Genomic Features of the Damselfly Calopteryx splendens Representing a Sister Clade to Most Insect Orders

Abstract

Insects comprise the most diverse and successful animal group with over one million described species that are found in almost every terrestrial and limnic habitat, with many being used as important models in genetics, ecology, and evolutionary research. Genome sequencing projects have greatly expanded the sampling of species from many insect orders, but genomic resources for species of certain insect lineages have remained relatively limited to date. To address this paucity, we sequenced the genome of the banded demoiselle, Calopteryx splendens, a damselfly (Odonata: Zygoptera) belonging to Palaeoptera, the clade containing the first winged insects. The 1.6 Gbp C. splendens draft genome assembly is one of the largest insect genomes sequenced to date and encodes a predicted set of 22,523 protein-coding genes. Comparative genomic analyses with other sequenced insects identified a relatively small repertoire of C. splendens detoxification genes, which could explain its previously noted sensitivity to habitat pollution. Intriguingly, this repertoire includes a cytochrome P450 gene not previously described in any insect genome. The C. splendens immune gene repertoire appears relatively complete and features several genes encoding novel multi-domain peptidoglycan recognition proteins. Analysis of chemosensory genes revealed the presence of both gustatory and ionotropic receptors, as well as the insect odorant receptor coreceptor gene ( OrCo) and at least four partner odorant receptors ( ORs). This represents the oldest known instance of a complete OrCo/OR system in insects, and provides the molecular underpinning for odonate olfaction. The C. splendens genome improves the sampling of insect lineages that diverged before the radiation of Holometabola and offers new opportunities for molecular-level evolutionary, ecological, and behavioral studies.