Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome
Authors: Panfilio Kristen A. , Vargas Jentzsch Iris M. , Benoit Joshua B. , Erezyilmaz Deniz , Suzuki Yuichiro , Colella Stefano , Robertson Hugh M. , Poelchau Monica F. , Waterhouse Robert M. , Ioannidis Panagiotis , Weirauch Matthew T. , Hughes Daniel S. T. , Murali Shwetha C. , Werren John H. , Jacobs Chris G. C. , Duncan Elizabeth J. , Armisén David , Vreede Barbara M. I. , Baa-Puyoulet Patrice , Berger Chloé S. , Chang Chun-che , Chao Hsu , Chen Mei-Ju M. , Chen Yen-Ta , Childers Christopher P. , Chipman Ariel D. , Cridge Andrew G. , Crumière Antonin J. J. , Dearden Peter K. , Didion Elise M. , Dinh Huyen , Doddapaneni Harsha Vardhan , Dolan Amanda , Dugan Shannon , Extavour Cassandra G. , Febvay Gérard , Friedrich Markus , Ginzburg Neta , Han Yi , Heger Peter , Holmes Christopher J. , Horn Thorsten , Hsiao Yi-min , Jennings Emily C. , Johnston J. Spencer , Jones Tamsin E. , Jones Jeffery W. , Khila Abderrahman , Koelzer Stefan , Kovacova Viera , Leask Megan , Lee Sandra L. , Lee Chien-Yueh , Lovegrove Mackenzie R. , Lu Hsiao-ling , Lu Yong , Moore Patricia J. , Munoz-Torres Monica C. , Muzny Donna M. , Palli Subba R. , Parisot Nicolas , Pick Leslie , Porter Megan L. , Qu Jiaxin , Refki Peter N. , Richter Rose , Rivera-Pomar Rolando , Rosendale Andrew J. , Roth Siegfried , Sachs Lena , Santos M. Emília , Seibert Jan , Sghaier Essia , Shukla Jayendra N. , Stancliffe Richard J. , Tidswell Olivia , Traverso Lucila , van der Zee Maurijn , Viala Séverine , Worley Kim C. , Zdobnov Evgeny M. , Gibbs Richard A. , Richards Stephen 
Published: April 2019

Background

The Hemiptera (aphids, cicadas, and true bugs) are a key insect order, with high diversity for feeding ecology and excellent experimental tractability for molecular genetics. Building upon recent sequencing of hemipteran pests such as phloem-feeding aphids and blood-feeding bed bugs, we present the genome sequence and comparative analyses centered on the milkweed bugOncopeltus fasciatus, a seed feeder of the family Lygaeidae.

Results

The 926-MbOncopeltusgenome is well represented by the current assembly and official gene set. We use our genomic and RNA-seq data not only to characterize the protein-coding gene repertoire and perform isoform-specific RNAi, but also to elucidate patterns of molecular evolution and physiology. We find ongoing, lineage-specific expansion and diversification of repressive C2H2 zinc finger proteins. The discovery of intron gain and turnover specific to the Hemiptera also prompted the evaluation of lineage and genome size as predictors of gene structure evolution. Furthermore, we identify enzymatic gains and losses that correlate with feeding biology, particularly for reductions associated with derived, fluid nutrition feeding.

Conclusions

With the milkweed bug, we now have a critical mass of sequenced species for a hemimetabolous insect order and close outgroup to the Holometabola, substantially improving the diversity of insect genomics. We thereby define commonalities among the Hemiptera and delve into how hemipteran genomes reflect distinct feeding ecologies. GivenOncopeltus’s strength as an experimental model, these new sequence resources bolster the foundation for molecular research and highlight technical considerations for the analysis of medium-sized invertebrate genomes.