Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates

Gene duplications can have a major role in adaptation, and gene families underlying chemosensation are particularly interesting due to their essential role in chemical recognition of mates, predators and food resources. Social insects add yet another dimension to the study of chemosensory genomics, as the key components of their social life rely on chemical communication. Still, chemosensory gene families are little studied in social insects. Here we annotated chemosensory protein (CSP) genes from seven ant genomes and studied their evolution. The number of functional CSP genes ranges from 11 to 21 depending on species, and the estimated rates of gene birth and death indicate high turnover of genes. Ant CSP genes include seven conservative orthologous groups present in all the ants, and a group of genes that has expanded independently in different ant lineages. Interestingly, the expanded group of genes has a differing mode of evolution from the orthologous groups. The expanded group shows rapid evolution as indicated by a high dN/dS (nonsynonymous to synonymous changes) ratio, several sites under positive selection and many pseudogenes, whereas the genes in the seven orthologous groups evolve slowly under purifying selection and include only one pseudogene. These results show that adaptive changes have played a role in ant CSP evolution. The expanded group of ant-specific genes is phylogenetically close to a conservative orthologous group CSP7, which includes genes known to be involved in ant nestmate recognition, raising an interesting possibility that the expanded CSPs function in ant chemical communication.

基因重复在物种适应进程中发挥关键作用，而化学感知相关基因家族因其在配偶、天敌与食物资源的化学识别中具备核心功能，格外受到学界关注。社会性昆虫为化学感受基因组学研究提供了全新维度，因其社会生活的核心环节均依赖化学通讯完成，但目前针对社会性昆虫的化学感受基因家族的研究仍较为匮乏。本研究对7种蚂蚁基因组中的化学感受蛋白（chemosensory protein, CSP）基因进行了注释，并分析其演化历程。不同蚂蚁物种的功能性CSP基因数量介于11至21之间，基因新生与丢失的估算速率显示其基因周转速率较高。蚂蚁的CSP基因包含7个在所有蚂蚁类群中均存在的保守直系同源组，以及一类在不同蚂蚁演化支系中独立发生扩张的基因簇。值得注意的是，该扩张基因簇的演化模式与各保守直系同源组存在显著差异：其dN/dS（非同义替换与同义替换速率比值）较高，存在多个受正选择作用的位点，且伴随大量假基因；而7个保守直系同源组的基因则在纯化选择压力下缓慢演化，仅含1个假基因。上述结果表明，适应性改变在蚂蚁CSP基因的演化过程中发挥了重要作用。这类蚂蚁特异性的扩张基因簇，在系统发育上与保守直系同源组CSP7亲缘关系紧密——CSP7组包含已知参与蚂蚁巢友识别的基因，这提示扩张的CSP基因可能在蚂蚁的化学通讯中发挥功能，该推论颇具研究价值。