Heat shock protein gene expression varies among populations but does not strongly track recent environmental conditions: implications for biomarker development

Global temperatures are rising, and scientists are mobilizing to uncover
which birds are most affected by the problem of heat. Heat shock proteins
(HSPs), for example, can shed light on this issue because they prevent
damage and promote recovery from heat. However, few studies have
investigated the relationship between HSPs and heat outside of
experimental contexts. Here, we ask whether natural variation in HSP gene
expression can serve as a biomarker of recent ambient conditions in wild
nestling tree swallows (Tachycineta bicolor). We focused on HSP90AA1
because this HSP increases mRNA abundance in avian blood after acute heat.
Using blood samples collected across ten degrees of latitude, we tested
for population differences in constitutive HSP90AA1 gene expression in
12-day-old nestlings. To quantify the specific time period over which
ambient conditions best predicted variation in HSP gene expression, we
used a climate window analysis, evaluating the predictive value of maximum
temperatures and maximum heat index in the hours and days from hatching
until sampling. We found a significant population difference in
constitutive HSP gene expression at the ends of our sampling range:
nestlings in South Carolina had nearly double the HSP90AA1 mRNA abundance
compared to nestlings in Massachusetts. There was no relationship between
HSP90AA1 and heat index at any time (hours or days), meaning that baseline
HSP gene expression is not a reliable biomarker for the combined effects
of heat and humidity, at least not when applying the heat index developed
for poultry. We found some evidence linking HSP90AA1 gene expression with
maximum temperatures three to four days before sampling; however, a
permutation test could not rule out the possibility of a false positive.
Thus, HSP90AA1 mRNA abundance is not necessarily an effective biomarker of
recent heat, and it may instead reflect other inherent population
differences. As heat waves intensify, this conclusion could change, and
other species could be more reactive to heat. We urge the avian biology
community to continue biomarker testing and better analytical tools for
estimating heat impacts on wild birds, as we seek to understand and
predict their persistence in the future.