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.

背景：真社会性膜翅目（eusocial Hymenoptera）已辐射演化至多样的热环境中，使其面临显著的生理胁迫压力。本研究针对12种膜翅目物种及其他4个昆虫目，重构了三类主要的抗热损伤分子伴侣——热休克蛋白（Heat Shock Proteins, Hsp90、Hsp70、Hsp40）的进化历史。同时，我们基于顺式调控热休克元件（cis-regulatory heat shock elements, HSEs）的存在情况，预测并验证了8个Hsp基因的热诱导特性，并检验了蚂蚁体内的Hsp诱导模式是否与不同热环境存在关联。
结果：我们在三类基因家族中的两类中发现了基因重复、丢失及顺式调控变异的证据。Hsp90家族的hsp83基因在膜翅目基部类群发生了重复，其新产生的拷贝的HSE基序发生了变异。蜜蜂类群保留了两个拷贝，而蚂蚁仅保留了携带新型HSE的拷贝。对于Hsp70家族，膜翅目缺失黑腹果蝇（Drosophila melanogaster）的主要热诱导直系同源基因，转而诱导组成型同源蛋白hsc70-4，该基因同样经历了早期重复事件。在hsc70-4基因重复事件发生前的分支上检测到了间歇式多样化选择，且该选择在重复后其中一条旁系同源分支上持续存在。8个Hsp基因中有4个具有热诱导性，且其诱导特性与基于保守HSE存在情况做出的预测相符。对于具有热诱导性的同源基因，耐热性更强的红收获蚁（Pogonomyrmex barbatus）在热胁迫下的Hsp基础表达水平与诱导幅度均高于耐热性较弱的黑凹头蚁（Aphaenogaster picea）。此外，Hsp的基础表达与诱导水平之间未出现权衡关系。
结论：本研究结果揭示了真社会性膜翅目Hsp基因独特的演化历史，其演化历程受基因获得、丢失及顺式调控变化共同塑造。蚂蚁以及极有可能的其他膜翅目物种，均采用谱系特异性的热诱导型Hsp，其表达模式与两种蚂蚁间耐热性的适应性变异相关联。综上，我们的分析表明，Hsp的序列与表达模式或许反映了作用于蚂蚁及其他社会性膜翅目耐热性的选择压力。