Journal of Pest Science

, Volume 92, Issue 1, pp 51–70 | Cite as

Biosurveillance of forest insects: part I—integration and application of genomic tools to the surveillance of non-native forest insects

  • Amanda D. RoeEmail author
  • Alex S. Torson
  • Guillaume Bilodeau
  • Pierre Bilodeau
  • Gwylim S. Blackburn
  • Mingming Cui
  • Michel Cusson
  • Daniel Doucet
  • Verena C. Griess
  • Valentine Lafond
  • Gregory Paradis
  • Ilga Porth
  • Julien Prunier
  • Vivek Srivastava
  • Emilie Tremblay
  • Adnan Uzunovic
  • Denys Yemshanov
  • Richard C. Hamelin


Invasive species pose significant threats to forest ecosystems. Early intervention strategies are the most cost-effective means to control biological invasions, but are reliant on robust biosurveillance. State-of-the-art genomic approaches can provide an unprecedented opportunity to access detailed information on the invasion process and adaptive potential of invasive insects that pose an immediate threat to forests environments. Genomics can improve diagnostics of the invader and identify its route of invasion by determining the source population(s), assess its probability of establishment and patterns of spread, as well as provide evidence of adaptation. Applied biosurveillance efforts by plant health regulatory agencies will benefit substantially from the detailed insights that genomic data bring to our understanding of biological invasions.


Biological invasion Biosecurity Surveillance Genomics High throughput sequencing 



We wish to thank Brent Sinclair, three anonymous reviewers, and the Subject Editor for thoughtful, insightful feedback we received on earlier versions of this manuscript. We also wish to thank the guest editors and journal editors for the opportunity to contribute to this special issue on invasive insect pests of forests. Finally, we wish to acknowledge funding support from Genome Canada, Genome British Columbia, and Genome Quebec for support for the Biosurveillance of Alien Forest Enemies (bioSAFE) as part of the Large-Scale Applied Research Project in Natural Resources and the Environment. Additional funding was also provided by the Genomics Research and Development Initiative (Natural Resources Canada).


This study was funded by Genome Canada, Genome British Columbia, Genome Quebec, and the Genomics Research and Development Initiative (Natural Resources Canada).

Compliance with ethical standards

Conflict of interest

The author declares that they have no conflict of interest.

Human and Animal statement

This article does not contain any studies with animals performed by any of the authors.


