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

TitleMolecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome.
Publication TypeJournal Article
Year of Publication2019
AuthorsPanfilio, KA, Jentzsch, IMVargas, Benoit, JB, Erezyilmaz, D, Suzuki, Y, Colella, S, Robertson, HM, Poelchau, MF, Waterhouse, RM, Ioannidis, P, Weirauch, MT, Hughes, DST, Murali, SC, Werren, JH, Jacobs, CGC, Duncan, EJ, Armisén, D, Vreede, BMI, Baa-Puyoulet, P, Berger, CS, Chang, C-C, Chao, H, Chen, M-JM, Chen, Y-T, Childers, CP, Chipman, AD, Cridge, AG, Crumière, AJJ, Dearden, PK, Didion, EM, Dinh, H, Doddapaneni, H, Dolan, A, Dugan, S, Extavour, CG, Febvay, G, Friedrich, M, Ginzburg, N, Han, Y, Heger, P, Holmes, CJ, Horn, T, Hsiao, Y-M, Jennings, EC, J Johnston, S, Jones, TE, Jones, JW, Khila, A, Koelzer, S, Kovacova, V, Leask, M, Lee, SL, Lee, C-Y, Lovegrove, MR, Lu, H-L, Lu, Y, Moore, PJ, Munoz-Torres, MC, Muzny, DM, Palli, SR, Parisot, N, Pick, L, Porter, ML, Qu, J, Refki, PN, Richter, R, Rivera-Pomar, R, Rosendale, AJ, Roth, S, Sachs, L, M Santos, E, Seibert, J, Sghaier, E, Shukla, JN, Stancliffe, RJ, Tidswell, O, Traverso, L, Van der Zee, M, Viala, S, Worley, KC, Zdobnov, EM, Gibbs, RA, Richards, S
JournalGenome Biol
Volume20
Issue1
Pagination64
Date Published2019 Apr 02
ISSN1474-760X
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.

DOI10.1186/s13059-019-1660-0
Alternate JournalGenome Biol.
PubMed ID30935422
PubMed Central IDPMC6444547
Grant List5R01GM080203 / / National Institute of General Medical Sciences /
ERC-CoG #616346 / / H2020 European Research Council /
5R01HG004483 / / National Human Genome Research Institute /
US NSF DEB1257053 / / National Science Foundation /
R01 GM080203 / GM / NIGMS NIH HHS / United States
R01 HG004483 / HG / NHGRI NIH HHS / United States
U54 HG003273 / / National Human Genome Research Institute /
U54 HG003273 / HG / NHGRI NIH HHS / United States
PP00P3_170664 / / Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung /
R01 GM113230 / GM / NIGMS NIH HHS / United States
31003A_143936 / / Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung /
PA 2044/1-1 / / Deutsche Forschungsgemeinschaft /
SFB 680 project A1 / / Deutsche Forschungsgemeinschaft /
SFB 680 project A12 / / Deutsche Forschungsgemeinschaft /
DE-AC02-05CH11231 / / U.S. Department of Energy /