Caste-biased genes in a subterranean termite are taxonomically restricted: implications for novel gene recruitment during termite caste evolution
The caste system of social insects presents a classic polyphenism in which widely divergent reproductive and non-reproductive phenotypes are expressed from the same genome. In termites, the sterile soldier caste is particularly divergent in phenotype and presumably evolved under selection for defensiveness. In this study, we use genomic phylostratigraphy to show that genes with soldier- and other caste-biased expression from the Eastern subterranean termite Reticulitermes flavipes are more taxonomically restricted on the tree of life than genes with no caste-biased expression. This pattern suggests that caste-biased genes are relatively young and implies past selection for novel gene recruitment during termite caste evolution. Moreover, a soldier-biased set of 74 genes contains a higher proportion of orphan genes with no known homology than does a nymph-biased set or any null gene sets. This again suggests that the termite caste—and soldiers in particular—makes disproportionate use of evolutionarily novel genes that are potentially recruited from non-coding regions of the genome. Given that Reticulitermes and most termite soldiers are sterile, any past selection for genetic novelty of this caste must have been indirect and mediated through reproducing relatives.
KeywordsSociogenomics Phylostrata Genetic novelty Orphan genes Reticulitermes
We thank Justin Croft and all members of the Social Biology Group at Western University (Canada) for discussion and advice throughout this study. This work was funded by a Faculty of Science Undergraduate Pre-Thesis Award to SB and a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant to GJT.
- Chernyshova AM, Saraceni J, Thompson GJ (2018) Soldier-biased gene expression in a termite implies indirect selection for defensiveness. In: Kocher S, Sumner S, Zayed A (eds) Biology and genomics of social insects. Cold Spring Harbor, New York, p 42Google Scholar
- Gadau J, Fewell J (eds) (2009) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, CambridgeGoogle Scholar
- Rust MK, Su NY (2012) Managing social insects of urban importance. Annu Rev Entomol 57:355–375. https://doi.org/10.1146/annurev-ento-120710-100634 CrossRefPubMedGoogle Scholar
- Su N-Y, Ye W, Ripa R et al (2006) Identification of Chilean Reticulitermes (Isoptera: Rhinotermitidae) inferred from three mitochondrial gene DNA sequences and soldier morphology. Ann Entomol Soc Am 99:352–363. https://doi.org/10.1603/0013-8746(2006)099%5B0352:IOCRIR%5D2.0.CO;2 CrossRefGoogle Scholar
- Thorne BL, Traniello JFA (2003) Comparative social biology of basal taxa of ants and termites. Annu Rev Entomol 48:283–306. https://doi.org/10.1146/annurev.ento.48.091801.112611 CrossRefPubMedGoogle Scholar
- Vargo EL, Husseneder C (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu Rev Entomol 54:379–403. https://doi.org/10.1146/annurev.ento.54.110807.090443 CrossRefPubMedGoogle Scholar
- Watson JAL, Okot-Kotber BM, Noirot CH (1985) Caste differentiation in social insects. Pergamon Press, OxfordGoogle Scholar
- Weesner FM (1970) Termites of the Nearctic region. In: Krishna K, Weesner FM (eds) Biology of termites, vol 2. Academic Press, Cambridge, pp 477–525Google Scholar