  1. Abdelfattah A, Malacrinòb A, Wisniewski M et al (2018) Metabarcoding: a powerful tool to investigate microbial communities and shape future plant protection strategies. Biol Control 120:1–20. Google Scholar
  2. Altshuler D, Pollara VJ, Cowles CR et al (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407:513–516Google Scholar
  3. Alvarez M, Schrey AW, Richards CL (2015) Ten years of transcriptomics in wild populations: What have we learned about their ecology and evolution? Mol Ecol 24:710–725. Google Scholar
  4. Andersen JC, Havill NP, Caccone A, Elkinton JS (2017) Postglacial recolonization shaped the genetic diversity of the winter moth (Operophtera brumata) in Europe. Ecol Evol 7:3312–3323. Google Scholar
  5. Andersson MN, Grosse-Wilde E, Keeling CI et al (2013) Antennal transcriptome analysis of the chemosensory gene families in the tree killing bark beetles, Ips typographus and Dendroctonus ponderosae (Coleoptera: Curculionidae: Scolytinae). BMC Genom 14:198. Google Scholar
  6. Andrews KR, Good JM, Miller MR et al (2016) Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet 17:81–92Google Scholar
  7. Arimoto M, Iwaizumi R (2014) Identification of Japanese Lymantria species (Lepidoptera: Lymantriidae) based on PCR-RFLP analysis of mitochondrial DNA. Appl Entomol Zool 49:159–169. Google Scholar
  8. Arimoto M, Iwaizumi R (2016) PCR-RFLP analysis of the ITS2 region to identify Japanese Lymantria species (Lepidoptera: Lymantriidae). Appl Entomol Zool 51:63–70. Google Scholar
  9. Auger-Rozenberg MA, Boivin T, Magnoux E et al (2012) Inferences on population history of a seed chalcid wasp: Invasion success despite a severe founder effect from an unexpected source population. Mol Ecol 21:6086–6103. Google Scholar
  10. Aukema JE, Leung B, Kovacs K et al (2011) Economic impacts of non-native forest insects in the continental United States. PLoS ONE 6:1–7. Google Scholar
  11. Baird NA, Etter PD, Atwood TS et al (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3:e3376. Google Scholar
  12. Bateson P (2015) Why are individuals so different from each other? Heredity (Edinb) 115:285–292. Google Scholar
  13. Batista PD, Janes JK, Boone CK et al (2016) Adaptive and neutral markers both show continent-wide population structure of mountain pine beetle (Dendroctonus ponderosae). Ecol Evol 6:6292–6300. Google Scholar
  14. Battisti A, Larsson S (2015) Climate change and insect pest distribution range. Climate change and insect pests. CAB International, Wallingford, pp 1–15Google Scholar
  15. Benazzo A, Ghirotto S, Vilaça ST, Hoban S (2015) Using ABC and microsatellite data to detect multiple introductions of invasive species from a single source. Heredity (Edinb) 115:262–272. Google Scholar
  16. Berardi L, Pivato M, Arrigoni G et al (2017) Proteome analysis of urticating setae from Thaumetopoea pityocampa (Lepidoptera: Notodontidae). J Med Entomol 54:1560–1566. Google Scholar
  17. Bilodeau P, Roe AD, Bilodeau G et al (2018) Biosurveillance of forest insects. Part II: adoption of genomic tools by end user communities and barriers to integration. J Pest Sci. Google Scholar
  18. Bista I, Carvalho GR, Tang M et al (2018) Performance of amplicon and shotgun sequencing for accurate biomass estimation in invertebrate community samples. Mol Ecol Res. Google Scholar
  19. Blackburn TM, Pyšek P, Bacher S et al (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339. Google Scholar
  20. Blaser S, Diem H, von Felten A et al (2018) From laboratory to point of entry: development and implementation of a loop-mediated isothermal amplification (LAMP)-based genetic identification system to prevent introduction of quarantine insect species. Pest Manag Sci. Google Scholar
  21. Bock DG, Caseys C, Cousens RD et al (2015) What we still don’t know about invasion genetics. Mol Ecol 24:2277–2297.Google Scholar
  22. Boissin E, Hurley B, Wingfield MJ et al (2012) Retracing the routes of introduction of invasive species: the case of the Sirex noctilio woodwasp. Mol Ecol 21:5728–5744. Google Scholar
  23. Boychuk EC, Smiley JT, Dahlhoff EP et al (2015) Cold tolerance of the montane Sierra leaf beetle, Chrysomela aeneicollis. J Insect Physiol 81:157–166. Google Scholar
  24. Boykin LM, Armstrong KF, Kubatko L, De Barro P (2012) Species delimitation and global biosecurity. Evol Bioinforma 8:1–37. Google Scholar
  25. Bradburd GS, Coop GM, Peter RL (2018) Inferring continuous and discrete population genetic structure across space. BioRxiv. Google Scholar
  26. Brasier CM, Buck KW (2001) Rapid evolutionary changes in a globally invading fungal pathogen (Dutch elm disease). Biol Invasions 3:223–233. Google Scholar
  27. Bray AM, Bauer LS, Poland TM et al (2011) Genetic analysis of emerald ash borer (Agrilus planipennis Fairmaire) populations in Asia and North America. Biol Invasions 13:2869–2887. Google Scholar
  28. Brightwell RJ, Labadie PE, Silverman J (2010) Northward expansion of the invasive Linepithema humile (Hymenoptera: Formicidae) in the eastern United States is constrained by winter soil temperatures. Environ Entomol 39:1659–1665. Google Scholar
  29. Brockerhoff EG, Liebhold AM (2017) Ecology of forest insect invasions. Biol Invasions 19:3141–3159. Google Scholar
  30. Burban C, Gautier M, Leblois R et al (2016) Evidence for low-level hybridization between two allochronic populations of the pine processionary moth, Thaumetopoea pityocampa (Lepidoptera: Notodontidae). Biol J Linn Soc 119:311–328. Google Scholar
  31. Campbell EO, Brunet BMT, Dupuis JR, Sperling FAH (2018) Would an RSS by any other name sound as RAD? Methods Ecol Evol. Google Scholar
  32. Cao C, Sun L, Wen R et al (2015) Characterization of the transcriptome of the Asian gypsy moth Lymantria dispar identifies numerous transcripts associated with insecticide resistance. Pestic Biochem Phys 119:54–61. Google Scholar
  33. Cao L-J, Wei S-J, Hoffmann AA et al (2016) Rapid genetic structuring of populations of the invasive fall webworm in relation to spatial expansion and control campaigns. Divers Distrib 22:1276–1287. Google Scholar
  34. Carter ME, Smith MT, Turgeon JJ, Harrison RG (2009) Analysis of genetic diversity in an invasive population of Asian long-horned beetles in Ontario, Canada. Can Entomol 141:582–594. Google Scholar
  35. Castalanelli MA, Cunningham RJ, Davis MB et al (2013) When genes go wild: highly variable internal transcibed spacer1 and conserved mitochondrial DNA haplotypes used to examine the genetic diversity and dispersal pathways of invasive Hylotrupes bajulus in Western Australia. Agric For Entomol 15:236–244. Google Scholar
