Gene expression profiling across ontogenetic stages in the wood white (Leptidea sinapis) reveals pathways linked to butterfly diapause regulation

Abstract

In temperate latitudes, many insects enter diapause (dormancy) during the cold season, a period during which developmental processes come to a standstill. The wood white (Leptidea sinapis) is a butterfly species distributed across western Eurasia that shows photoperiod-induced diapause with variation in critical day-length across populations at different latitudes. We assembled transcriptomes and estimated gene expression levels at different developmental stages in experimentally induced directly developing and diapausing cohorts of a single Swedish population of L. sinapis to investigate the regulatory mechanisms underpinning diapause initiation. Different day lengths resulted in expression changes of developmental genes and affected the rate of accumulation of signal molecules, suggesting that diapause induction might be controlled by increased activity of monoamine neurotransmitters in larvae reared under short-day light conditions. Expression differences between light treatment groups of two monoamine regulator genes (DDC and ST) were observed already in instar III larvae. Once developmental pathways were irreversibly set at instar V, a handful of genes related to dopamine production were differentially expressed leading to a significant decrease in expression of global metabolic genes and increase in expression of genes related to fatty acid synthesis and sequestration. This is in line with a time-dependent (hour-glass) model of diapause regulation where a gradual shift in the concentration of monoamine neurotransmitters and their metabolites during development of larvae under short-day conditions leads to increased storage of fat, decreased energy expenditures, and ultimately developmental stasis at the pupal stage.

Multilayered Tuning of Dosage Compensation and Z-Chromosome Masculinization in the Wood White (Leptidea sinapis) Butterfly

“…Gene expression levels were assessed using recently published RNA-seq data obtained for distinct developmental stages of L. sinapis (Leal et al. 2018).…”

“…Substantial changes in overall gene expression between developmental stage transitions has previously been observed (e.g., Leal et al. 2018), but the impact of metamorphosis on temporal patterns of dosage compensation has not been thoroughly analyzed in any lepidopteran species.…”

Transcriptome and gene expression analysis of three developmental stages of the coffee berry borer, Hypothenemus hampei

“…The availability of sequence databases is very useful for a better understanding of host-pathogen interactions 19 , feeding mechanisms 20 , development 21 , and defense pathways in phytophagous insects 22 . Additionally, a significant number of studies using transcriptomic-based approaches have focused on identifying genes involved in developmental processes, with expression profiles among different life stages reported in several insect species 21,23,24 . Recent studies have reported such gene expression analyses across different developmental stages in lepidopteran pests of global economic relevance 24–26 .…”

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

“…Furthermore, we show that environmental conditions (we predict cold temperature in this case) modulate the timer and propose that this may occur through cryoprotectant accumulation. Accumulation of small molecule cryoprotectants (e.g., sorbitol, alanine, etc) in response to cold exposure has been observed in diapause and implicated in diapause termination in other insects (e.g., Leal et al, ; Lehmann et al, ; Michaud & Denlinger, ; Wang, Egi, Takeda, Oishi, & Sakamoto, ). Calcium signalling mediates osmotic stress due to small molecule cryoprotectant accumulation in insects (Storey, ).…”

“…Accumulation of small molecule cryoprotectants (e.g., sorbitol, alanine, etc) in response to cold exposure has been observed in diapause and implicated in diapause termination in other insects (e.g., Leal et al, 2018;Lehmann et al, 2018;Michaud & Denlinger, 2007;Wang, Egi, Takeda, Oishi, & Sakamoto, 2014). Calcium signalling mediates osmotic stress due to small molecule cryoprotectant accumulation in insects (Storey, 1990).…”