Data from: The evolution of heat shock protein sequences, cis-regulatory elements, and expression profiles in the eusocial Hymenoptera

Background: The eusocial Hymenoptera have radiated across a wide range of
thermal environments, exposing them to significant physiological
stressors. We reconstructed the evolutionary history of three families of
Heat Shock Proteins (Hsp90, Hsp70, Hsp40), the primary molecular
chaperones protecting against thermal damage, across 12 Hymenopteran
species and four other insect orders. We also predicted and tested for
thermal inducibility of eight Hsps from the presence of cis-regulatory
heat shock elements (HSEs). We tested whether Hsp induction patterns in
ants were associated with different thermal environments. Results: We
found evidence for duplications, losses, and cis-regulatory changes in two
of the three gene families. One member of the Hsp90 gene family, hsp83,
duplicated basally in the Hymenoptera, with shifts in HSE motifs in the
novel copy. Both copies were retained in bees, but ants retained only the
novel HSE copy. For Hsp70, Hymenoptera lack the primary heat-inducible
orthologue from Drosophila melanogaster and instead induce the cognate
form, hsc70-4, which also underwent an early duplication. Episodic
diversifying selection was detected along the branch predating the
duplication of hsc70-4 and continued along one of the paralogue branches
after duplication. Four out of eight Hsp genes were heat-inducible and
matched the predictions based on presence of conserved HSEs. For the
inducible homologues, the more thermally tolerant species, Pogonomyrmex
barbatus, had greater Hsp basal expression and induction in response to
heat stress than did the less thermally tolerant species, Aphaenogaster
picea. Furthermore, there was no trade-off between basal expression and
induction. Conclusions: Our results highlight the unique evolutionary
history of Hsps in eusocial Hymenoptera, which has been shaped by gains,
losses, and changes in cis-regulation. Ants, and most likely other
Hymenoptera, utilize lineage-specific heat inducible Hsps, whose
expression patterns are associated with adaptive variation in thermal
tolerance between two ant species. Collectively, our analyses suggest that
Hsp sequence and expression patterns may reflect the forces of selection
acting on thermal tolerance in ants and other social Hymenoptera.