  36. Chown SL, Hodgins KA, Griffin PC et al (2015) Biological invasions, climate change and genomics. Evol Appl 8:23–46. Google Scholar
  37. Clavijo McCormick A, Grosse-Wilde E, Wheeler D et al (2017) Comparing the expression of olfaction-related genes in gypsy moth (Lymantria dispar) adult females and larvae from one flightless and two flight-capabale populations. Front Ecol Evol 5:115. Google Scholar
  38. Cognato AI, Sun J-H, Anducho-Reyes MA, Owen DR (2005) Genetic variation and origin of red turpentine beetle (Dendroctonus valens LeConte) introduced to the People’s Republic of China. Agric For Entomol 7:87–94. Google Scholar
  39. Colautti RI, Lau JA (2015) Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol Ecol 24:1999–2017. Google Scholar
  40. Collins RA, Cruickshank RH (2012) The seven deadly sins of DNA barcoding. Mol Ecol Res 13:969–975. Google Scholar
  41. Comtet T, Sandionigi A, Viard F, Casiraghi M (2015) DNA (meta)barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing aliens. Biol Invasions 17:905–922. Google Scholar
  42. Cornuet JM, Santos F, Beaumont MA et al (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713–2719. Google Scholar
  43. Cristescu ME (2015) Genetic reconstructions of invasion history. Mol Ecol 24:2212–2225. Google Scholar
  44. Cullingham CI, James PMA, Cooke JEK, Coltman DW (2012) Characterizing the physical and genetic structure of the lodgepole pine × jack pine hybrid zone: mosaic structure and differential introgression. Evol Appl 5:879–891. Google Scholar
  45. DAISIE (2009) Handbook on alien species in Europe. In: Drake J (ed) Invading nature, Springer series in invasion ecology, vol 3. Springer, Knoxville, pp 1–26Google Scholar
  46. de Villemereuil P, Frichot É, Bazin É et al (2014) Genome scan methods against more complex models: when and how much should we trust them? Mol Ecol 23:2006–2019. Google Scholar
  47. Dennis AB, Dunning LT, Sinclair BJ, Buckley TR (2015) Parallel molecular routes to cold adaptation in eight genera of New Zealand stick insects. Sci Rep 5:13965. Google Scholar
  48. Derks MFL, Smit S, Salis L et al (2015) The genome of winter moth (Operophtera brumata) provides a genomic perspective on sexual dimorphism and phenology. Genome Biol Evol 7:2321–2332. Google Scholar
  49. deWaard JR, Mitchell A, Keena MA et al (2010) Towards a global barcode library for Lymantria (Lepidoptera: Lymantriinae) tussock moths of biosecurity concern. PLoS ONE 5:1–10. Google Scholar
  50. Djoumad A, Nisole A, Zahiri R et al (2017) Comparative analysis of mitochondrial genomes of geographic variants of the gypsy moth, Lymantria dispar, reveals a previously undescribed genotypic entity. Sci Rep 7:1–12. Google Scholar
  51. Dowle EJ, Bracewell RR, Pfrender ME et al (2017) Reproductive isolation and environmental adaptation shape the phylogeography of mountain pine beetle (Dendroctonus ponderosae). Mol Ecol 26:6071–6084. Google Scholar
  52. Duan J, Ladd T, Doucet D et al (2015) Transcriptome analysis of the emerald ash borer (EAB), Agrilus planipennis: De novo assembly, functional annotation and comparative analysis. PLoS ONE 10:1–19. Google Scholar
  53. Duan X, Wang K, Tian R et al (2017) De novo transcriptome analysis and microsatellite marker development for population genetic study of a serious insect pest, Rhopalosiphum padi (L.) (Hemiptera: Aphididae). PLoS ONE. Google Scholar
  54. Dupuis JR, Roe AD, Sperling FAH (2012) Multi-locus species delimitation in closely related animals and fungi: one marker is not enough. Mol Ecol 21:4422–4436. Google Scholar
  55. Durand E, Jay F, Gaggiotti OE, François O (2009) Spatial inference of admixture proportions and secondary contact zones. Mol Biol Evol 26:1963–1973. Google Scholar
  56. Dwinell LD (1997) The pinewood nematode: regulation and mitigation. Annu Rev Phytopathol 35:153–166. Google Scholar
  57. Ekblom R, Wolf JBW (2014) A field guide to whole-genome sequencing, assembly and annotation. Evol Appl 5:879–891. Google Scholar
  58. Elshire RJ, Glaubitz JC, Sun Q et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379. Google Scholar
  59. Epanchin-Niell RS, Liebhold AM (2015) Benefits of invasion prevention: effect of time lags, spread rates, and damage persistence. Ecol Econ 116:146–153. Google Scholar
  60. Fahrner S, Aukema BH (2018) Correlates of spread rates for introduced insects. Glob Ecol Biogeogr. Google Scholar
  61. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587Google Scholar
  62. Fournier RE, Turgeon JJ (2017) Surveillance during monitoring phase of an eradication programme against Anoplophora glabripennis (Motschulsky) guided by a spatial decision support system. Biol Invasions 19:3013–3035. Google Scholar
  63. Gardy JL, Loman NJ (2017) Towards a genomics-informed, real-time, global pathogen surveillance system. Nat Rev Genet 19:9–20. Google Scholar
  64. Garnas JR, Auger-Rozenberg MA, Roques A et al (2016) Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences. Biol Invasions 18:935–952. Google Scholar
  65. Gayathri Samarasekera GDN, Bartell NV, Lindgren BS et al (2012) Spatial genetic structure of the mountain pine beetle (Dendroctonus ponderosae) outbreak in western Canada: historical patterns and contemporary dispersal. Mol Ecol 21:2931–2948. Google Scholar
  66. Glenn TC (2011) Field guide to next-generation DNA sequencers. Mol Ecol Resour 11:759–769. Google Scholar
  67. Goddard ME, Kemper KE, MacLeod IM et al (2016) Genetics of complex traits: prediction of phenotype, identification of causal polymorphisms and genetic architecture. Proc Biol Sci 283:1173–1186. Google Scholar
  68. Gohli J, Selvarajah T, Kirkendall LR, Jordal BH (2016) Globally distributed Xyleborus species reveal recurrent intercontinental dispersal in a landscape of ancient worldwide distributions. BMC Evol Biol 16:37. Google Scholar
  69. González VL, Devine AM, Trizna M et al (2018) Open access genomic resources for terrestrial arthropods. Curr Opin Insect Sci 25:91–98. Google Scholar
  70. Goodwin S, McPherson JD, McCombie WR (2016) Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet 17:333–351. Google Scholar
  71. Gray DR (2017) Risk analysis of the invasion pathway of the Asian gypsy moth: a known forest invader. Biol Invasions 19:3259–3272. Google Scholar
  72. Grebner DL, Jacobson MG, Fajvan MA (2014) Forest ecosystem services and the scourge of invasive species. J For 112:620–622. Google Scholar
  73. Grubaugh ND, Lander JT, Moritz UG et al (2017) Genomic epidemiology reveals multiple introductions of Zika virus into the United States. Nature 546:401–405. Google Scholar
