Genomic and transcriptomic analyses of a social hemipteran provide new insights into insect sociality

Abstract

The origin of sociality represents one of the most important evolutionary transitions. Insect sociality evolved in some hemipteran aphids, which can produce soldiers and normal nymphs with distinct morphology and behaviour through parthenogenesis. The lack of genomic data resources has hindered the investigations into molecular mechanisms underlying their social evolution. Herein, we generated the first chromosomal-level genome of a social hemipteran (Pseudoregma bambucicola) with highly specialized soldiers and performed comparative genomic and transcriptomic analyses to elucidate the molecular signatures and regulatory mechanisms of caste differentiation. P. bambucicola has a larger known aphid genome of 582.2 Mb with an N50 length of 11.24 Mb, and about 99.6% of the assembly was anchored to six chromosomes with a scaffold N50 of 98.27 Mb. A total of 14,027 protein-coding genes were predicted and 37.33% of the assembly were identified as repeat sequences. The social evolution is accompanied by a variety of changes in genome organization, including expansion of gene families related to transcription factors, transposable elements, as well as species-specific expansions of certain sugar transporters and UGPases involved in carbohydrate metabolism. We also characterized large candidate gene sets linked to caste differentiation and found evidence of expression regulation and positive selection acting on energy metabolism and muscle structure, explaining the soldier-specific traits including morphological and behavioural specialization, developmental arrest and infertility. Overall, this study offers new insights into the molecular basis of social aphids and the evolution of insect sociality and also provides valuable data resources for further comparative and functional studies.