Energy and lipid metabolism during direct and diapause development in a pierid butterfly

Abstract

Diapause is a fundamental component of the life cycle in the majority of insects living in environments characterized by strong seasonality. The present study addresses poorly understood associations and trade-offs between endogenous diapause duration, thermal sensitivity of development, energetic cost of development and cold tolerance. Diapause intensity, metabolic rate trajectories and lipid profiles of directly developing and diapausing animals were studied using pupae and adults of Pieris napi butterflies from a population in which endogenous diapause has been well studied. Endogenous diapause was terminated after 3 months and termination required chilling. Metabolic and post-diapause development rates increased with diapause duration, while the metabolic cost of post-diapause development decreased, indicating that once diapause is terminated, development proceeds at a low rate even at low temperature. Diapausing pupae had larger lipid stores than the directly developing pupae, and lipids constituted the primary energy source during diapause. However, during diapause, lipid stores did not decrease. Thus, despite lipid catabolism meeting the low energy costs of the diapausing pupae, primary lipid store utilization did not occur until the onset of growth and metamorphosis in spring. In line with this finding, diapausing pupae contained low amounts of mitochondria-derived cardiolipins, which suggests a low capacity for fatty acid β-oxidation. While ontogenic development had a large effect on lipid and fatty acid profiles, only small changes in these were seen during diapause. The data therefore indicate that the diapause lipidomic phenotype is developed early, when pupae are still at high temperature, and retained until post-diapause development.

Idiosyncratic development of sensory structures in brains of diapausing butterfly pupae: implications for information processing

“…Additionally, we investigated newly eclosed (2-day-old) adults from both pathways and 69- and 114-day-old pupae in diapause (P69 and P114 henceforth). Based on previous data, we know diapause is terminated in the studied population after approximately 114 days [5,15]. Therefore, we took out post-termination pupae from the cold after 144 days and sampled after 4 days at 10°C (P148 henceforth), 7 days at 10°C plus 1 day at 20°C (P152 henceforth) and finally, 7 days at 10°C plus 7 days at 20°C (P158 henceforth).…”

Monarch butterflies use an environmentally sensitive, internal timer to control overwintering dynamics

“…The defining feature of diapause is that it fundamentally changes organismal response to environment, rendering individuals insensitive to normally permissive environmental cues. Much previous work has been dedicated to understanding the molecular mechanisms behind the maintenance of environmental insensitivity (e.g., Lehmann et al, ), or rather how gene expression differs between diapause and either nondiapause or post‐diapause quiescence states (e.g., Poelchau, Reynolds, Elsik, Denlinger, & Armbruster, ; Ragland & Keep, ). Here we are able to address an equally important but open problem: through what genetic mechanisms is diapause acting to change response to environmental conditions?…”

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

“…These physiological differences culminate in the life stage that is capable of entering diapause, because surviving a long adverse period in the dormant state of diapause necessitates a very different physiology compared to direct development into reproductive adult (e.g. Han and Bauce, 1998; Hahn and Denlinger, 2007, 2011; Liu et al, 2007, 2016; Rozsypal et al, 2013; Lehmann et al, 2016, 2018).…”

“…Besides metabolic rate, the diapause and direct development pathways are expected to show also other pre-diapause physiological differences. Overwinter survival necessitates energy reserves that can fuel metabolism through the whole dormant period during which feeding is either not possible at all or insufficient to fully fuel metabolism (Tauber et al, 1986; Danks, 1987; Hahn and Denlinger, 2007, 2011; Lehmann et al, 2016, 2018; see Liu et al, 2016 for energy reserves for summer diapause). These energy reserves must be accumulated before the beginning of diapause, which may result in differences between pathways in the allocation of resources to building reserves (Tauber et al, 1986; Danks, 1987; Hahn and Denlinger, 2007, 2011; Liu et al, 2007).…”

“…This information is vital to fully understand the physiology of alternative developmental pathways. In P. napi , diapause pupae contain more storage lipids than pupae that develop directly into adult six days after pupation, lipidomes and metabolomes differing between the developmental pathways in the same phase of pupal development as well (Lehmann et al, 2016, 2018). It remains unknown if these differences appear already in the larval stage during which lipid reserves are accumulated in P. napi (Kivelä et al, 2016b) and many other insects (Tauber et al, 1986; Hahn and Denlinger, 2007, 2011).…”