  74. Gschloessl B, Vogel H, Burban C et al (2014) Comparative analysis of two phenologically divergent populations of the pine processionary moth (Thaumetopoea pityocampa) by de novo transcriptome sequencing. Insect Biochem Mol Biol 46:31–42. Google Scholar
  75. Gschloessl B, Dorkeld F, Berges H et al (2018) Draft genome and reference transcriptomic resources for the urticating pine defoliator Thaumetopoea pityocampa (Lepidoptera: Notodontidae). Mol Ecol Resour 00:1–18. Google Scholar
  76. Gu X-C, Zhang Y-N, Kang K et al (2015) Antennal transcriptome analysis of odorant reception genes in the red turpentine beetle (RTB), Dendroctonus valens. PLoS ONE 10:e0125159. Google Scholar
  77. Gwiazdowski RA, Elkinton JS, Dewaard JR, Sremac M (2013) Phylogeographic diversity of the winter moths Operophtera brumata and O. bruceata (Lepidoptera: Geometridae) in Europe and North America. Ann Entomol Soc Am 106:143–151. Google Scholar
  78. Hajibabaei M, Shokralla S, Zhou X et al (2011) Environmental barcoding: a next-generation sequencing approach for biomonitoring applications using river benthos. PLoS ONE 6:e17497. Google Scholar
  79. Han E-N, Gatehouse AG (1993) Flight capacity: genetic determination and physiological constraints in a migratory moth Mythimna separata. Physiol Entomol 18:183–188. Google Scholar
  80. Havill NP, Shiyake S, Lamb Galloway A et al (2016) Ancient and modern colonization of North America by hemlock woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae), an invasive insect from East Asia. Mol Ecol 25:2065–2080. Google Scholar
  81. Havill NP, Elkinton J, Andersen JC et al (2017) Asymmetric hybridization between non-native winter moth, Operophtera brumata (Lepidoptera: Geometridae), and native bruce spanworm, Operophtera bruceata, in the Northeastern United States, assessed with novel microsatellites and SNPs. Bull Entomol Res 107:241–250. Google Scholar
  82. Hayward SAL, Manso B, Cossins AR (2014) Molecular basis of chill resistance adaptations in poikilothermic animals. J Exp Biol 217:6–15. Google Scholar
  83. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270:313–321. Google Scholar
  84. Hendrickson O (2002) Invasive alien species in Canadian forests. In: Claudi R, Nantel P, Muckle-Jeffs E (eds) Alien invaders in Canada’s waters, wetlands, and forests. Canadian Forest Service, Natural Resources Canada, Ottawa, pp 59–71Google Scholar
  85. Hill MP, Thomson LJ (2015) Species distribution modelling in predicting response to climate change. Climate change and insect pests. CAB International, Wallingford, pp 16–37Google Scholar
  86. Hoban S (2014) An overview of the utility of population simulation software in molecular ecology. Mol Ecol 23:2383–2401. Google Scholar
  87. Hoban S, Bertorelle G, Gaggiotti OE (2011) Computer simulations: tools for population and evolutionary genetics. Nat Rev Genet 13:110–122. Google Scholar
  88. Hoban S, Kelley JL, Lotterhos KE et al (2016) Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am Nat 188:379–397. Google Scholar
  89. i5 K Consortium (2013) The i5 K Initiative: advancing arthropod genomics for knowledge, human health, agriculture, and the environment. J Hered 104:595–600. Google Scholar
  90. Ibáñez I, Diez JM, Miller LP et al (2014) Integrated assessment of biological invasions. Ecol Appl 24:25–37. Google Scholar
  91. Jakubowska A, Nalcacioglu R, Millán-Leiva A et al (2015) In Search of Pathogens: Transcriptome-based identification of viral sequences from the pine processionary oth (Thaumetopoea pityocampa). Viruses 7:456–479. Google Scholar
  92. Janes JK, Li Y, Keeling CI et al (2014) How the mountain pine beetle (Dendroctonus ponderosae) breached the Canadian Rocky Mountains. Mol Biol Evol 31:1803–1815. Google Scholar
  93. Janes JK, Roe AD, Rice AV et al (2016) Polygamy and an absence of fine-scale structure in Dendroctonus ponderosae (Hopk.) (Coleoptera: Curcilionidae) confirmed using molecular markers. Heredity (Edinb) 116:68–74. Google Scholar
  94. Jansen JJ, Allwood JW, Marsden-Edwards E et al (2008) Metabolomic analysis of the interaction between plants and herbivores. Metabolomics 5:150–161. Google Scholar
  95. Jarošík V, Kenis M, Honěk A et al (2015) Invasive insects differ from non-invasives in their thermal requirements. PLoS ONE 10:e0131072. Google Scholar
  96. Javal M, Roques A, Haran J et al (2017) Complex invasion history of the Asian long-horned beetle: fifteen years after first detection in Europe. J Pest Sci. Google Scholar
  97. Joost S, Bonin A, Bruford MW et al (2007) A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Mol Ecol 16:3955–3969. Google Scholar
  98. Ju R-T, Gao L, Wei S-J, Li B (2017) Spring warming increases the abundance of an invasive specialist insect: links to phenology and life history. Sci Rep 7:14805. Google Scholar
  99. Kang TH, Lee K-S, Lee H-S (2015) DNA Barcoding of the Korean Lymantria Hübner, 1819 (Lepidoptera: Erebidae: Lymantriinae) for quarantine inspection. J Econ Entomol 108:1596–1611. Google Scholar
  100. Kang TH, Han SH, Lee HS (2017) Genetic structure and demographic history of Lymantria dispar (Linnaeus, 1758) (Lepidoptera: Erebidae) in its area of origin and adjacent areas. Ecol Evol 7:9162–9178. Google Scholar
  101. Keeling CI, Henderson H, Li M et al (2012) Transcriptome and full-length cDNA resources for the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major insect pest of pine forests. Insect Biochem Mol Biol 42:525–536. Google Scholar
  102. Keeling CI, Yuen MM, Liao NY et al (2013) Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol 14:R27. Google Scholar
  103. Keeling CI, Li M, Sandhu HK et al (2016) Quantitative metabolome, proteome and transcriptome analysis of midgut and fat body tissues in the mountain pine beetle, Dendroctonus ponderosae Hopkins, and insights into pheromone biosynthesis. Insect Biochem Mol Biol 70:170–183. Google Scholar
  104. Keena MA, Côté M-J, Grinberg PS, Wallner WE (2008) World distribution of female flight and genetic variation in Lymantria dispar (Lepidoptera: Lymantriidae). Environ Entomol 37:636–649.[636:wdoffa];2 Google Scholar
  105. Keever CC, Nieman C, Ramsay L et al (2013) Microsatellite population genetics of the emerald ash borer (Agrilus planipennis Fairmaire): comparisons between Asian and North American populations. Biol Invasions 15:1537–1559. Google Scholar
  106. Keller SR, Taylor DR (2010) Genomic admixture increases fitness during a biological invasion. J Evol Biol 23:1720–1731. Google Scholar
