Effects of adult temperature on gene expression in a butterfly: identifying pathways associated with thermal acclimation

Abstract

BackgroundPhenotypic plasticity is a pervasive property of all organisms and considered to be of key importance for dealing with environmental variation. Plastic responses to temperature, which is one of the most important ecological factors, have received much attention over recent decades. A recurrent pattern of temperature-induced adaptive plasticity includes increased heat tolerance after exposure to warmer temperatures and increased cold tolerance after exposure to cooler temperatures. However, the mechanisms underlying these plastic responses are hitherto not well understood. Therefore, we here investigate effects of adult acclimation on gene expression in the tropical butterfly Bicyclus anynana, using an RNAseq approach.ResultsWe show that several antioxidant markers (e.g. peroxidase, cytochrome P450) were up-regulated at a higher temperature compared with a lower adult temperature, which might play an important role in the acclamatory responses subsequently providing increased heat tolerance. Furthermore, several metabolic pathways were up-regulated at the higher temperature, likely reflecting increased metabolic rates. In contrast, we found no evidence for a decisive role of the heat shock response.ConclusionsAlthough the important role of antioxidant defence mechanisms in alleviating detrimental effects of oxidative stress is firmly established, we speculate that its potentially important role in mediating heat tolerance and survival under stress has been underestimated thus far and thus deserves more attention.Electronic supplementary materialThe online version of this article (10.1186/s12862-019-1362-y) contains supplementary material, which is available to authorized users.

Clinal variation in investment into reproduction versus maintenance suggests a ‘pace-of-life’ syndrome in a widespread butterfly

“…Plastic responses to environmental change entail a large number of relatively fast physiological mechanisms. In response to thermally challenging conditions, two mechanisms seem to be of particular importance, antioxidant defence mechanisms and the heat shock response (Sørensen et al 2003 ; Zhang et al 2015 ; Franke et al 2019 ). High temperatures generally increase the production of reactive oxygen species (ROS), a by-product of the aerobic metabolism, which act on organic substrates and may induce oxidative damage.…”

The ghost of temperature past: interactive effects of previous and current thermal conditions on gene expression in Manduca sexta

“…Expression patterns of other genes including those involved in metabolism, antioxidant production, transport activity, immune response and transcription also appear to be strongly altered by short-term heat stress (Colinet et al, 2013;Cui et al, 2019;DeBiasse and Kelly, 2016;Franke et al, 2019;Gleason and Burton, 2015;López-Maury et al, 2008;Schoville et al, 2012;Sørensen et al, 2005;Vihervaara et al, 2018). Similar pathways may also be involved in longer-term acclimation under constant temperatures (Metzger and Schulte, 2018).…”

Genome‐wide gene expression profiles of the pea aphid (Acyrthosiphon pisum) under cold temperatures provide insights into body color variation

“…Cold tolerance is a critical environmental factor determining the distribution and population abundance of insects (Fischer & Karl, 2010; Franke et al, 2019; Laiolo & Obeso, 2015; Overgaard & MacMillan, 2017; Plantamp et al, 2019; Stoks et al, 2014). The adaptation and acclimation responses in insects to low temperatures are multifactorial and involve several physiological systems, biochemical adjustments, and a complex combination of changes in gene expression regulation (Laiolo & Obeso, 2015; Liu et al, 2020; Spranghers et al, 2017; Teets et al, 2012).…”

“…Despite the fact that the metabolic activity of insects is relatively low when facing cold conditions, their metabolic processes (e.g., energy, lipid, and sugar metabolisms) are still active (Monika et al, 2012). Gene expression studies of many insect species have identified several genes related to cold tolerance (Dunning et al, 2014; Franke et al, 2019; Wang et al, 2014; Zhang et al, 2015). Frost ( Fst ) is a candidate gene associated with the response to hypothermic stress in adult Drosophila melanogaster (Udaka et al, 2013).…”