Conifer-feeding bark beetles are important herbivores and decomposers in forest ecosystems. These species complete their life cycle in nutritionally poor substrates and some can kill enormous numbers of trees during population outbreaks. The Eurasian spruce bark beetle (Ips typographus) can destroy >100 million m3 of spruce in a single year. We report a 236.8 Mb I. typographus genome assembly using PacBio long-read sequencing. The final phased assembly has a contig N50 of 6.65 Mb in 272 contigs and is predicted to contain 23,923 protein-coding genes. We reveal expanded gene families associated with plant cell wall degradation, including pectinases, aspartyl proteases, and glycosyl hydrolases. This genome sequence from the genus Ips provides timely resources to address questions about the evolutionary biology of the true weevils (Curculionidae), one of the most species-rich animal families. In forests of today, increasingly stressed by global warming, this draft genome may assist in developing pest control strategies to mitigate outbreaks.

Czech University of Life Sciences Prague Faculty of Forestry and Wood Sciences EVA 4 0 Unit Kamýcká 129 Praha 6 Suchdol Czech Republic

Czech University of Life Sciences Prague Faculty of Forestry and Wood Sciences Excellent Team for Mitigation Kamýcká 129 Praha 6 Suchdol Czech Republic

Department of Biology Lund University Lund Sweden

Department of Plant Protection Biology Swedish University of Agricultural Sciences Alnarp Sweden

Division of Biotechnology and Plant Health Norwegian Institute of Bioeconomy Research Ås Norway

Entomology Department Max Planck Institute for Chemical Ecology Jena Germany

Global Change Ecology Research Group School of Science Technology and Engineering University of the Sunshine Coast Sippy Downs QLD Australia

Zobrazit více v PubMed

Edmonds RL, Eglitis A. The role of the Douglas-fir beetle and wood borers in the decomposition of and nutrient release from Douglas-fir logs. Can. J. Res. 1989;19:853–859. doi: 10.1139/x89-130. DOI

Hlásny, T. et al. Living with bark beetles: impacts, outlook and management options. In: From Science to Policy 8. European Forest Institute (2019).

Raffa, K. F., Andersson, M. N. & Schlyter, F. Host selection by bark beetles: Playing the odds in a high‐stakes game. In: Adv. Insect Physiol. (eds Blomquist G., Tittinger C.), Vol 50, 1–74. Elsevier Ltd. (2016).

Biedermann PHW, et al. Bark beetle population dynamics in the Anthropocene: challenges and solutions. Trends Ecol. Evol. 2019;34:914–924. doi: 10.1016/j.tree.2019.06.002. PubMed DOI

Kurz WA, et al. Mountain pine beetle and forest carbon feedback to climate change. Nature. 2008;452:987–990. doi: 10.1038/nature06777. PubMed DOI

Marini L, et al. Climate drivers of bark beetle outbreak dynamics in Norway spruce forests. Ecography. 2017;40:1426–1435. doi: 10.1111/ecog.02769. DOI

Allen CD, et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Ecol. Manag. 2010;259:660–684. doi: 10.1016/j.foreco.2009.09.001. DOI

Seidl R, Schelhaas M-J, Rammer W, Verkerk PJ. Increasing forest disturbances in Europe and their impact on carbon storage. Nat. Clim. Change. 2014;4:806–810. doi: 10.1038/nclimate2318. PubMed DOI PMC

Ebner, G. Significantly more damaged wood in 2019. https://www.timber-online.net/log_wood/2020/02/significantly-more-damaged-wood-in-2019.html (2020).

Schlyter F, Birgersson G, Byers JA, Löfqvist J, Bergström G. Field response of spruce bark beetle, Ips typographus, to aggregation pheromone candidates. J. Chem. Ecol. 1987;13:701–716. doi: 10.1007/BF01020153. PubMed DOI

Andersson MN, et al. Peripheral modulation of pheromone response by inhibitory host compound in a beetle. J. Exp. Biol. 2010;213:3332–3339. doi: 10.1242/jeb.044396. PubMed DOI

Schlyter F, Birgersson G, Leufvén A. Inhibition of attraction to aggregation pheromone by verbenone and ipsenol: Density regulation mechanisms in bark beetle Ips typographus. J. Chem. Ecol. 1989;15:2263–2277. doi: 10.1007/BF01014114. PubMed DOI