  107. Kerdelhué C, Boivin T, Burban C (2014) Contrasted invasion processes imprint the genetic structure of an invasive scale insect across southern Europe. Heredity (Edinb) 113:390–400. Google Scholar
  108. Kethidi DR, Roden DB, Ladd TR et al (2003) Development of SCAR markers for the DNA-based detection of the Asian long-horned beetle, Anoplophora glabripennis (Motschulsky). Arch Insect Biochem Physiol 52:193–204. Google Scholar
  109. Kleynhans E, Mitchell K, Conlong D et al (2014) Evolved variation in cold tolerance among populations of Eldana saccharina (Lepidoptera: Pyralidae) in South Africa. J Evol Biol 27:1149–1159Google Scholar
  110. Kononov A, Ustyantsev K, Blinov A et al (2016) Genetic diversity of aboriginal and invasive populations of four-eyed fir bark beetle Polygraphus proximus Blandford (Coleoptera, Curculionidae, Scolytinae). Agric For Entomol 18:294–301. Google Scholar
  111. Koštál V, Korbelová J, Štětina T et al (2016) Physiological basis for low-temperature survival and storage of quiescent larvae of the fruit fly Drosophila melanogaster. Sci Rep 6:32346. Google Scholar
  112. Landi L, Gómez D, Braccini CL et al (2017) Morphological and molecular identification of the invasive Xylosandrus crassiusculus (Coleoptera: Curculionidae: Scolytinae) and its south American range extending into Argentina and Uruguay. Ann Entomol Soc Am 110:344–349. Google Scholar
  113. Larson K, Duan J (2016) Differences in the reproductive biology and diapause of two congeneric species of egg parasitoides (Hymenoptera: Encyrtidae) from north east Asia: implications for biological control of the invasive emerald ash borer (Coleoptera: Buprestidae). Biol Control 103:39–45. Google Scholar
  114. Lawson DJ, Falush D (2012) Population identification using genetic data. Annu Rev Genom Hum Genet 13:337–361. Google Scholar
  115. Lawson Handley LJ, Estoup A, Evans DM et al (2011) Ecological genetics of invasive alien species. Biocontrol 56:409–428. Google Scholar
  116. Leblois R, Gautier M, Rohfritsch A et al (2018) Deciphering the demographic history of allochronic differentiation in the pine processionary moth Thaumetopoea pityocampa. Mol Ecol 27:264–278. Google Scholar
  117. Lehmann P, Kaunisto S, Koštál V et al (2015) Comparative ecophysiology of cold-tolerance-related traits: assessing range expansion potential for an invasive insect at high latitude. Physiol Biochem Zool 88:254–265Google Scholar
  118. Lemmon AR, Emme SA, Lemmon EM (2012) Anchored hybrid enrichment for massively high-throughput phylogenomics. Syst Biol 61:727–744. Google Scholar
  119. Lesieur V, Lombaert E, Guillemaud T et al (2018) The rapid spread of Leptoglossus occidentalis in Europe: a bridgehead invasion. J Pest Sci. Google Scholar
  120. Leung B, Lodge DM, Finnoff D et al (2002) An ounce of prevention or a pound of cure: Bioeconomic risk analysis of invasive species. Proc Biol Sci 269:2407–2413. Google Scholar
  121. Li F, Wang R, Qu C et al (2016) Sequencing and characterization of the invasive sycamore lace bug Corythucha ciliata (Hemiptera: Tingidae) transcriptome. PLoS ONE 11:e0160609. Google Scholar
  122. Li F-Q, Fu N-N, Qu C et al (2017) Understanding the mechanisms of dormancy in an invasive alien Sycamore lace bug, Corythucha ciliata through transcript and metabolite profiling. Sci Rep 7:2631. Google Scholar
  123. Lin T, Cai Z, Wu H (2015) Transcriptome analysis of the Japanese pine sawyer beetle, Monochamus alternatus (Coleoptera: Cerambycidae) by high-throughput Illumina sequencing. J Asia Pac Entomol 18:439–445. Google Scholar
  124. Liu Z, Tao J, Luo Y (2017) Development and characterization of polymorphic genomic-SSR markers in Asian long-horned beetle (Anoplophora glabripennis). Bull Entomol Res 107:749–755. Google Scholar
  125. Liu N-Y, Li Z-B, Zhao N et al (2018) Identification and characterization of chemosensory gene families in the bark beetle, Tomicus yunnanensis. Comp Biochem Physiol Part D Genom Proteom 25:73–85. Google Scholar
  126. Lo N, Montagu A, Noack A et al (2018) Population genetics of the Australian eucalypt pest Thaumastocoris peregrinus: evidence for a recent invasion of Sydney. J Pest Sci. Google Scholar
  127. Lodge DM, Williams S, MacIsaac HJ et al (2006) Biological invasions: recommendations for U.S. policy and management. Ecol Appl 16:2035–2054.[2035:BIRFUP]2.0.CO;2 Google Scholar
  128. Lombaert E, Estoup A, Facon B et al (2014) Rapid increase in dispersal during range expansion in the invasive ladybird Harmonia axyridis. J Evol Biol 27:508–517. Google Scholar
  129. Loo JA (2009) Ecological impacts of non-indigenous invasive fungi as forest pathogens. Biol Invasions 11:81–96. Google Scholar
  130. Lord NP, Plimpton RL, Sharkey CR et al (2016) A cure for the blues: opsin duplication and subfunctionalization for short-wavelength sensitivity in jewel beetles (Coleoptera: Buprestidae). BMC Evol Biol 16:107. Google Scholar
  131. Lowry DB (2010) Landscape evolutionary genomics. Biol Lett 6:502–504. Google Scholar
  132. Lugo AE (2015) Forestry in the Anthropocene. Science 349:771. Google Scholar
  133. Macke E, Tasiemski A, Massol F et al (2017) Life history and eco-evolutionary dynamics in light of the gut microbiota. Oikos 126:508–531. Google Scholar
  134. Maino JL, Kong JD, Hoffmann AA et al (2016) Mechanistic models for predicting insect responses to climate change. Curr Opin Insect Sci 17:81–86. Google Scholar
  135. Malacrinò A, Rassati D, Schena L et al (2017) Fungal communities associated with bark and ambrosia beetles trapped at international harbours. Fungal Ecol 28:44–52. Google Scholar
  136. Mamidala P, Wijeratne AJ, Wijeratne S et al (2013) Identification of odor-processing genes in the emerald ash borer, Agrilus planipennis. PLoS ONE 8:56555. Google Scholar
  137. Märtens K, Hallin J, Warringer J et al (2016) Predicting quantitative traits from genome and phenome with near perfect accuracy. Nat Commun 7:11512. Google Scholar
  138. Mason CJ, Scully ED, Geib SM, Hoover K (2016) Contrasting diets reveal metabolic plasticity in the tree-killing beetle, Anoplophora glabripennis (Cerambycidae: Lamiinae). Sci Rep 6:33813. Google Scholar
  139. McCormack JE, Faircloth BC (2013) Next-generation phylogenetics takes root. Mol Ecol 22:19–21. Google Scholar
  140. McKenna DD, Scully ED, Pauchet Y et al (2016) 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 17:227. Google Scholar
  141. McVean G (2009) A Genealogical interpretation of principal components analysis. PLoS Genet 5:e1000686. Google Scholar
  142. Millar CI, Stephenson NL (2015) Temperate forest health in an era of emerging megadisturbance. Science 349:823–826. Google Scholar
