Dataset Information

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

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.

SUBMITTER: Panfilio KA

PROVIDER: S-EPMC6444547 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

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

Panfilio Kristen A KA Vargas Jentzsch Iris M IM Benoit Joshua B JB Erezyilmaz Deniz D Suzuki Yuichiro Y Colella Stefano S Robertson Hugh M HM Poelchau Monica F MF Waterhouse Robert M RM Ioannidis Panagiotis P Weirauch Matthew T MT Hughes Daniel S T DST Murali Shwetha C SC Werren John H JH Jacobs Chris G C CGC Duncan Elizabeth J EJ Armisén David D Vreede Barbara M I BMI Baa-Puyoulet Patrice P Berger Chloé S CS Chang Chun-Che CC Chao Hsu H Chen Mei-Ju M MM Chen Yen-Ta YT Childers Christopher P CP Chipman Ariel D AD Cridge Andrew G AG Crumière Antonin J J AJJ Dearden Peter K PK Didion Elise M EM Dinh Huyen H Doddapaneni Harsha Vardhan HV Dolan Amanda A Dugan Shannon S Extavour Cassandra G CG Febvay Gérard G Friedrich Markus M Ginzburg Neta N Han Yi Y Heger Peter P Holmes Christopher J CJ Horn Thorsten T Hsiao Yi-Min YM Jennings Emily C EC Johnston J Spencer JS Jones Tamsin E TE Jones Jeffery W JW Khila Abderrahman A Koelzer Stefan S Kovacova Viera V Leask Megan M Lee Sandra L SL Lee Chien-Yueh CY Lovegrove Mackenzie R MR Lu Hsiao-Ling HL Lu Yong Y Moore Patricia J PJ Munoz-Torres Monica C MC Muzny Donna M DM Palli Subba R SR Parisot Nicolas N Pick Leslie L Porter Megan L ML Qu Jiaxin J Refki Peter N PN Richter Rose R Rivera-Pomar Rolando R Rosendale Andrew J AJ Roth Siegfried S Sachs Lena L Santos M Emília ME Seibert Jan J Sghaier Essia E Shukla Jayendra N JN Stancliffe Richard J RJ Tidswell Olivia O Traverso Lucila L van der Zee Maurijn M Viala Séverine S Worley Kim C KC Zdobnov Evgeny M EM Gibbs Richard A RA Richards Stephen S

Genome biology 20190402 1

<h4>Background</h4>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.<h4>Results</h4>The 926-Mb Oncopeltus genome is wel ...[more]

PMID: 30935422

Similar Datasets

Project description:The Hemiptera comprise the most species-rich order of the hemimetabolous insects. Members of a number of superfamilies, most notably especially the more basal ones such as white flies, psyllids and aphids, belong to the most destructive agricultural insects known worldwide. At the other end of the phylogenetic tree are hemipterans that are notorious medical pests (e.g. kissing bugs). Most of the hemipteran species are good flyers, and lipid oxidation plays a pivotal role to power the contraction of flight muscles and, in aquatic water bugs, also deliver the ATP for the extensive swimming action of the leg muscles. Mobilization of stored lipids (mostly triacylglycerols in the fat body) to circulating diacylglycerols in the hemolymph is regulated by a set of small neuropeptides, the adipokinetic hormones (AKHs). We searched the literature and publicly available databases of transcriptomes and genomes to present here AKH sequences from 191 hemipteran species. Only few of these peptides were sequenced via Edman degradation or mass spectrometry, and even fewer were characterized with molecular biology methods; thus, the majority of the AKHs we have identified by bioinformatics are merely predicted sequences at this stage. Nonetheless, a total of 42 AKH primary sequences are assigned to Hemiptera. About 50% of these structures occur also in other insect orders, while the remaining 50% are currently unique for Hemiptera. We find 9 novel AKHs not shown to be synthesized before in any insect. Most of the hemipteran AKHs are octapeptides (28) but there is an impressive number of decapeptides (12) compared to other speciose orders such as Diptera and Lepidoptera. We attempt to construct a hypothetical molecular peptide evolution of hemipteran AKHs and find quite a bit of overlapping with current phylogenetic ideas of the Hemiptera. Lastly, we discuss the possibility to use the sequence of the aphid AKH as lead peptide for the research into a peptide mimetic fulfilling criteria of a green insecticide.

