Shin G. Goto

Maternal perception of environmental conditions can direct offspring developmental trajectories, providing adaptive flexibility across taxa. In the band-legged ground cricket Dianemobius nigrofasciatus, maternal exposure to short days induces embryonic diapause at the cellular blastoderm stage in offspring. Here, we investigate molecular mechanisms underlying this transgenerational adaptation through genome assembly (1.45 Gbp) and a time-series transcriptomic analysis of diapause and non-diapause eggs from 12 to 72 hours post-oviposition. Despite morphological similarity, diapause-destined eggs show early upregulation of ATP-dependent chromatin remodeling genes at 24 hours. ATAC-seq reveals reduced chromatin accessibility at neural and cell cycle-related genes. Time-series clustering identifies precocious shifts in RNA processing machinery (peaking at 24 versus 40 hours in non-diapause eggs), followed by metabolic regulation toward amino acid catabolism and gluconeogenesis sustaining long-term survival during developmental arrest. Our findings reveal diapause as actively coordinated molecular programming involving epigenetic, transcriptional, and metabolic remodeling, providing insights into transgenerational environmental adaptation.

Maternal perception of environmental conditions can direct offspring developmental trajectories, providing adaptive flexibility across taxa. In the band-legged ground cricket Dianemobius nigrofasciatus , maternal exposure to short days induces embryonic diapause at the cellular blastoderm stage in offspring. Here, we investigate molecular mechanisms underlying this transgenerational adaptation through genome assembly (1.45 Gbp) and time-series transcriptomic analyses of diapause and non-diapause eggs from 12 to 72 hours post-oviposition. Despite morphological similarity, diapause-destined eggs show early upregulation of ATP-dependent chromatin remodeling genes at 24 hours. ATAC-seq reveals reduced chromatin accessibility at neural and cell cycle-related genes. Time-series clustering identifies precocious shifts in RNA processing machinery (peaking at 24 versus 40 hours in non-diapause eggs), followed by metabolic regulation toward amino acid catabolism and gluconeogenesis sustaining long-term survival during developmental arrest. Our findings reveal diapause as actively coordinated molecular programming involving epigenetic, transcriptional, and metabolic remodeling, providing insights into transgenerational environmental adaptation.

The Antarctic midge, Belgica antarctica, is a unique insect endemic to Antarctica. It has a 2-year life cycle, with larvae overwintering in two different instars and adults emerging the following summer. This seasonality is crucial for adaptation to Antarctica’s harsh climates and ephemeral growing seasons; however, the underlying mechanisms remain unclear. We found that, under summer-like conditions, larvae could develop from egg to the fourth-instar larval stage without interruption, but they never pupated. Spontaneous developmental arrest at this stage suggests that they overwinter in obligate diapause, a genetically determined period of dormancy. The winter cold can terminate this diapause, and long-term cold exposure is more effective. Although this species can utilise two alternative cold tolerance strategies with diapause for overwintering, freezing was more successful than cryoprotective dehydration in allowing survival and developmental resumption in our experimental conditions. In contrast, the first three larval instars continued their development under the same conditions as the fourth-instar larvae. Although we do not exclude the possibility of facultative diapause, they likely overwinter in a quiescent state, an immediate developmental arrest in response to adversity, to maximise exploitation of the short Antarctic summer. Diapause and quiescence ensure developmental and reproductive success in this extremophile insect.

Larvae of the flesh fly, Sarcophaga similis exhibit photoperiodic responses to control pupal diapause. Although the external coincidence model is applicable to S. similis photoperiodism, it remains unknown how the circadian clock system integrates day-length information. To explore the mechanisms, we examined the neural circuitry involving circadian clock lateral neurons (LNs) and prothoracicotropic hormone (PTTH) neurons. We also examined the photoperiodic effects on LN-fiber patterns in third-instar S. similis larvae. Immunohistochemistry showed that the clock protein PERIOD and the neuropeptide pigment-dispersing factor (PDF) were co-localized in four cells per brain hemisphere, and we named these PDF-LNs of S. similis. Single-cell polymerase chain reaction of backfilled neurons from the ring gland showed that two pairs of pars lateralis neurons with contralateral axons (PL-c neurons) to the ring gland expressed ptth. Double labeling with immunohistochemistry and backfills revealed that PDF-immunoreactive varicose fibers projected close to fibers from PL-c neurons. short neuropeptide f (snpf) receptor and glutamate-gated chloride channel but not pdf receptor were expressed in PL-c neurons. sNPF and L-glutamate but not PDF acutely inhibited the spontaneous firing activity of PL-c neurons. The number of PDF-immunoreactive varicosities of PDF-LNs in the dorsal protocerebrum was significantly higher under short-day than that under long-day conditions in a time-dependent manner. These results suggest that sNPF and/or glutamate signaling to PTTH neurons and PDF-LNs form a potential neural circuity for the photoperiodic control of pupal diapause and that photoperiod modifies the connectivity strength between PDF-LNs and their post- or pre-neurons in the circuitry.