Heat Shock Protein Expression is Upregulated after Acute Heat Exposure in Three Species of Australian Desert Birds

Abstract

Desert birds must cope with occasional and unpredictable heat waves, which are slowly becoming more frequent with climate change. Different orders of birds have different physiological and behavioural capacities that may aid survival during a heat wave. To date, the expression of genes related to heat exposure have not been studied across different bird orders. We hypothesised that acutely exposing native Australian birds whose natural habitat include arid environments to a high temperature (45 °C), similar to during a heat wave, would result in the upregulation of genes with protective effects against cell damage (BCL-2, VEGFA and heat shock proteins) and inflammation (interleukins), as well as the downregulation of genes involved in the coagulation pathway (fibrinogen). We used eight each of captive-bred Budgerigars (Melopsittacus undulatus), Zebra Finches (Taeniopygia guttata) and Diamond Doves (Geopelia cuneata). Four birds of each species were exposed to a temperature that was within the zone of thermal neutrality (35 °C), while the other four birds were exposed to a higher temperature (45 °C). The mRNA expression of selected genes were then measured using high-throughput qPCR platform (Fluidigm®, BioMark™). The results supported the hypothesis that acute exposure to a high temperature would result in the upregulation of heat shock protein (HSP) genes, but there was no significant upregulation of other genes with protective effects against cell damage nor genes associated with inflammation. The results also do not support the hypothesis that acute heat exposure would result in downregulation of the genes involved in the coagulation pathway in these birds. Among all the tissues that were analysed, the gastrointestinal tissue had the highest number of upregulated HSP genes, possibly indicating that this tissue requires the most protection to continue functioning. Diamond Dove organs also had the highest number of HSP genes upregulated, possibly a reflection of their ability to better protect their cells at high temperatures.

The Physiology of Heat Tolerance in Small Endotherms

“…for its wide range of functions in normal and abnormal environments (39). In both birds and mammals, heat exposure induces the expression of a number of HSP families (HSP 25, HSP 60, HSP 70, HSP 90) (60,147). HSPs are believed to act by preventing protein denaturation or by processing protein fragments and unfolded proteins (88, 109a).…”

“…HSPs are believed to act by preventing protein denaturation or by processing protein fragments and unfolded proteins (88, 109a). In addition to HSPs, the upregulation of genes such as BCL-2 and VEGFA may also provide protection, and the upregulation of interleukins may affect the inflammatory responses associated with heat exposure (147). The downregulation of genes such as those associated with coagulation pathways (fibrinogen) may also benefit animals during extreme heat exposure.…”

Extreme hyperthermia tolerance in the world’s most abundant wild bird

“…Moreover, they identify red-billed queleas as a model for future studies of the physiological and molecular bases of extreme hyperthermia tolerance. We speculate that this species' ability to tolerate T b as high as 48-49 °C arises from an array of anatomical and molecular mechanisms, including a well-developed rete opthalmicum to maintain brain temperature well below core T b [46][47][48] and pronounced heat shock protein expression 44,49 . Understanding the processes underlying the queleas' ability to tolerate T b values lethal to other endotherms may, we suspect, prove useful for biotechnology aimed at developing greater heat tolerance in birds and other organisms.…”

“…That desert birds apparently lack the ability to tolerate comparably high body temperatures, despite strong selection for water conservation 43 , suggests there are substantial costs to such extreme hyperthermia tolerance. These costs could potentially be related the synthesis of heat shock proteins (HSPs) and interactions with stress responses via the modification of glucocorticoid receptor function 9,44 .…”

From climate warming to accelerated cellular ageing: an experimental study in wild birds

“…2°C increase in temperature might be too low to induce oxidative stress or a heat shock response (compared to heat stress experiments in the lab that often use > +10°C; e.g. [37]). Yet, the gene expression of the glucocorticoid receptor nr3c1 was increased in heated nests, suggesting either a response to a stressful stimulus (e.g.…”