly.

Additive and non‐additive effects of day and night temperatures on thermally plastic traits in a model for adaptive seasonal plasticity

“…And studies in other lepidopterans have documented seasonal plasticity in metabolism (Kivelä et al. 2019). Aside from association to food acquisition and processing, potential day‐night differences in temperature perception could also contribute to day temperature having a higher impact on development time.…”

“…Studies in different insects have, indeed, documented associations between temperature and various metabolism-related variables, including food ingestion efficiency (Rall et al 2010), depletion of energy reserves (Klepsatel et al 2016, Klepsatel et al 2019, lipid storage (Jang and Lee 2018), and effects of macro-nutrient diet in development (Kutz et al 2019). And studies in other lepidopterans have documented seasonal plasticity in metabolism (Kivelä et al 2019). Aside from association to food acquisition and processing, potential day-night differences in temperature perception could also contribute to day temperature having a higher impact on development time.…”

Watching the days go by: Asymmetric regulation of caterpillar development by changes in photoperiod

“…Hence, if the physiological preparations required for successful diapause take a longer time to establish than those required for nondiapause development, it may be adaptive to resist a sudden switch to diapause development, even given environmental cues signaling the end of the season. However, the metabolomic similarity of diapause‐destined and nondiapause‐destined larvae seen in some species (Kivelä et al., 2019) speaks against this hypothesis. The asymmetric pattern may also be a result of other selective drivers, such as the multiplicative increase afforded by an additional generation, or the risks associated with entering diapause too early.…”