Zhang Q-H, Schlyter F. Olfactory recognition and behavioural avoidance of angiosperm nonhost volatiles by conifer-inhabiting bark beetles. Agric. For. Entomol. 2004;6:1–19. doi: 10.1111/j.1461-9555.2004.00202.x. DOI

Andersson MN, et al. Antennal transcriptome analysis of the chemosensory gene families in the tree killing bark beetles, Ips typographus and Dendroctonus ponderosae (Coleoptera: Curculionidae: Scolytinae) BMC Genomics. 2013;14:198. doi: 10.1186/1471-2164-14-198. PubMed DOI PMC

Yuvaraj JK, et al. Putative ligand binding sites of two functionally characterized bark beetle odorant receptors. BMC Biol. 2021;19:16. doi: 10.1186/s12915-020-00946-6. PubMed DOI PMC

Hou, X.-Q. et al. Functional evolution of a bark beetle odorant receptor clade detecting monoterpenoids of different ecological origins. Mol. Biol. Evol. msab218, 10.1093/molbev/msab1218 (2021). PubMed PMC

Filipiak M, Weiner J. Nutritional dynamics during the development of xylophagous beetles related to changes in the stoichiometry of 11 elements. Physiol. Entomol. 2017;42:73–84. doi: 10.1111/phen.12168. DOI

Kirk, T. K. & Cowling, E. B. Biological decomposition of solid wood. In: The Chemistry of Solid Wood (ed Rowell R.) 455-487. ACS Publications. 10.1021/ba-1984-0207.ch012 (1984).

Chakraborty A, et al. Unravelling the gut bacteriome of Ips (Coleoptera: Curculionidae: Scolytinae): Identifying core bacterial assemblage and their ecological relevance. Sci. Rep. 2020;10:18572. doi: 10.1038/s41598-020-75203-5. PubMed DOI PMC

Chakraborty A, et al. Core mycobiome and their ecological relevance in the gut of five Ips bark beetles (Coleoptera: Curculionidae: Scolytinae) Front. Microbiol. 2020;11:2134. PubMed PMC

Davis TS. The ecology of yeasts in the bark beetle holobiont: A century of research revisited. Microb. Ecol. 2015;69:723–732. doi: 10.1007/s00248-014-0479-1. PubMed DOI

Kirisits, T. Fungal associates of european bark beetles with special emphasis on the ophiostomatoid fungi. In: Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis (eds et al.) 181-236. Springer Netherlands (2007).

Christiansen E. Ceratocystis polonica inoculated in Norway spruce: Blue‐staining in relation to inoculum density, resinosis and tree growth. Eur. J. Pathol. 1985;15:160–167. doi: 10.1111/j.1439-0329.1985.tb00880.x. DOI

Kandasamy D, Gershenzon J, Andersson MN, Hammerbacher A. Volatile organic compounds influence the interaction of the Eurasian spruce bark beetle (Ips typographus) with its fungal symbionts. ISME J. 2019;13:1788–1800. doi: 10.1038/s41396-019-0390-3. PubMed DOI PMC

Zhao T, et al. Fungal associates of the tree-killing bark beetle, Ips typographus, vary in virulence, ability to degrade conifer phenolics and influence bark beetle tunneling behavior. Fungal Ecol. 2019;38:71–79. doi: 10.1016/j.funeco.2018.06.003. DOI

Keeling CI, et al. Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol. 2013;14:R27. doi: 10.1186/gb-2013-14-3-r27. PubMed DOI PMC

Vega FE, et al. Draft genome of the most devastating insect pest of coffee worldwide: the coffee berry borer, Hypothenemus hampei. Sci. Rep. 2015;5:12525. doi: 10.1038/srep12525. PubMed DOI PMC

Smith SG. Chromosome numbers of Coleoptera. II. Heredity. 1953;7:31–48. doi: 10.1038/hdy.1953.3. DOI

Wang S, Lorenzen MD, Beeman RW, Brown SJ. Analysis of repetitive DNA distribution patterns in the Tribolium castaneum genome. Genome Biol. 2008;9:R61. doi: 10.1186/gb-2008-9-3-r61. PubMed DOI PMC

Herndon N, et al. Enhanced genome assembly and a new official gene set for Tribolium castaneum. BMC Genomics. 2020;21:47. doi: 10.1186/s12864-019-6394-6. PubMed DOI PMC

McKenna DD, et al. Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface. Genome Biol. 2016;17:227. doi: 10.1186/s13059-016-1088-8. PubMed DOI PMC

