Sawfly genomes reveal evolutionary acquisitions that fostered the mega-radiation of parasitoid and eusocial Hymenoptera

Authors: OEYEN, JAN PHILIP - Zoological Research Museum Alexnder Koenig; STAHL, AARON - University Of Cincinnati; DONATH, ALEXANDER - Zoological Research Museum Alexnder Koenig; MARTYNOV, ALEXANDER - Skolkovo Institute Of Science And Technology; SOTIROPOULOS, ALEXANDROS - University Of Copenhagen; DOLAN, AMANDA - University Of Rochester; CRIDGE, ANDREW - University Of Otago; ROSENDALE, ANDREW - University Of Cincinnati; BUTTSTEDT, ANJA - Technical University Dresden; HANSSON, BILL - Max Planck Institute Of Chemical Ecology; Oppert, Brenda; Childers, Christopher; Poelchau, Monica

Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/19/2020
Publication Date: 7/1/2020
Citation: Oeyen, J. P., P. Baa-Puyoulet, J. B. Benoit, L. W. Beukeboom, E. Bomberg-Bauer, A. Buttstedt, F. Calevro, E. I. Cash, H. Chao, H. Charles, M.-J. M. Chen, C. Childers, A. G. Cridge, P. Dearden, H. Dinh, H. V. Doddapaneni, A. Dolan, A. Donath, D. Dowling, S. Dugan, E. Duncan, E. N. Elpidina, M. Friedrich, E. Geuverink, J. D. Gibson, S. Grath, C. J. P. Grimmelikhuijzen, E. Große-Wilde, C. Gudobba, Y. Han, B. S. Hansson, F. Hauser, D. S. T. Hughes, P. Ioannidis, E. Jacquin-Joly, E. C. Jennings, J. W. Jones, S. Klasberg, S. L. Lee, P. Lesný, M. Lovegrove, S. Martin, A. G. Martynov, C. Mayer, N. Montagné, V. C. Moris, M. Munoz-Torres, S. C. Murali, D. M. Muzny, B. Oppert, N. Parisot, T. Pauli, R. S. Peters, M. Petersen, C. Pick, E. Persyn, L. Podsiadlowski, M. F. Poelchau, P. Provataris, J. Qu, M. J. M. F. Reijnders, B. M. von Reumont, A. J. Rosendale, F. A. Simao, J. Skelly, A. G. Sotiropoulos, A. L. Stahl, M. Sumitani E. M. Szuter, O. Tidswell, E. Tsitlakidis, L. Vedder, R. M. Waterhouse, J. H. Werren, J. Wilbrandt, K. C. Worley, D. S. Yamanoto, L. van de Zande, E. M. Zdobnov, T. Ziesmann, R. A. Gibbs, S. Richards, M. Hatakeyama, B. Misof, and O. Niehuis. 2020. Sawfly genomes reveal evolutionary acquisitions that fostered the mega-radiation of parasitoid and eusocial Hymenoptera. Genome Biology and Evolution. 12(7):1099-1188. https://doi.org/10.1093/gbe/evaa106.
DOI: https://doi.org/10.1093/gbe/evaa106

Interpretive Summary: A summary of interpretations of the draft genomes of the turnip sawfly and the parasitoid sawfly is presented. Genes previously not found in other insects belonging to the family Hymenoptera (sawflies, wasps, ants, bees) were found in these genomes, such as those that enable carbon dioxide and light detection. In addition, larger numbers of sensory receptors were associated with these two sawfly genomes in comparison to other herbivorous insects and parasitoids. These draft genomes provide novel insights into how these insects locate and interact with their host plants and prey and will be useful for future research into this important group of pollinators.

Technical Abstract: The enormous species richness of Hymenoptera (sawflies, wasps, ants, bees) is thought to have been fostered by the evolution of parasitoidism which characterizes most hymenopterans [1, 2]. However, parasitoidism alone does signify species richness, as the parasitoid sawfly family Orussidae and the primarily parasitoid Apocrita (wasp-waisted Hymenoptera) share exactly the same evolutionary age [1], yet differ dramatically in species-richness [3]. Apparently, the evolutionary acquisition of additional traits was necessary to promote speciation in parasitoids. Here, we present draft genomes of the ectophytophagous turnip sawfly (Athalia rosae) and of the parasitoid sawfly (Orussus abietinus) and compare these with genomes of parasitoid and eusocial Apocrita to shed light on the early evolution of hymenopteran genomes, and on traits likely having fostered speciation in parasitoid hymenopterans. We find that the two sawflies genomes contain genes previously thought to be absent in Hymenoptera (e.g., for CO2 and light detection), and identified genes and other genomic traits previously known only from genomes of stinging Hymenotpera (Aculeata) (e.g., genes important for queen development in honeybees). We discovered that the genomes of parasitoid and eusocial Apocrita encode significantly more olfactory receptors than those of phytophagous and parasitoid sawflies, which may explain the tremendous diversification of parasitoid and eusocial Apocrita. These draft genomes thus provide novel insights into the early evolution of an ecologically and economically important group of insects and establishes the basis for future comparative genomic studies.