Genome-Wide Comparative Analysis of Chemosensory Gene Families in Five Tsetse Fly Species

For decades, odour-baited traps have been used for control of tsetse flies (Diptera; Glossinidae), vectors of African trypanosomes. However, differential responses to known attractants have been reported in different Glossina species, hindering establishment of a universal vector control tool. Availability of full genome sequences of five Glossina species offers an opportunity to compare their chemosensory repertoire and enhance our understanding of their biology in relation to chemosensation. Here, we identified and annotated the major chemosensory gene families in Glossina. We identified a total of 118, 115, 124, and 123 chemosensory genes in Glossina austeni, G. brevipalpis, G. f. fuscipes, G. pallidipes, respectively, relative to 127 reported in G. m. morsitans. Our results show that tsetse fly genomes have fewer chemosensory genes when compared to other dipterans such as Musca domestica (n>393), Drosophila melanogaster (n = 246) and Anopheles gambiae (n>247). We also found that Glossina chemosensory genes are dispersed across distantly located scaffolds in their respective genomes, in contrast to other insects like D. melanogaster whose genes occur in clusters. Further, Glossina appears to be devoid of sugar receptors and to have expanded CO2 associated receptors, potentially reflecting Glossina's obligate hematophagy and the need to detect hosts that may be out of sight. We also identified, in all species, homologs of Ir84a; a Drosophila-specific ionotropic receptor that promotes male courtship suggesting that this is a conserved trait in tsetse flies. Notably, our selection analysis revealed that a total of four gene loci (Gr21a, GluRIIA, Gr28b, and Obp83a) were under positive selection, which confers fitness advantage to species. These findings provide a platform for studies to further define the language of communication of tsetse with their environment, and influence development of novel approaches for control.

数十年来，气味诱捕器（odour-baited traps）一直被用于防控舌蝇（双翅目Diptera；舌蝇科Glossinidae）——非洲锥虫（African trypanosomes）的传播媒介。然而，不同舌蝇物种对已知引诱剂的响应存在差异化，这阻碍了通用媒介防控工具的研发。五份舌蝇物种的全基因组序列数据的公开，为比较它们的化学感受基因库、深化对其化学感受相关生物学特性的认知提供了契机。本研究鉴定并注释了舌蝇中的主要化学感受基因家族：相较于已在莫氏舌蝇莫氏亚种（G. m. morsitans）中报道的127个基因，我们分别在奥氏舌蝇（Glossina austeni）、短须舌蝇（G. brevipalpis）、棕舌蝇指名亚种（G. f. fuscipes）、淡足舌蝇（G. pallidipes）中鉴定出118、115、124和123个化学感受基因。研究结果显示，与家蝇（Musca domestica，n>393）、黑腹果蝇（Drosophila melanogaster，n=246）、冈比亚按蚊（Anopheles gambiae，n>247）等其他双翅目昆虫相比，舌蝇基因组中的化学感受基因数量更少。此外，与黑腹果蝇等化学感受基因呈簇状分布的昆虫不同，舌蝇的化学感受基因分散在各自基因组中彼此相距较远的基因组支架序列（scaffolds）上。进一步分析发现，舌蝇似乎缺乏糖受体（sugar receptors），且拥有扩增的二氧化碳相关受体（CO2 associated receptors），这可能与舌蝇的专性吸血习性（obligate hematophagy）以及其需要探测视野之外宿主的生存需求相契合。我们还在所有物种中鉴定出了离子型受体Ir84a（ionotropic receptor Ir84a）的同源基因——该受体为黑腹果蝇所特有，可促进雄性求偶行为，这表明该特征在舌蝇中具有保守性。值得注意的是，选择压力分析显示，共有4个基因位点（Gr21a、GluRIIA、Gr28b和Obp83a）受到正选择（positive selection），这为物种赋予了适合度优势（fitness advantage）。这些研究结果为进一步解析舌蝇与环境的交流语言提供了研究平台，也将推动新型防控方法的研发。