The First Termite Genome Fills a Gap in Social Insect Genomics

Like ants and honey bee, termites are also eusocial insects. In colonies of termites, only a few individuals have reproductive ability (called queens and kings), while other individuals perform non-reproduction tasks like foraging, brood care or defense (called workers and soldiers). Living in societies has helped termites adapt to their environments and contributed to their ecological success. As major detritivores, termites play pivotal roles in maintaining biodiversity, particularly in tropical habitats. On the other hand, termite are considered as major pests of human structures, with an annual worldwide cost in damage and control estimated at US$40 billions.

Although sharing many similarities with ants and honey bee, which belong to Hymenoptera and have the unique haplodiploidy sex determination system, termites evolved the eusociality in a distantly related order called Isoptera. Termites also exhibit different patterns regarding sociality compared to social Hymenopterans. For instance, the kings of termites, which are long-term male reproductives and have the same status as the queens, are absent in social Hymenopterans. Therefore termites are a highly valuable system for studying social evolution. By far 10 social Hymenopteran genomes (8 ants and 2 bees) have been published, but no termite genome has been published yet. In a study published online today in Nature Communications, researchers from China, America and Germany have reported the sequences and analyses of the first termite genome (Zootermopsis nevadensis), revealing new insights into the molecular underpinning of complex societies in termites.

Z. nevadensis belongs to the family of dampwood termites (Termopsidae) which are rather basal termite species. Z. nevadensis has the smallest genome size known among termites (only about 500Mb), which is beneficial to building the assembly with short sequencing reads. In addition to the genomic data, the researchers also generated transcriptomic data for 25 samples, representing different sexes, developmental stages and castes, for functional genomics.

“One of the major findings in our study is that we found four gene families involved in spermatogenesis have specifically expanded in the termite genome, and from the transcriptome data we also observed up-regulated expression of these genes in male reproductive individuals”, said Cai Li, one of the lead co-authors of this project. “This is very interesting, because in a termite colony, queens and kings mate repeatedly during their long lives, while in the eusocial Hymenopterans, the reproduction system is usually queen-centralized and single-time mating. Our findings shed light on the molecular explanations for such difference, though a full understanding about this feature still needs further work.”

Compared to other insect genomes, Z. nevadensis have a considerably different repertoire of chemoreceptor genes, the important components in sensory systems of insects. Z. nevadensis has much fewer odorant receptors (ORs), which were found expanded in ants and honey bee. However, the ionotropic receptor (IR) family has expanded largely in termite. “The lower number of olfactory receptors reflects this termite’s lifestyle. Z. nevadensis is a basal termite, living their entire lives within a single log. Most of the ants and the honey bee show sophisticated communication behaviour and nestmate recognition and need more ORs to discriminate volatile substances and communicate with conspecifics. However, we predict the ‘higher’ termites, with a more sophisticated division of labor, would show an increase in OR genes.” said Jürgen Liebig of Arizona State University, one of corresponding authors of this study.

By comparing with other eusocial insect genomes, the researchers also found some gene families (e.g. vitellogenins, cytochrome P450s and hexamerins) involved in caste differentiation and reproductive division of labour in social Hymenopteran insects show similar patterns in termites, suggesting convergent evolution of these regulatory mechanisms.

“This first termite genome represents an important step, because it fills a big gap in social insect genomics. It has been a puzzle for a long time that if there is any common mechanism leading to the development of eusociality in different eusocial insect groups. We found several regulatory factors like vitellogenins, juvenile hormone et al., displaying significant gene expression changes among castes of termite. Similar patterns were also observed in other eusocial insects before.” said Guojie Zhang of China National Genebank, another corresponding author of this study, ‘With more and more social insect genomes available, we can have a closer look at this question with comparative genomic analysis among different social insect groups and will hopefully get a more thorough understanding of social evolution’

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