期刊名称:Proceedings of the National Academy of Sciences
印刷版ISSN:0027-8424
电子版ISSN:1091-6490
出版年度:2016
卷号:113
期号:49
页码:14091-14096
DOI:10.1073/pnas.1610800113
语种:English
出版社:The National Academy of Sciences of the United States of America
摘要:SignificanceDespite the importance of sociality in the evolutionary history of life, its molecular basis is still poorly understood. The role of novel genes vs. conserved genes is particularly hotly debated. Here we present evidence that a group of 180 odorant receptor genes in the clonal raider ant are expressed in neurons that have been shown to detect cuticular hydrocarbons, one of the most important classes of ant chemical signals. We show that these genes underwent a period of rapid gene duplication in the ancestors of ants and now comprise 0.5%-1.5% of all genes in ant genomes. This discovery provides a striking example of the importance of novel genes in social evolution. A major aim of sociogenomic research is to uncover common principles in the molecular evolution of sociality. This endeavor has been hampered by the small number of specific genes currently known to function in social behavior. Here we provide several lines of evidence suggesting that ants have evolved a large and novel clade of odorant receptor (OR) genes to perceive hydrocarbon-based pheromones, arguably the most important signals in ant communication. This genomic expansion is also mirrored in the ant brain via a corresponding expansion of a specific cluster of glomeruli in the antennal lobe. We show that in the clonal raider ant, hydrocarbon-sensitive basiconic sensilla are found only on the ventral surface of the female antennal club. Correspondingly, nearly all genes in a clade of 180 ORs within the 9-exon subfamily of ORs are expressed exclusively in females and are highly enriched in expression in the ventral half of the antennal club. Furthermore, we found that across species and sexes, the number of 9-exon ORs expressed in antennae is tightly correlated with the number of glomeruli in the antennal lobe region innervated by odorant receptor neurons from basiconic sensilla. Evolutionary analyses show that this clade underwent a striking gene expansion in the ancestors of all ants and slower but continued expansion in extant ant lineages. This evidence suggests that ants have evolved a large clade of genes to support pheromone perception and that gene duplications have played an important role in the molecular evolution of ant communication.