Genome sequence of the wheat stem sawfly, Cephus cinctus, representing an early-branching lineage of the Hymenoptera, illuminates evolution of hymenopteran chemoreceptors

Abstract

The wheat stem sawfly, Cephus cinctus, is a major pest of wheat and key ecological player in the grasslands of western North America. It also represents the distinctive Cephoidea superfamily of sawflies (Symphyta) that appeared early during the hymenopteran radiation, but after three early-branching eusymphytan superfamilies that form the base of the order Hymenoptera. We present a high-quality draft genome assembly of 162 Mb in 1,976 scaffolds with a scaffold N50 of 622 kb. Automated gene annotation identified 11,210 protein-coding gene models and 1,307 noncoding RNA models. Thirteen percent of the assembly consists of ∼58,000 transposable elements partitioned equally between Class-I and Class-II elements. Orthology analysis reveals that 86% of Cephus proteins have identifiable orthologs in other insects. Phylogenomic analysis of conserved subsets of these proteins supports the placement of the Cephoidea between the Eusymphyta and the parasitic woodwasp superfamily Orussoidea. Manual annotation and phylogenetic analysis of families of odorant, gustatory, and ionotropic receptors, plus odorant-binding proteins, shows that Cephus has representatives for most conserved and expanded gene lineages in the Apocrita (wasps, ants, and bees). Cephus has also maintained several insect gene lineages that have been lost from the Apocrita, most prominently the carbon dioxide receptor subfamily. Furthermore, Cephus encodes a few small lineage-specific chemoreceptor gene family expansions that might be involved in adaptations to new grasses including wheat. These comparative analyses identify gene family members likely to have been present in the hymenopteran ancestor and provide a new perspective on the evolution of the chemosensory gene repertoire.

Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera

“…The assemblies are close in size to that of the wheat stem sawfly, Ce. cinctus (Cephidae; 205 Mb; Hanrahan and Johnston 2011 ; Robertson et al. 2018 ), and fall within the lower range of the known genome sizes of Hymenoptera (98 Mb–1.3 Gb; Ardila-Garcia et al.…”

“…2018 ), but closely match the reported numbers of protein-coding genes in the draft genomes of Ce. cinctus (11,206; Robertson et al. 2018 ) and the European paper wasp, Polistes dominula ( fig.…”

“…2018 ). The only published draft genome of a sawfly is that of the wheat stem sawfly, Cephus cinctus (Cephoidea) ( Robertson et al. 2018 ).…”

The diversity and evolution of odorant receptors in beetles (Coleoptera)

“…) or proliferate within an OR subfamily (eg Groups 3 and 5A; Figs and ). Similar expansions have been observed in the gall midges (Diptera), where they were attributed to their specialized gall‐forming lifestyle (Zhao et al ., ), and amongst the Hymenoptera, where they were attributed to sociality (Zhou et al ., ; Robertson et al ., ). However, the single species in our dataset that exhibits subsocial behaviour, N. vespilloides (Cunningham et al ., ), presented a relatively small complement of ORs, and the primary expansion of NvesORs in Group 3 was comparable to expansions in nonsocial beetles (Fig.…”

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

“…We manually annotated more than 1000 genes (719 for A. ervi and 644 for L. fabarum, Table 3) from functional categories that are key to parasitoid life history and adaptation. This is especially important for large gene families, which are usually poorly annotated by automatic prediction [147]. Expansion and reductions in such gene families potentially underlie key adaptive differences between the two parasitoids, and necessitate accurate annotation.…”