  143. Miller KE, Hopkins K, Inward DJG, Vogler AP (2016) Metabarcoding of fungal communities associated with bark beetles. Ecol Evol 6:1590–1600. Google Scholar
  144. Mitchell RF, Hughes DT, Luetje CW et al (2012) Sequencing and characterizing odorant receptors of the cerambycid beetle Megacyllene caryae. Insect Biochem Mol Biol 42:499–505. Google Scholar
  145. Mitchell RF, Hall LP, Reagel PF et al (2017) Odorant receptors and antennal lobe morphology offer a new approach to understanding olfaction in the Asian longhorned beetle. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 203:99–109. Google Scholar
  146. Mittapalli O, Bai X, Mamidala P et al (2010) Tissue-specific transcriptomics of the exotic invasive insect pest emerald ash borer (Agrilus planipennis). PLoS ONE 5:13708. Google Scholar
  147. Mock KE, Bentz BJ, O’neill EM et al (2007) Landscape-scale genetic variation in a forest outbreak species, the mountain pine beetle (Dendroctonus ponderosae). Mol Ecol 16:553–568. Google Scholar
  148. Nackley LL, West AG, Skowno AL, Bond WJ (2017) The nebulous ecology of native invasions. Trends Ecol Evol 32:814–824. Google Scholar
  149. Nadeau JA, Petereit J, Tillett RL et al (2017) Comparative transcriptomics of mountain pine beetle pheromone-biosynthetic tissues and functional analysis of CYP6DE3. BMC Genom 18:311. Google Scholar
  150. Nealis VG, Cooke BJ (2014) Risk assessment of the threat of mountain pine beetle to Canada’s boreal and eastern pine forests. Canadian Council of Forest Ministers, Ottawa, p 27Google Scholar
  151. Nielsen R, Akey JM, Jakobsson M et al (2017) Tracing the peopling of the world through genomics. Nature 541:302–310. Google Scholar
  152. Novembre J, Stephens M (2008) Interpreting principal component analyses of spatial population genetic variation. Nat Genet 40:646–649. Google Scholar
  153. Novembre J, Johnson T, Bryc K et al (2008) Genes mirror geography within Europe. Nature 456:89–101. Google Scholar
  154. Papadopoulou A, Taberlet P, Zinger L (2015) Metagenome skimming for phylogenetic community ecology: A new era in biodiversity research. Mol Ecol 14:3515–3517. Google Scholar
  155. Pardo-Diaz C, Salazar C, Jiggins CD (2015) Towards the identification of the loci of adaptive evolution. Methods Ecol Evol 6:445–464. Google Scholar
  156. Pauchet Y, Kirsch R, Giraud S et al (2014) Identification and characterization of plant cell wall degrading enzymes from three glycoside hydrolase families in the cerambycid beetle Apriona japonica. Insect Biochem Mol Biol 49:1–13. Google Scholar
  157. Philibert A, Desprez-Loustau M-L, Fabre B et al (2011) Predicting invasion success of forest pathogenic fungi from species traits. J Appl Ecol 48:1381–1390. Google Scholar
  158. Philippe H, Brinkmann H, Lavrov DV et al (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol. Google Scholar
  159. Philippe H, de Vienne DM, Ranwez V et al (2017) Pitfalls in supermatrix phylogenomics. Eur J Taxon 283:1–25. Google Scholar
  160. Picq S, Keena M, Havill N et al (2017) Assessing the potential of genotyping-by-sequencing-derived single nucleotide polymorphisms to identify the geographic origins of intercepted gypsy moth (Lymantria dispar) specimens: a proof-of-concept study. Evol Appl 11:325–339. Google Scholar
  161. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  162. Raj A, Stephens M, Pritchard JK (2014) fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197:573–589. Google Scholar
  163. Rajarapu SP, Mamidala P, Herms DA et al (2011) Antioxidant genes of the emerald ash borer (Agrilus planipennis): Gene characterization and expression profiles. J Insect Physiol 57:819–824. Google Scholar
  164. Rellstab C, Gugerli F, Eckert AJ et al (2015) A practical guide to environmental association analysis in landscape genomics. Mol Ecol 24:4348–4370. Google Scholar
  165. Ricciardi A, Blackburn TM, Carlton JT et al (2017) Invasion science: looking forward rather than revisiting old ground: a reply to Zenni et al. Trends Ecol Evol 32:809–810. Google Scholar
  166. Richards S, Murali SC (2015) Best practices in insect genome sequencing: what works and what doesn’t. Curr Opin Insect Sci 7:1–7. Google Scholar
  167. Rius M, Bourne S, Hornsby HG, Chapman MA (2015) Applications of next-generation sequencing to the study of biological invasions. Curr Zool 61:488–504. Google Scholar
  168. Robert JA, Bonnett T, Pitt C et al (2016) Gene expression analysis of overwintering mountain pine beetle larvae suggests multiple systems involved in overwintering stress, cold hardiness, and preparation for spring development. PeerJ 4:2109. Google Scholar
  169. Rodrigues TB, Rieske LK, Duan J et al (2017) Development of RNAi method for screening candidate genes to control emerald ash borer, Agrilus planipennis. Sci Rep 7:7379. Google Scholar
  170. Rodriguez-Castañeda G, MacVean C, Cardona C, Hof AR (2017) What limits the distribution of Liriomyza huidobrensis and its congener Liriomyza sativae in their native niche: when temperature and competition affect species’ distribution range in Guatemala. J Insect Sci 17:88–101. Google Scholar
  171. Ryan K, de Groot P, Davis C, Smith SM (2012) Effect of two bark beetle-vectored fungi on the on-host search and oviposition behavior of the introduced woodwasp Sirex noctilio (Hymenoptera: Siricidae) on Pinus sylvestris trees and logs. J Insect Behav 25:453–466. Google Scholar
  172. Safranyik L, Wilson B (2006) Effects of the mountain pine beetle on lodgepole pine stand structure and dynamics. Canadian Forest Service, Natural Resources Canada, VictoriaGoogle Scholar
  173. Salvato P, Battisti A, Concato S et al (2002) Genetic differentiation in the winter pine processionary moth (Thaumetopoea pityocampa-wilkinsoni complex), inferred by AFLP and mitochondrial DNA markers. Mol Ecol 11:2435–2444. Google Scholar
  174. Santos H, Burban C, Rousselet J et al (2011) Incipient allochronic speciation in the pine processionary moth (Thaumetopoea pityocampa, Lepidoptera, Notodontidae). J Evol Biol 24:146–158. Google Scholar
  175. Schoville SD, Bonin A, François O et al (2012) Adaptive genetic variation on the landscape: methods and cases. Annu Rev Ecol Evol Syst 43:23–43. Google Scholar
  176. Scully ED, Geib SM, Hoover K et al (2013) Metagenomic profiling reveals lignocellulose degrading system in a microbial community associated with a wood-feeding beetle. PLoS ONE 8:73827. Google Scholar
  177. Scully ED, Geib SM, Carlson JE et al (2014) Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal insights into the digestive physiology and nutritional ecology of wood feeding beetles. BMC Genom 15:1096. Google Scholar
