Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome

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

Research output: Contribution to journalArticle

Abstract

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 bug Oncopeltus fasciatus, a seed feeder of the family Lygaeidae. Results: The 926-Mb Oncopeltus genome 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. Given Oncopeltus'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.

Original languageEnglish (US)
Article number64
JournalGenome biology
Volume20
Issue number1
DOIs
StatePublished - Apr 2 2019

Keywords

  • Evolution of development
  • Gene family evolution
  • Gene structure
  • Lateral gene transfer
  • Phytophagy
  • RNAi
  • Transcription factors

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Cell Biology

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  • Cite this

    Panfilio, K. A., Vargas Jentzsch, I. M., Benoit, J. B., Erezyilmaz, D., Suzuki, Y., Colella, S., Robertson, H. M., Poelchau, M. F., Waterhouse, R. M., Ioannidis, P., Weirauch, M. T., Hughes, D. S. T., Murali, S. C., Werren, J. H., Jacobs, C. G. C., Duncan, E. J., Armisén, D., Vreede, B. M. I., Baa-Puyoulet, P., ... Richards, S. (2019). Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome. Genome biology, 20(1), [64]. https://doi.org/10.1186/s13059-019-1660-0