Genomic and transcriptomic analyses of the subterranean termite Reticulitermes speratus: Gene duplication facilitates social evolution

Shuji Shigenobu*, Yoshinobu Hayashi, Dai Watanabe, Gaku Tokuda, Masaru Y. Hojo, Kouhei Toga, Ryota Saiki, Hajime Yaguchi, Yudai Masuoka, Ryutaro Suzuki, Shogo Suzuki, Moe Kimura, Masatoshi Matsunami, Yasuhiro Sugime, Kohei Oguchi, Teruyuki Niimi, Hiroki Gotoh, Masaru K. Hojo, Satoshi Miyazaki, Atsushi ToyodaToru Miura*, Kiyoto Maekawa*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

39 Scopus citations

Abstract

Termites are model social organisms characterized by a polyphenic caste system. Subterranean termites (Rhinotermitidae) are ecologically and economically important species, including acting as destructive pests. Rhinotermitidae occupies an important evolutionary position within the clade representing a transitional taxon between the higher (Termitidae) and lower (other families) termites. Here, we report the genome, transcriptome, and methylome of the Japanese subterranean termite Reticulitermes speratus. Our analyses highlight the significance of gene duplication in social evolution in this termite. Gene duplication associated with caste-biased gene expression was prevalent in the R. speratus genome. The duplicated genes comprised diverse categories related to social functions, including lipocalins (chemical communication), cellulases (wood digestion and social interaction), lysozymes (social immunity), geranylgeranyl diphosphate synthase (social defense), and a novel class of termite lineage–specific genes with unknown functions. Paralogous genes were often observed in tandem in the genome, but their expression patterns were highly variable, exhibiting caste biases. Some of the assayed duplicated genes were expressed in caste-specific organs, such as the accessory glands of the queen ovary and the frontal glands of soldier heads.We propose that gene duplication facilitates social evolution through regulatory diversification, leading to caste-biased expression and subfunctionalization and/or neofunctionalization conferring caste-specialized functions.

Original languageEnglish
Article numbere2110361119
JournalProceedings of the National Academy of Sciences of the United States of America
Volume119
Issue number3
DOIs
StatePublished - 2022/01/18

ASJC Scopus subject areas

  • General

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