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

Abstract

BackgroundThe 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.ResultsWe 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0573-0) contains supplementary material, which is available to authorized users.

Proteome stability, heat hardening, and heat-shock protein expression profiles in Cataglyphis desert ants

“…For those that have, HSP70 synthesis has largely been the focus (Gehring and Wehner, 1995;Maisov et al, 2007). However, Nguyen et al (2016) recently showed that the primary inducible gene involved in HSR in Drosophila -hsp70 -has been completely lost in Hymenoptera, which instead employs two hsc70-4 paralogues. Like Gehring and Wehner (1995), we found that HSC70 is constitutively expressed in C. bombycina.…”

“…The second study investigated hsp60, hsp75 and hsp90 expression in response to temperature in the wood ant Formica cinerea and found no significant effects (Ślipinśki et al, 2015). The third study compared heat-shock-related expression patterns of several hsp genes between Pogonomyrmex barbatus, an ant living in hot and arid climates, and Aphaenogaster picea, an ant living in cool woodlands (Nguyen et al, 2016). These authors showed that expression of hsc70-4, hsp83 and hsp40 was upregulated in response to heat stress and the species differed significantly in relative expression levels.…”

“…Ultimately, proteins of thermophiles are more stable than those of mesophiles, whether as a result of structural changes or as a consequence of large amounts of constitutive HSPs (Evgen'ev et al, 2014). It has been shown that both the duplication of hsp genes and shifts in HSE arrangement and position allow for greater HSR functional plasticity, helping organisms adopt the bestsuited response to environmental heat stress (Bettencourt and Feder, 2001;Tian et al, 2010;Nguyen et al, 2016). The use of this system is well developed in ectotherms, which cannot regulate their body temperatures and whose metabolic processes and stability therefore depend on microclimatic conditions (Hazel, 1995;Lin and Somero, 1995;Willmer et al, 2000).…”

“…Previous studies have shown that foragers of the Saharan silver ant, Cataglyphis bombycina, produce what was thought to be HSP70 before emerging from the nest, thereby bypassing the need to acclimate to sudden heat exposure (Gehring and Wehner, 1995). However, more recently, it was discovered that the primary heat-induced gene hsp70 has been completely lost in Hymenoptera; instead, two hsc70-4 paralogues are expressed (Nguyen et al, 2016). At present, the ability to express other HSPs and to induce gene expression in response to heat stress remains completely unexplored in Cataglyphis.…”

“…Third, we compared the levels of constitutively expressed HSC70 between the two species. Fourth, we characterised the induced expression of several hsp genes -hsf1, hsc70-4h, hsp83 and hsc70-5 -known to be associated with HSR, heat tolerance and protein folding (Sarge et al, 1993;Feder and Hofmann, 1999;Nguyen et al, 2016). Based on current knowledge regarding the molecular mechanisms underlying adaptations to extreme environments (Evgen'ev et al, 2014), we predicted that the more thermophilic species, C. bombycina, would constitutively express molecular chaperones at higher levels than would the more mesophilic species, C. mauritanica.…”