Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect

Abstract

Insects living in the temperate zone enter a physiological state of arrested or slowed development to overcome an adverse season, such as winter. Developmental arrest, called diapause, occurs at a species-specific developmental stage, and embryonic and pupal diapauses have been extensively studied in mostly holometabolous insects. Some other insects overwinter in the nymphal stage with slow growth for which the mechanism is poorly understood. Here, we show that this nymphal period of slow growth is regulated by temperature and photoperiod through separate pathways in the cricket Modicogryllus siamensis. The former regulates the growth rate, at least in part, through the insulin / target of rapamycin (TOR) signaling pathway. Lower temperature down-regulates the expression of insulin-like peptide (Ms’Ilp) and Target of rapamycin (Ms’Tor) genes to slow down the growth rate without affecting the number of molts. The latter regulates the number of molts independent of temperature. Short days increase the number of molts through activation of the juvenile hormone (JH) pathway and down-regulation of myoglianin (Ms’myo), a member of the TGFβ family, which induces adult metamorphosis. In contrast, long days regulate Ms’myo expression to increase during the fifth to sixth instar to initiate adult metamorphosis. When Ms’myo expression is suppressed, juvenile hormone O-methyl transferase (Ms’jhamt) was up-regulated and increased molts to prolong the nymphal period even under long-day conditions. The present findings suggested that the photoperiod regulated Ms’myo, and the JH signaling pathway and the temperature-controlled insulin/TOR pathway cooperated to regulate nymphal development for overwintering to achieve seasonal adaptation of the life cycle in M. siamensis.

Chromosome-level genome assembly of Chironomus striatipennis Kieffer provides insights into benthic adaptation and metamorphosis mechanism

“…It can change the developmental trajectory to deal with different environments, which is also a strategy for adapting the environment. Like most insects, chironomid midge is also coordinately regulated by ecdysone and juvenile hormone from larva to pupa and to adult, juvenile hormone can prevent metamorphosis induced by ecdysone (Guo et al, 2019;Hu X. L. et al, 2019;Miki et al, 2020;Santos et al, 2019). The genes involved in biosynthesis of ecdysone and juvenile hormone which regulate insect development were also recognized inC. striatipennis.…”

Constraints and Opportunities for the Evolution of Metamorphic Organisms in a Changing Climate

“…However, the environment can impact hormones that regulate growth. A recent study on the cricket Modicogryllus siamensis demonstrated that higher rearing temperatures lead to enhanced Insulin/TOR signaling, leading to faster growth rate (Miki et al, 2020). Insulin/TOR signaling, however, does not impact the number of instars in M. siamensis; instead, the timing of JH decline impacts the duration of the juvenile growth period in a photoperiod-dependent manner (Miki et al, 2020).…”

“…A recent study on the cricket Modicogryllus siamensis demonstrated that higher rearing temperatures lead to enhanced Insulin/TOR signaling, leading to faster growth rate (Miki et al, 2020). Insulin/TOR signaling, however, does not impact the number of instars in M. siamensis; instead, the timing of JH decline impacts the duration of the juvenile growth period in a photoperiod-dependent manner (Miki et al, 2020). Thus, body size determination appears to rely on a complex interaction of endocrine regulators that respond differently to distinct environmental cues.…”

Designing a Seasonal Acclimation Study Presents Challenges and Opportunities

“…Interestingly, freeze tolerance in the cricket Gryllus veletis requires shifts in both T b and photoperiod ( Toxopeus et al. 2019 ); and nymphal development in the cricket Modicogryllus siamensis depends on both photoperiod and temperatures pathways ( Miki et al. 2020 ).…”