Termites are a lineage of social cockroaches abundant in tropical ecosystems where they are key decomposers of organic matter. Despite their ecological significance, only a handful of reference-quality termite genomes have been sequenced, which is insufficient to unravel the genetic mechanisms that have contributed to their ecological success. Here, we perform sequencing and hybrid assembly of 45 taxonomically and ecologically diverse termites and two cockroaches, resulting in haplotype-merged genome assemblies of 47 species, 22 of which were near-chromosome level. Next, we examine the link between termite dietary evolution and major genomic events. We find that Termitidae, which include ~80% of described termite species, have larger genomes with more genes and a higher proportion of transposons than other termites. Our analyses identify a gene number expansion early in the evolution of Termitidae, including an expansion of the repertoire of CAZymes, the genes involved in lignocellulose degradation. Notably, this expansion of genomes and gene repertoires coincided with the origin of soil-feeding in Termitidae and remained unchanged in lineages that secondarily reverted to a wood-based diet. Overall, our sequencing effort multiplies the number of available termite genomes by six and provides insights into the genome evolution of an ancient lineage of social insects.

Biology Centre of the Czech Academy of Sciences Institute of Entomology České Budějovice Czech Republic

Centre for Health and Life Sciences Coventry University Coventry UK

College of Life Sciences Chongqing Normal University Chongqing People's Republic of China

College of Plant Protection Southwest University Chongqing China

Department for Materials and the Environment BAM Federal Institute for Materials Research and Testing Berlin Germany

Faculty of Tropical AgriSciences Czech University of Life Sciences Kamýcká 129 Prague Czech Republic

Institute for Evolution and Biodiversity University of Münster Hüfferstraße 1 Münster Germany

Institute of Biology Freie Universität Berlin Berlin Germany

Okinawa Institute of Science and Technology Graduate University 1919 1 Tancha Onna son Okinawa Japan

Tropical Biosphere Research Center University of the Ryukyus 1 Senbaru Nishihara Okinawa Japan

Universidade Federal do ABC Avenida dos Estados 5001 Santo André SP Brazil

University Sorbonne Paris Nord Laboratory of Experimental and Comparative Ethology UR4443 99 avenue Jean Baptiste Clément Villetaneuse France

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