Project description:BackgroundMost evolutionary developmental biology ("evo-devo") studies of emerging model organisms focus on small numbers of candidate genes cloned individually using degenerate PCR. However, newly available sequencing technologies such as 454 pyrosequencing have recently begun to allow for massive gene discovery in animals without sequenced genomes. Within insects, although large volumes of sequence data are available for holometabolous insects, developmental studies of basally branching hemimetabolous insects typically suffer from low rates of gene discovery.ResultsWe used 454 pyrosequencing to sequence over 500 million bases of cDNA from the ovaries and embryos of the milkweed bug Oncopeltus fasciatus, which lacks a sequenced genome. This indirectly developing insect occupies an important phylogenetic position, branching basal to Diptera (including fruit flies) and Hymenoptera (including honeybees), and is an experimentally tractable model for short-germ development. 2,087,410 reads from both normalized and non-normalized cDNA assembled into 21,097 sequences (isotigs) and 112,531 singletons. The assembled sequences fell into 16,617 unique gene models, and included predictions of splicing isoforms, which we examined experimentally. Discovery of new genes plateaued after assembly of ~1.5 million reads, suggesting that we have sequenced nearly all transcripts present in the cDNA sampled. Many transcripts have been assembled at close to full length, and there is a net gain of sequence data for over half of the pre-existing O. fasciatus accessions for developmental genes in GenBank. We identified 10,775 unique genes, including members of all major conserved metazoan signaling pathways and genes involved in several major categories of early developmental processes. We also specifically address the effects of cDNA normalization on gene discovery in de novo transcriptome analyses.ConclusionsOur sequencing, assembly and annotation framework provide a simple and effective way to achieve high-throughput gene discovery for organisms lacking a sequenced genome. These data will have applications to the study of the evolution of arthropod genes and genetic pathways, and to the wider evolution, development and genomics communities working with emerging model organisms.[The sequence data from this study have been submitted to GenBank under study accession number SRP002610 (http://www.ncbi.nlm.nih.gov/sra?term=SRP002610). Custom scripts generated are available at http://www.extavourlab.com/protocols/index.html. Seven Additional files are available.].

Project description:The damselfishes (family Pomacentridae) inhabit near-shore communities in tropical and temperature oceans as one of the major lineages in coral reef fish assemblages. Our understanding of their evolutionary ecology, morphology and function has often been advanced by increasingly detailed and accurate molecular phylogenies. Here we present the next stage of multi-locus, molecular phylogenetics for the group based on analysis of 12 nuclear and mitochondrial gene sequences from 345 of the 422 damselfishes. The resulting well-resolved phylogeny helps to address several important questions about higher-level damselfish relationships, their evolutionary history and patterns of divergence. A time-calibrated phylogenetic tree yields a root age for the family of 55.5 mya, refines the age of origin for a number of diverse genera, and shows that ecological changes during the Eocene-Oligocene transition provided opportunities for damselfish diversification. We explored the idea that body size extremes have evolved repeatedly among the Pomacentridae, and demonstrate that large and small body sizes have evolved independently at least 40 times and with asymmetric rates of transition among size classes. We tested the hypothesis that transitions among dietary ecotypes (benthic herbivory, pelagic planktivory and intermediate omnivory) are asymmetric, with higher transition rates from intermediate omnivory to either planktivory or herbivory. Using multistate hidden-state speciation and extinction models, we found that both body size and dietary ecotype are significantly associated with patterns of diversification across the damselfishes, and that the highest rates of net diversification are associated with medium body size and pelagic planktivory. We also conclude that the pattern of evolutionary diversification in feeding ecology, with frequent and asymmetrical transitions between feeding ecotypes, is largely restricted to the subfamily Pomacentrinae in the Indo-West Pacific. Trait diversification patterns for damselfishes across a fully resolved phylogeny challenge many recent general conclusions about the evolution of reef fishes.

Dataset Information

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

Background

Results

Conclusions

Publications

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

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets