Changes in Energy Reserves and Gene Expression Elicited by Freezing and Supercooling in the Antarctic Midge, Belgica antarctica

Abstract

Freeze-tolerance, or the ability to survive internal ice formation, is relatively rare among insects. Larvae of the Antarctic midge Belgica antarctica are freeze-tolerant year-round, but in dry environments, the larvae can remain supercooled (i.e., unfrozen) at subzero temperatures. In previous work with summer-acclimatized larvae, we showed that freezing is considerably more stressful than remaining supercooled. Here, these findings are extended by comparing survival, tissue damage, energetic costs, and stress gene expression in larvae that have undergone an artificial winter acclimation regime and are either frozen or supercooled at −5 °C. In contrast to summer larvae, winter larvae survive at −5 °C equally well for up to 14 days, whether frozen or supercooled, and there is no tissue damage at these conditions. In subsequent experiments, we measured energy stores and stress gene expression following cold exposure at −5 °C for either 24 h or 14 days, with and without a 12 h recovery period. We observed slight energetic costs to freezing, as frozen larvae tended to have lower glycogen stores across all groups. In addition, the abundance of two heat shock protein transcripts, hsp60 and hsp90, tended to be higher in frozen larvae, indicating higher levels of protein damage following freezing. Together, these results indicate a slight cost to being frozen relative to remaining supercooled, which may have implications for the selection of hibernacula and responses to climate change.

Surviving the Antarctic Winter—Life Stage Cold Tolerance and Ice Entrapment Survival in The Invasive Chironomid Midge Eretmoptera murphyi

“…The physiological mechanisms involved in E. murphyi cold tolerance are likely to be governed by similar mechanisms to that of B. Antarctica, which has recently been found to draw heavily on glycogen reserves in response to cold exposures [67]. The resulting glucose mobilization is well documented to act as a cryoprotectant and aid cold tolerance [68]. Lipids may also play a role, with these reserves drawn on during repeated cold exposures by B. Antarctica [69].…”

Belgica antarctica (Diptera: Chironomidae): A natural model organism for extreme environments

“…Rather, the larvae can tolerate controlled ice formation in extracellular fluids (Baust & Lee, 1987) and survive temperatures as low as −20°С in this state (Teets et al, 2008;Teets & Denlinger, 2014). While winter-acclimated larvae survive freezing and supercooling equally well, freezing results in slightly greater energetic costs and elevated expression of certain heat shock proteins (Teets et al, 2020). Freezing tolerance varies seasonally, with larvae collected during summer dying at higher temperatures on average (−6°С) than those collected in winter (−12°С) (Lee et al, 2006).…”

Gene family expansions in Antarctic winged midge as a strategy for adaptation to cold environments

“…As a result, Antarctic terrestrial biodiversity is low and ecosystems restricted to low-altitude coastal regions of the Antarctic Peninsula, where seasonal snowmelt occurs 1 , 2 . Among the estimated 5.5 million species of insects worldwide 3 , only three species, Belgica antarctica , Eretmoptera murphyi , and Parochlus steinenii, have been recorded in the maritime Antarctic region 4 . These species belong to the family Chironomidae and overwinter in their larval stage.…”