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

Abstract

High temperatures can negatively impact the performance and survival of organisms, particularly ectotherms. While an organism's response to high temperature stress clearly depends on current thermal conditions, its response may also be affected by the temporal pattern and duration of past temperature exposures. We used RNA sequencing of Manduca sexta larvae fat body tissue to evaluate how diurnal temperature fluctuations during development affected gene expression both independently and in conjunction with subsequent heat stress. Additionally, we compared gene expression between two M. sexta populations, a lab colony and a genetically related field population that have been separated for >300 generations and differ in their thermal sensitivities. Lab-adapted larvae were predicted to show increased expression responses to both single and repeated thermal stress, whereas recurrent exposure could decrease later stress responses for field individuals. We found large differences in overall gene expression patterns between the two populations across all treatments, as well as population-specific transcriptomic responses to temperature; more differentially expressed genes were upregulated in the field compared with lab larvae. Developmental temperature fluctuations alone had minimal effects on long-term gene expression patterns, with the exception of a somewhat elevated stress response in the lab population. Fluctuating rearing conditions did alter gene expression during exposure to later heat stress, but this effect depended on both the population and the particular temperature conditions. This study contributes to increased knowledge of molecular mechanisms underlying physiological responses of organisms to temperature fluctuations, which is needed for the development of more accurate thermal performance models.

Growth, stress, and acclimation responses to fluctuating temperatures in field and domesticated populations of Manduca sexta

“…In contrast, patterns of HSP gene expression in response to heat shocks are similar in the two populations (Alston et al, 2020).…”

“…This is consistent with the finding that larval survival at high, constant temperatures (35°C) is lower in the laboratory than the field population (Kingsolver & Nagle, 2007). In contrast, patterns of HSP gene expression in response to heat shocks are similar in the two populations (Alston et al., 2020).…”

The interactive effects of heat stress, parasitism and host plant quality in a host–parasitoid system

“…In this system, a lethal threshold for one interacting organism (the parasitoid wasp) triggers a different developmental outcome for another organism (the caterpillar). This concept relates back to individual variability when considering research regarding thermal acclimation and tolerance, where previous thermal history can change individual responses to stressful temperatures (Alston et al., 2020; Kingsolver et al., 2015; Marshall & Sinclair, 2012; Sinclair et al., 2003). While all caterpillars in this study experienced the same thermal conditions within treatment groups, the caterpillars' parental identity is unknown.…”

Behavioral thermoregulation of caterpillars is altered by temperature, but not parasitism: An empirical field study

“…We found that the black weed barrier treatment significantly increased the daily maximum T op seen in the middle of the tobacco plants when compared to the gray weed barrier treatment (post hoc Student's t test, t = −2.831, df = 209.73, p = 0.0051; Figure 1B; Appendix S2: Table S1 and Figure S6A,D). T op in the middle of the plant was consistently 1 C-3 C higher in the black weed barrier treatment than the gray (Figure 1B), a difference that can have important sublethal effects at high temperatures (Alston et al, 2020;Kingsolver et al, 2015;Ma et al, 2018). By contrast, daily minimum temperatures were similar in the two treatments, because of the lack of solar radiative heat differences during the night (LM, F 1,416 = 0.03, p = 0.8677; Figure 1D-F; Appendix S2: Table S1 and Figure S6B,E).…”

“…Of particular interest to thermal biologists in recent years are the sublethal effects of high temperatures. For ectothermic organisms, even short exposures to temperatures near their upper thermal limit can have cascading physiological effects such as reduced feeding and growth, reduced movement, reduced fecundity, upregulation of heat shock proteins, and more (Alston et al, 2020; Kingsolver et al, 2015; Ma et al, 2018). If hosts and parasites differ in their thermal sensitivity or tolerance, increasing temperatures can change the dynamics or even the outcomes of species interactions (Furlong & Zalucki, 2017; Schreven et al, 2017).…”