Data from: Comparative genomics and transcriptomics in ants provide new insights into the evolution and function of odorant binding and chemosensory proteins

Background: The complex societies of ants and other social insects rely on sophisticated chemical communication. Two families of small soluble proteins, the odorant binding and chemosensory proteins (OBPs and CSPs), are believed to be important in insect chemosensation. To better understand the role of these proteins in ant olfaction, we examined their evolution and expression across the ants using phylogenetics and sex- and tissue-specific RNA-seq. Results: We find that subsets of both OBPs and CSPs are expressed in the antennae, contradicting the previous hypothesis that CSPs have replaced OBPs in ant olfaction. Both protein families have several highly conserved clades with a single ortholog in all eusocial hymenopterans, as well as clades with more dynamic evolution and many taxon-specific radiations. The dynamically evolving OBPs and CSPs have been hypothesized to function in chemical communication. Intriguingly, we find that seven members of the conserved clades are expressed specifically in the antennae of the clonal raider ant Cerapachys biroi, whereas only one dynamically evolving CSP is antenna specific. The orthologs of the conserved, antenna-specific C. biroi genes are also expressed in antennae of the ants Camponotus floridanus and Harpegnathos saltator, indicating that antenna-specific expression of these OBPs and CSPs is conserved across ants. Most members of the dynamically evolving clades in both protein families are expressed primarily in non-chemosensory tissues and thus likely do not fulfill chemosensory functions. Conclusions: Our results identify candidate OBPs and CSPs that are likely involved in conserved aspects of ant olfaction, and suggest that OBPs and CSPs may not rapidly evolve to recognize species-specific signals.

研究背景：蚂蚁与其他社会性昆虫的复杂社会体系，依赖精密的化学通讯系统。两类小型可溶性蛋白——气味结合蛋白（odorant binding proteins, OBPs）与化学感受蛋白（chemosensory proteins, CSPs）——被认为在昆虫化学感受过程中发挥关键作用。为深入解析这类蛋白在蚂蚁嗅觉系统中的作用，本研究通过系统发育分析、性别及组织特异性RNA-seq技术，全面探究了两类蛋白在蚂蚁类群中的演化与表达模式。
研究结果：本研究发现，OBPs与CSPs均有部分亚型在触角中表达，这与此前“蚂蚁嗅觉系统中CSPs已取代OBPs功能”的假说相悖。两类蛋白家族均包含多个高度保守的演化支：这些支系在所有真社会性膜翅目昆虫中仅存在单个直系同源基因；同时还存在演化动态性更强、存在大量类群特异性辐射演化的支系。此前有假说认为，这类演化动态性较强的OBPs与CSPs参与化学通讯过程。值得关注的是，本研究发现7个保守演化支的蛋白成员仅在克隆掠夺蚁（Cerapachys biroi）的触角中表达，而仅1个演化动态性较强的CSP呈现触角特异性表达。上述克隆掠夺蚁中保守且具触角特异性表达的基因，其直系同源基因在佛罗里达弓背蚁（Camponotus floridanus）与猎镰猛蚁（Harpegnathos saltator）的触角中同样存在表达，表明这类OBPs与CSPs的触角特异性表达模式在蚂蚁类群中具有保守性。两类蛋白家族中演化动态性较强的支系的多数成员，主要在非化学感受组织中表达，因此其大概率不承担化学感受相关功能。
研究结论：本研究筛选出了可能参与蚂蚁嗅觉保守通路的候选OBPs与CSPs，并提出OBPs与CSPs可能并不会快速演化以识别物种特异性信号。