  178. Slippers B, Hurley BP, Wingfield MJ (2015) Sirex woodwasp: a model for evolving management paradigms of invasive forest pests. Annu Rev Entomol 60:601–619. Google Scholar
  179. Sparks ME, Blackburn MB, Kuhar D, Gundersen-Rindal DE (2013) Transcriptome of the Lymantria dispar (gypsy moth) larval midgut in response to infection by Bacillus thuringiensis. PLoS ONE 8:61190. Google Scholar
  180. Sperling F, Roe A (2009) Molecular dimensions of insect taxonomy. In: Foottit R, Adler P (eds) Insect biodiversity: science and society. Wiley-Blackwell, West Sussex, pp 397–417Google Scholar
  181. Stewart D, Zahiri R, Djoumad A et al (2016) A multi-species TaqMan PCR assay for the identification of Asian gypsy moths (Lymantria spp.) and other invasive lymantriines of biosecurity concern to North America. PLoS ONE 11:0160878. Google Scholar
  182. Storer C, Payton A, McDaniel S et al (2017) Cryptic genetic variation in an inbreeding and cosmopolitan pest, Xylosandrus crassiusculus, revealed using ddRADseq. Ecol Evol 7:10974–10986. Google Scholar
  183. Storz JF, Bridgham JT, Kelly SA, Garland T Jr. (2015) Genetic approaches in comparative and evolutionary physiology. Am J Physiol Regul Integr Comp Physiol 309:R197–R214Google Scholar
  184. Streifel MA, Tobin PC, Hunt L et al (2017) Landscape-level patterns of elevated fs1 Asian allele frequencies in populations of gypsy moth (Lepidoptera: Erebidae) at a northern U.S. boundary. Environ Entomol 46:403–412. Google Scholar
  185. Suez M, Gidoin C, Lefèvre F et al (2013) Temporal population genetics of time travelling insects: a long term study in a seed-specialized wasp. PLoS ONE 8:0070818. Google Scholar
  186. Taberlet P, Coissac E, Pompanon F et al (2012a) Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol 21:2045–2050. Google Scholar
  187. Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH (2012b) Environmental DNA. Mol Ecol 21:1789–1793. Google Scholar
  188. Taerum SJ, Konečný A, de Beer ZW et al (2016) Population genetics and symbiont assemblages support opposing invasion scenarios for the red turpentine beetle (Dendroctonus valens). Biol J Linn Soc 118:486–502. Google Scholar
  189. Teets NM, Peyton JT, Ragland GJ et al (2012) Combined transcriptomic and metabolomic approach uncovers molecular mechanisms of cold tolerance in a temperate flesh fly. Physiol Genom 44:764–777. Google Scholar
  190. Todd EV, Black MA, Gemmell NJ (2016) The power and promise of RNA-seq in ecology and evolution. Mol Ecol 25:1224–1241. Google Scholar
  191. Tremblay E, Duceppe M-O, Kimoto T et al (2017) Development of a NGS-based detection method to identify exotic forest pathogens from fungal spores suspended in air and occurring on insect vectors. Phytopathology 107(S5):206. Google Scholar
  192. Trucchi E, Mazzarella AB, Gilfillan GD et al (2016) BsRADseq: screening DNA methylation in natural populations of non-model species. Mol Ecol 25:1697–1713. Google Scholar
  193. Trumbore S, Brando P, Hartmann H et al (2015) Forest health and global change. Science 349:814Google Scholar
  194. Valade R, Kenis M, Hernandez-Lopez A et al (2009) Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae). Mol Ecol 18:3458–3470. Google Scholar
  195. van Buijtenen JP (2001) Genomics and quantitative genetics. Can J For Res 31:617. Google Scholar
  196. Walther TC, Mann M (2010) Mass spectrometry-based proteomics in cell biology. J Cell Biol 190:491–500. Google Scholar
  197. Wang J, Li D-Z, Min S-F et al (2014) Analysis of chemosensory gene families in the beetle Monochamus alternatus and its parasitoid Dastarcus helophoroides. Comp Biochem Physiol Part D Genom Proteom 11:1–8. Google Scholar
  198. Wittenberg R, Cock MJW (2001) Invasive alien species: a toolkit of best prevention and management practices. CAB International, Wallingford, p xvii-228. Google Scholar
  199. Wondafrash M, Slippers B, Garnas J et al (2016) Identification and genetic diversity of two invasive Pissodes spp. Germar (Coleoptera: Curculionidae) in their introduced range in the southern hemisphere. Biol Invasion 18:2283–2297. Google Scholar
  200. Wu Y, Molongoski JJ, Winograd DF et al (2015) Genetic structure, admixture and invasion success in a Holarctic defoliator, the gypsy moth (Lymantria dispar, Lepidoptera: Erebidae). Mol Ecol 24:1275–1291. Google Scholar
  201. Wu S, Zhu X, Liu Z et al (2016) Identification of genes relevant to pesticides and biology from global transcriptome data of Monochamus alternatus Hope (Coleoptera: Cerambycidae) larvae. PLoS ONE 11:0147855. Google Scholar
  202. Wu Y, Trepanowski NF, Molongoski JJ et al (2017) Identification of wood-boring beetles (Cerambycidae and Buprestidae) intercepted in trade-associated solid wood packaging material using DNA barcoding and morphology. Sci Rep 7:40316. Google Scholar
  203. Xiaojun F, Chun Y, Jianhong L et al (2017) Sequencing and de novo assembly of the Asian gypsy moth transcriptome using the Illumina platform. Genet Mol Biol 40:160–167. Google Scholar
  204. Yang Z, Rannala B (2017) Bayesian species identification under the multispecies coalescent provides significant improvements to DNA barcoding analyses. Mol Ecol. Google Scholar
  205. Yang W-Y, Tang X-T, Ju R-T et al (2017) The population genetic structure of Corythucha ciliata (Say) (Hemiptera: Tingidae) provides insights into its distribution and invasiveness. Sci Rep 7:635. Google Scholar
  206. Yemshanov D, Koch FH, Ducey M, Koehler K (2012) Trade-associated pathways of alien forest insect entries in Canada. Biol Invasions 14:797–812. Google Scholar
  207. Yin C, Shen G, Guo D et al (2016) InsectBase: a resource for insect genomes and transcriptomes. Nucleic Acids Res 44:D801–D807. Google Scholar
  208. Zhang Q, Lu Y-X, Xu W-H (2013) Proteomic and metabolomic profiles of larval hemolymph associated with diapause in the cotton bollworm, Helicoverpa armigera. BMC Genom 14:751. Google Scholar
  209. Zhang L-W, Kang K, Jiang S-C et al (2016) Analysis of the antennal transcriptome and insights into olfactory genes in Hyphantria cunea (Drury). PLoS ONE 11:e0164729. Google Scholar
  210. Zhang W, Meng J, Ning J et al (2017) Differential immune responses of Monochamus alternatus against symbiotic and entomopathogenic fungi. Sci China Life Sci 60:902–910. Google Scholar
  211. Zhou J, Yu H-Y, Zhang W et al (2017) Comparative analysis of the Monochamus alternatus immune system. Insect Sci. Google Scholar
  212. Zhu J-Y, Zhao N, Yang B (2012) Global transcriptome profiling of the pine shoot beetle, Tomicus yunnanensis (Coleoptera: Scolytinae). PLoS ONE 7:32291. Google Scholar