Eyun, S. I. et al. Molecular evolution of glycoside hydrolase genes in the western corn rootworm (Diabrotica virgifera virgifera). PLoS ONE9, (2014). PubMed PMC

McKenna DD, et al. The evolution and genomic basis of beetle diversity. Proc. Natl Acad. Sci. USA. 2019;116:24729–24737. doi: 10.1073/pnas.1909655116. PubMed DOI PMC

Berger E, Zhang D, Zverlov VV, Schwarz WH. Two noncellulosomal cellulases of Clostridium thermocellum, Cel9I and Cel48Y, hydrolyse crystalline cellulose synergistically. FEMS Microbiol. Lett. 2007;268:194–201. doi: 10.1111/j.1574-6968.2006.00583.x. PubMed DOI

Chu C-C, et al. Patterns of differential gene expression in adult rotation-resistant and wild-type western corn rootworm digestive tracts. Evol. Appl. 2015;8:692–704. doi: 10.1111/eva.12278. PubMed DOI PMC

Pauchet Y, Heckel DG. The genome of the mustard leaf beetle encodes two active xylanases originally acquired from bacteria through horizontal gene transfer. Proc. R. Soc. B: Biol. Sci. 2013;280:20131021. doi: 10.1098/rspb.2013.1021. PubMed DOI PMC

Fujita K, Shimomura K, Yamamoto K-I, Yamashita T, Suzuki K. A chitinase structurally related to the glycoside hydrolase family 48 is indispensable for the hormonally induced diapause termination in a beetle. Biochem. Biophys. Res. Commun. 2006;345:502–507. doi: 10.1016/j.bbrc.2006.04.126. PubMed DOI

Santamaría ME, et al. Digestive proteases in bodies and faeces of the two-spotted spider mite, Tetranychus urticae. J. Insect Physiol. 2015;78:69–77. doi: 10.1016/j.jinsphys.2015.05.002. PubMed DOI

Schoville SD, et al. A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) Sci. Rep. 2018;8:1931. doi: 10.1038/s41598-018-20154-1. PubMed DOI PMC

Netherer S, et al. Interactions among Norway spruce, the bark beetle Ips typographus and its fungal symbionts in times of drought. J. Pest Sci. 2021;94:591–614. doi: 10.1007/s10340-021-01341-y. PubMed DOI PMC

Schiebe C, et al. Inducibility of chemical defences in Norway spruce bark is correlated with unsuccessful mass attacks by the spruce bark beetle. Oecologia. 2012;170:183–198. doi: 10.1007/s00442-012-2298-8. PubMed DOI

Hedges LV. Distribution theory for glass’s estimator of effect size and related estimators. J. Educ. Stat. 1981;6:107–128. doi: 10.3102/10769986006002107. DOI

Everaerts, C., Grégoire, J.-C. & Merlin, J. The toxicity of Norway spruce monoterpenes to two bark beetle species and their associates. In: Mechanisms of Woody Plant Defenses Against Insects (eds Mattson W. J., Levieux J., Bernard-Dagan C.) 335-344. Springer (1988).

Franceschi VR, Krokene P, Christiansen E, Krekling T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. N. Phytol. 2005;167:353–376. doi: 10.1111/j.1469-8137.2005.01436.x. PubMed DOI

Andersson MN, Newcomb RD. Pest control compounds targeting insect chemoreceptors: another silent spring? Front. Ecol. Evol. 2017;5:5. doi: 10.3389/fevo.2017.00005. DOI

Anderbrant O, Schlyter F, Birgersson G. Intraspecific competition affecting parents and offspring in the bark beetle Ips typographus. Oikos. 1985;45:89–98. doi: 10.2307/3565226. DOI

Schlyter F, Cederholm I. Separation of the sexes of living spruce bark beetles, Ips typographus (L.), (Coleoptera: Scolytidae) J. Appl. Entomol. 1981;92:42–47.

