Journal Article

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

Zdobnov, Evgeny M., Colella, Stefano, Vargas Jentzsch, Iris M., Weirauch, Matthew T., Santos, M. Emília, Jennings, Emily C., Muzny, Donna M., Rosendale, Andrew J., Qu, Jiaxin, Werren, John H., Jacobs, Chris G. C., Stancliffe, Richard J., Ioannidis, Panagiotis, Horn, Thorsten, Febvay, Gérard, Lu, Hsiao-ling, Dugan, Shannon, Gibbs, Richard A., Chao, Hsu, Dolan, Amanda, Leask, Megan, Crumière, Antonin J. J., Koelzer, Stefan, Viala, Séverine, Doddapaneni, Harsha Vardhan, Jones, Jeffery W., Richter, Rose, Murali, Shwetha C., Refki, Peter N., Dinh, Huyen, Porter, Megan L., Richards, Stephen, Chen, Yen-Ta, Worley, Kim C., Baa-Puyoulet, Patrice, Munoz-Torres, Monica C., Kovacova, Viera, Pick, Leslie, Khila, Abderrahman, Heger, Peter, Chipman, Ariel D., Childers, Christopher P., Cridge, Andrew G., Hughes, Daniel S. T., Benoit, Joshua B., Lee, Sandra L., Waterhouse, Robert M., Armisén, David, Rivera-Pomar, Rolando, Vreede, Barbara M. I., Roth, Siegfried, Suzuki, Yuichiro, Didion, Elise M., Moore, Patricia J., Sachs, Lena, Dearden, Peter K., Ginzburg, Neta, Shukla, Jayendra N., Berger, Chloé S., Lu, Yong, Tidswell

2019

Overview

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.

• Publisher: BioMed Central,Springer Nature B.V,BMC
• Subject: Amino Acid Sequence / Animal behavior / Animal Genetics and Genomics / Animals / Aphidoidea / BASIC BIOLOGICAL SCIENCES / Bioinformatics / Biology / Biomedical and Life Sciences / Consortia / CYS2-HIS2 Zinc Fingers / Ecology / Evolution & development / evolution of development / Evolution, Molecular / Evolutionary Biology / family / Feeding / Feeding Behavior / Gene Dosage / Gene expression / Gene Expression Profiling / Gene family evolution / Gene structure / gene strucutre / Gene Transfer, Horizontal / Genes, Homeobox / Genetics / Genome, Insect / Genomes / Genomics / hematophagy / Hemiptera / Hemiptera - genetics / Hemiptera - growth & development / Hemiptera - metabolism / Human Genetics / insects / Integrated software / introns / Invertebrates / Lateral gene transfer / Life Sciences / Metabolism / Microbial Genetics and Genomics / Molecular evolution / Nucleotide sequence / nutrition / Oncopeltus / Oncopeltus fasciatus / Pests / Phylogenetics / physiology / Phytophagy / Pigmentation - genetics / Plant Genetics and Genomics / Ribonucleic acid / RNA / RNA-mediated interference / RNAi / sequence analysis / Smell / species / Transcription factors / Transcription Factors - genetics / zinc finger motif / Zinc finger proteins