Hemimetabolous genomes reveal molecular basis of termite eusociality

Abstract

Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the first, 2GB genome of a cockroach, Blattella germanica, and the 1.3GB genome of the drywood termite, Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination.Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.Eusociality, the reproductive division of labour with overlapping generations and cooperative brood care, 1 is one of the major evolutionary transitions in biology.1 Although rare, eusociality has been observed 2 in a diverse range of organisms, including shrimps, mole-rats and several insect lineages. bees and ants appeared. 5 Therefore, identifying the molecular mechanisms common to both origins of 7 eusociality is crucial to understanding the fundamental signatures of these rare evolutionary transitions. 8While the availability of genomes from many eusocial and non-eusocial hymenopteran species 8 has allowed 9 extensive research into the origins of eusociality within ants and bees, 9, 10, 11 a paucity of genomic data 10 from cockroaches and termites has precluded large-scale investigations into the evolution of eusociality 11 in this hemimetabolous clade. 12The conditions under which eusociality arose differ greatly between the two groups. peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/181909 doi: bioRxiv preprint first posted online Aug. 29, 2017; lower and all higher termites) form large, complex societies, in which worker castes can be irreversible. 12 24For this reason, higher, but not lower, termites can be classed as superorganismal.13 Similarly, within 25Hymenoptera, varying levels of eusociality exist. 26Here we provide insights into the molecular signatures of eusociality within the termites. We analysed 27 the genomes of two lower and one higher termite species and compared them to the first cockroach genome, 28as a closely-related non-eusocial outgroup. Furthermore, differences in expression between nymphs and 29 adults of the cockroach were compared to differences in expression between workers and reproductives of Material) and large expansions in many manually annotated gene families offer high confidence in the 52 accuracy of this proteome size....

Transcriptomic changes during caste development through social interactions in the termite Zootermopsis nevadensis

“…Especially, expression levels of three genes involved in ecdysone synthesis (shadow, shade, and spookier) were highly upregulated. This was consistent with the previous reports, which showed that ecdysone receptor signaling activity was important for presoldier and soldier formations in Z. nevadensis (Masuoka & Maekawa, 2016), and that the caste-specific expressions of ecdysone synthesis genes were broadly observed among three termite species including Z. nevadensis (Harrison et al, 2018).…”

Involvement of integument‐rich CYP4G19 in hydrocarbon biosynthesis and cuticular penetration resistance in Blattella germanica (L.)

“…35 To date, at least one CYP4G gene has been found in all insects with sequenced genomes. The B. germanica genome contains only one CYP4G gene, 33 and we have found that it plays a role in hydrocarbon production. Likewise, Acyrthosiphon pisum CYP4G51 and Apis mellifera CYP4G11, the only CYP4G member in each species, have also been shown to be involved in hydrocarbon biosynthesis.…”

“…31 However, two CYP4G subfamily genes, CYP4G16 and CYP4G17, have been reported to be positively associated with cuticular resistance via catalyzing the production of CHCs in A. gambiae. 9,32 The only CYP4G member in B. germanica, CYP4G19, 33 was reported to be overexpressed in a pyrethroid-resistant strain, 34 but no role in insecticide resistance has been attributed to CYP4G19. Several CYP4G genes have been functionally characterized to be involved in the final decarbonylation step of hydrocarbon biosynthesis by baculovirus expression system 9,[35][36][37] or RNAi-based functional studies.…”

An expression atlas of chemosensory ionotropic glutamate receptors identifies a molecular basis of carbonation detection

“…A second large repertoire of 3 receptors implicated in insect gustation is the Ionotropic Receptor (IR) family, which are ligand-gated ion channels that have derived from synaptic ionotropic glutamate receptors (iGluRs) [14][15][16][17] . Unlike iGluRs, IRs display enormous diversification both in the size of the repertoire across insects (ranging from tens to several hundreds 15,16,18 ), and in their protein sequences (with as little as 10% amino acid identity between pairs of receptors). IRs have been best-characterised in the vinegar fly, Drosophila melanogaster, which possesses 60 intact Ir genes.…”