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

Abstract

Diapause is an important escape mechanism from seasonal stress in many insects. A certain minimum amount of time in diapause is generally needed in order for it to terminate. The mechanisms of time-keeping in diapause are poorly understood, but it can be hypothesized that a well-developed neural system is required. However, because neural tissue is metabolically costly to maintain, there might exist conflicting selective pressures on overall brain development during diapause, on the one hand to save energy and on the other hand to provide reliable information processing during diapause. We performed the first ever investigation of neural development during diapause and non-diapause (direct) development in pupae of the butterfly Pieris napi from a population whose diapause duration is known. The brain grew in size similarly in pupae of both pathways up to 3 days after pupation, when development in the diapause brain was arrested. While development in the brain of direct pupae continued steadily after this point, no further development occurred during diapause until temperatures increased far after diapause termination. Interestingly, sensory structures related to vision were remarkably well developed in pupae from both pathways, in contrast with neuropils related to olfaction, which only developed in direct pupae. The results suggest that a well-developed visual system might be important for normal diapause development.

Genome-wide variation and transcriptional changes in diverse developmental processes underlie the rapid evolution of seasonal adaptation

“…We did not detect pulses, or waves of gene expression at the whole-CNS level that are often associated with metamorphosis (61) and neurogenesis (60), although such patterns may be present in specific neuron subtypes or may have been obscured by interindividual variation within our sampling pools. Gross CNS morphology did not change during 6 mo of diapause, a pattern also observed based on fineresolution imaging of brain substructures over time in diapausing butterfly pupae (62). However, the overall signal of development in the transcriptomic data, for example up-regulation of cell fate proteins associated with cell differentiation, and many transcripts associated with neurogenesis, is most consistent with some sort of developmental progression.…”

“…Such an evolutionary innovation would represent an extreme analog of the well-documented phenomenon of substantial variation in the duration of all individual life cycle stages across Insecta ( 65 ). Indeed, the developmental steps during CNS metamorphosis are indistinguishable between direct developing and diapausing pupae of the butterfly Pieris napi ( 62 ). Moreover, measurable morphogenesis seems to occur during diapause in other insects, particularly gonadal development during adult reproductive diapause ( 26 , 28 ).…”

Diapause research in insects: historical review and recent work perspectives

“…Recently, Lehmann et al. () demonstrated that in the butterfly Pieris napi (L.), the sensory structures linked to vision are well developed in pupae in diapause, unlike other cerebral structures. These results, although preliminary, suggest that these structures may play a role in maintaining and terminating diapause (Lehmann et al., ).…”

“…In insects, neural mechanisms associated with the detection of photoperiodism could be involved in measuring the amount of time elapsed since the onset of diapause (Saunders, 2012). Recently, Lehmann et al (2017a) demonstrated that in the butterfly Pieris napi (L.), the sensory structures linked to vision are well developed in pupae in diapause, unlike other cerebral structures. These results, although preliminary, suggest that these structures may play a role in maintaining and terminating diapause (Lehmann et al, 2017a).…”

“…Recently, Lehmann et al (2017a) demonstrated that in the butterfly Pieris napi (L.), the sensory structures linked to vision are well developed in pupae in diapause, unlike other cerebral structures. These results, although preliminary, suggest that these structures may play a role in maintaining and terminating diapause (Lehmann et al, 2017a). More in-depth exploring of the role of insulin signaling pathway in diapause regulation would also be necessary to better understand diapause termination mechanisms in insects (Sim & Denlinger, 2013).…”