Chin CS, et al. Phased diploid genome assembly with single-molecule real-time sequencing. Nat. Methods. 2016;13:1050–1054. doi: 10.1038/nmeth.4035. PubMed DOI PMC

Kurtz S, et al. Versatile and open software for comparing large genomes. Genome Biol. 2004;5:R12. doi: 10.1186/gb-2004-5-2-r12. PubMed DOI PMC

Simão FA, Waterhouse RM, Loannidis P, Kriventseva EV, Zdobnov EM. BUSCO: Assessing genome assembly and annotation completeness withqaz single-copy orthologs. Bioinformatics. 2015;31:3210–3212. doi: 10.1093/bioinformatics/btv351. PubMed DOI

Marçais G, Kingsford C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics. 2011;27:764–770. doi: 10.1093/bioinformatics/btr011. PubMed DOI PMC

Ranallo-Benavidez TR, Jaron KS, Schatz MC. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat. Commun. 2020;11:1432. doi: 10.1038/s41467-020-14998-3. PubMed DOI PMC

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. PubMed PMC

Haas BJ, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 2013;8:1494–1512. doi: 10.1038/nprot.2013.084. PubMed DOI PMC

Li H, et al. The sequence alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC

R Core Team. R: A Language and Environment for Statistical Computing.). R Foundation for Statistical Computing (2020).

Kim D, Langmead B, Salzberg SL. HISAT: A fast spliced aligner with low memory requirements. Nat. Methods. 2015;12:357–360. doi: 10.1038/nmeth.3317. PubMed DOI PMC

Pertea M, et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 2015;33:290–295. doi: 10.1038/nbt.3122. PubMed DOI PMC

Hoff KJ, Lange S, Lomsadze A, Borodovsky M, Stanke M. BRAKER1: Unsupervised RNA-Seq-based genome annotation with GeneMark-ET and AUGUSTUS. Bioinformatics. 2015;32:767–769. doi: 10.1093/bioinformatics/btv661. PubMed DOI PMC

Holt C, Yandell M. MAKER2: An annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinform. 2011;12:491. doi: 10.1186/1471-2105-12-491. PubMed DOI PMC

Korf I. Gene finding in novel genomes. BMC Bioinform. 2004;5:59. doi: 10.1186/1471-2105-5-59. PubMed DOI PMC

Finn RD, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42:D222–D230. doi: 10.1093/nar/gkt1223. PubMed DOI PMC

Potter SC, et al. HMMER web server: 2018 update. Nucleic Acids Res. 2018;46:W200–W204. doi: 10.1093/nar/gky448. PubMed DOI PMC

Hall MR, et al. The crown-of-thorns starfish genome as a guide for biocontrol of this coral reef pest. Nature. 2017;544:231–234. doi: 10.1038/nature22033. PubMed DOI

Albertin CB, et al. The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature. 2015;524:220–224. doi: 10.1038/nature14668. PubMed DOI PMC

Simakov O, et al. Insights into bilaterian evolution from three spiralian genomes. Nature. 2013;493:526–531. doi: 10.1038/nature11696. PubMed DOI PMC

Xu L, et al. OrthoVenn2: A web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res. 2019;47:W52–W58. doi: 10.1093/nar/gkz333. PubMed DOI PMC

Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20:238–238. doi: 10.1186/s13059-019-1832-y. PubMed DOI PMC

Han MV, Thomas GW, Lugo-Martinez J, Hahn MW. Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. Mol. Biol. Evol. 2013;30:1987–1997. doi: 10.1093/molbev/mst100. PubMed DOI

Nakagawa S, Cuthill IC. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. Camb. Philos. Soc. 2007;82:591–605. doi: 10.1111/j.1469-185X.2007.00027.x. PubMed DOI

Coe, R. Effect size calculator. Cambridge CEM (2000).

Complex Genomic Landscape of Inversion Polymorphism in Europe's Most Destructive Forest Pest

Insights into the Detoxification of Spruce Monoterpenes by the Eurasian Spruce Bark Beetle

Antennal Transcriptome Screening and Identification of Chemosensory Proteins in the Double-Spine European Spruce Bark Beetle, Ips duplicatus (Coleoptera: Scolytinae)

Comparative gut proteomics study revealing adaptive physiology of Eurasian spruce bark beetle, Ips typographus (Coleoptera: Scolytinae)

Genome and transcriptome of Ips nitidus provide insights into high-altitude hypoxia adaptation and symbiosis

Weak population genetic structure in Eurasian spruce bark beetle over large regional scales in Sweden

Identifying optimal reference genes for gene expression studies in Eurasian spruce bark beetle, Ips typographus (Coleoptera: Curculionidae: Scolytinae)

RNA Interference-Based Forest Protection Products (FPPs) Against Wood-Boring Coleopterans: Hope or Hype?

Interactions among Norway spruce, the bark beetle Ips typographus and its fungal symbionts in times of drought

Zobrazit více v PubMed

figshare
10.6084/m9.figshare.14503065