Copyright information

© Crown 2018

Authors and Affiliations

  • Amanda D. Roe
    • 1
    Email author
  • Alex S. Torson
    • 2
  • Guillaume Bilodeau
    • 3
  • Pierre Bilodeau
    • 3
  • Gwylim S. Blackburn
    • 4
    • 5
  • Mingming Cui
    • 4
    • 6
    • 10
  • Michel Cusson
    • 5
  • Daniel Doucet
    • 1
  • Verena C. Griess
    • 7
  • Valentine Lafond
    • 7
  • Gregory Paradis
    • 7
  • Ilga Porth
    • 4
    • 6
    • 10
  • Julien Prunier
    • 4
  • Vivek Srivastava
    • 7
  • Emilie Tremblay
    • 3
  • Adnan Uzunovic
    • 8
  • Denys Yemshanov
    • 1
  • Richard C. Hamelin
    • 9
  1. 1.Natural Resources CanadaCanadian Forest ServiceSault Ste. MarieCanada
  2. 2.Department of BiologyWestern UniversityLondonCanada
  3. 3.Canadian Food Inspection AgencyOttawaCanada
  4. 4.L’Institut de biologie intégrative et des systèmesUniversité LavalQuébec CityCanada
  5. 5.Natural Resource Canada - Canadian Forest ServiceQuébec CityCanada
  6. 6.Département des sciences du bois et de la forêtUniversité LavalQuébecCanada
  7. 7.Department of Forest Resources ManagementUniversity of British ColumbiaVancouverCanada
  8. 8.FPInnovationsVancouverCanada
  9. 9.Department of Forest and Conservation ScienceUniversity of British ColumbiaVancouverCanada
  10. 10.Centre d’étude de la forêtUniversité LavalQuébecCanada

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