Hemimetabolous genomes reveal molecular basis of termite eusociality

Mark C Harrison,Sandra L Lee,Monica Poelchau,Hsu Chao,Kim C Worley,Qiaolin Xie,Christopher P Childers,Hugh M Robertson,Guillem Ylla,Harshavardhan Doddapaneni,Huyen Dinh,Ayako Wada‐Katsumata ,Nicolas Arning,Evelien Jongepier,Haofu Hu,Coby Schal,Alberto Lopez-Ezquerra,Lukas P.m Kremer ,Yi Han,Saria Otani,Ludovic Mallet,Donna M Muzny,Xavier Bellés ,Jose M Monroy-Kuhn,Richard A Gibbs,Tristan Bitard‐Feildel ,Florentine Schaub,Carsten Kemena,Daniel Hughes ,Jiaxin Qu,Ann Kathrin Huylmans ,Judith Korb,Annabell Moser,Michael Poulsen,Carolin Greiner,Stephen Richards,Shwetha C Murali,Johannes Gowin,Maria Dolors Piulachs ,Shannon Dugan,Erich Bornberg‐Bauer

doi:10.1038/s41559-017-0459-1

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 2-Gb genome of the German cockroach, Blattella germanica, and the 1.3-Gb 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.

Highlights

Eusociality, the reproductive division of labour with overlapping generations and cooperative brood care, is one of the major evolutionary transitions in biology[1]
Underlining a change in expression along with the evolution of castes, we found 35 Ionotropic receptors (IRs) to be differentially expressed between workers and queens in Z. nevadensis, 11 in C. secundus and 10 in M. natalensis (Fig. 2 and Supplementary Table 10)
These changes in copy number and caste-specific expression of genes involved in moulting and metamorphosis within termites compared to the German cockroach demonstrate that changes occurred in the control of the developmental pathway along with the evolution of castes. This interpretation needs to be experimentally verified. These results, considered alongside many studies on eusociality in Hymenoptera9, 10, 14,36 provide evidence that major changes in gene regulation and the evolution of sophisticated chemical communication are fundamental to the transition to eusociality in insects

Summary

C TM1 TM2 TM3 TM4 TM5 TM6 TM7

IRs. c, The upper schematic diagram depicts the 2D structure of an IR, containing ligand-binding lobes (S1 and S2), transmembrane regions (TM1–3) and the pore domain (P). Queen-biased genes were significantly over-represented among ZF genes for each of the termites (P < 2 × 10−10; χ2 test; Supplementary Table 17), indicating an important role of ZF genes in the regulation of genes related to caste-specific tasks and colony organization in the termites This is in contrast to the significant under-representation of differentially expressed ZF genes within B. germanica (P = 4.8 × 10−5; χ2-test). In C. secundus, expression is more varied, with four workerbiased, seven king-biased and two queen-biased genes (Fig. 2 and Supplementary Table 20) These changes in copy number and caste-specific expression of genes involved in moulting and metamorphosis within termites compared to the German cockroach demonstrate that changes occurred in the control of the developmental pathway along with the evolution of castes.

Conclusions

Methods

Replication

Statistical parameters

Findings

Antibodies