Preservation of reproductive behaviors during modest cooling: rapid cold-hardening fine-tunes organismal response

Abstract

SUMMARY The primary objectives of this study were to determine (1) whether rapid cold-hardening (RCH) preserves reproductive behaviors during modest cooling,(2) whether increased mating success at a lower temperature comes at the cost of decreased performance at a higher temperature and (3) whether RCH is associated with an elevated metabolic rate. Drosophila melanogaster(Diptera: Drosphilidae) were rapidly cold-hardened by a 2-h exposure to 16°C prior to experiments. A temperature decrease of only 7°C(23°C to 16°C) prevented half (11/22) of the control pairs of D. melanogaster from engaging in any courtship activity. By contrast, most RCH pairs courted (17/20). Additionally, the 7°C transfer prevented mating in every pair of control flies, whereas more than half (11/20) of the RCH pairs mated. There was no evidence of impaired courtship or mating performance when RCH pairs were tested at 23°C. Finally, RCH is apparently not an energy-demanding process because no increase in the metabolic rate was detected during its induction. Overall, these data demonstrate that RCH serves to constantly fine-tune an insect's physiological state to match slight changes in environmental temperature. Furthermore, the RCH response is not restricted to cryoprotection and survival in the cold but also preserves more subtle behaviors, such as courtship, at moderate to high temperatures throughout the year.

Histamine and Its Receptors Modulate Temperature-Preference Behaviors inDrosophila

“…Drosophila showed an increase in cold tolerance and a decrease in hot tolerance when there are defects in histamine function. This coincides with previous reports that resetting the lower thermal limit may come at the expense of a corresponding decrease in the upper thermal limit (Bale, 2002;Shreve et al, 2004).…”

“…Drosophila strains with mutations in these genes showed abnormal temperature preferences. Furthermore, we found that these genes are essential in determin-ing critical thermal limits (insects enter a state of coma when they go beyond this temperature limit) (Shreve et al, 2004). Moreover, expression of these genes was detected in various regions of the brain, further supporting their critical roles.…”

“…These thermal limits (torpor occurs at or beyond these temperatures) or "critical thermal limits" can be adjusted or reset according to accommodated environmental or physiological conditions (Kelty and Lee, 1999; for review, see Bale, 2002;Shreve et al, 2004). Given that changes in temperature preference occur in the range of critical thermal limits (Hedgecock and Russell, 1975), it is possible that the mechanism causing changes of temperature preference might also adjust the range of critical thermal limits at the same time (or in parallel).…”

Responses of invertebrates to temperature and water stress: A polar perspective

“…Drosophila melanogaster, courting and reproduction were 35 and 55% greater at 16 o C, respectively, 286 following RCH (Shreve et al 2004). Further sub-lethal improvements have included the maintenance 287 of the proboscis extension reflex and grooming behaviour in flesh flies (Kelty et al 1996), the 288 preservation of learning and spatial conditioning (Kim et al 2005), and the sustenance of flight 289 (Larsen and Lee 1994).…”

CRISPR-induced null alleles show that Frost protects Drosophila melanogaster reproduction after cold exposure

“…Cold tolerance of D. melanogaster is plastic: variation among natural populations indicates evolutionary adaptation (Hoffmann et al, 2001); acclimation responses improve cold tolerance over a period of days (Watson and Hoffmann, 1996); and rapid cold-hardening (RCH) improves tolerance response after a brief exposure to cold (Czajka and Lee, 1990). This RCH also preserves reproductive behavior (Shreve et al, 2004). The molecular underpinnings of Drosophila cold tolerance have been explored extensively via microarrays (Qin et al, 2005;Zhang et al, 2011), quantitative trait loci (QTL) (Morgan and Mackay, 2006;Gerken et al, 2015), RNA sequencing (MacMillan et al, 2016) and proteomics (Sørensen et al, 2017), yet surprisingly few genes are consistently upregulated or associated with low temperatures.…”