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A first inference of the phylogeography of the worldwide invader Xylosandrus compactus

Abstract

Native to Southeastern Asia, the ambrosia beetle Xylosandrus compactus is invasive worldwide. Its invasion is favoured by its cryptic lifestyle, symbiosis with a fungus that facilitates a broad range of host plants, and predominant sib-mating reproduction. X. compactus invaded Africa more than a century ago and the Americas and Pacific Islands in the middle of the twentieth century. It was not detected in Europe before 2011, when it was first reported in Italy before quickly spreading to France, Greece and Spain. Despite the negative environmental, agricultural and economic consequences of the invasion of X. compactus, its invasion history and main pathways remain poorly documented. We used COI and RAD sequencing to (i) characterise the worldwide genetic structure of the species, (ii) disentangle the origin(s) of the non-native populations on the three invaded continents and (iii) analyse the genetic diversity and pathways within each invaded region. Three mitochondrial lineages were identified in the native range. Populations invading Europe and the American-Pacific region originated from the first lineage and were only slightly genetically differentiated at nuclear SNP markers, suggesting independent introductions from close sources in or near Shanghai, ca. 60 years apart. Populations invading Africa originated from the second lineage, likely from India or Vietnam.

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Availability of data and material

Individual RAD sequence files are available in a fq.gz format at the Sequence Read Archive (SRA) (Study Accession no. PRJNA771401). The VCF files Xylosandruscompactus.vcf and Ambrosiellaxylebori.vcf used for population genomic analyses, as well as the popmap used in STACK’ population module and specimens' metadata (e.g., GPS coordinates) are available on Portail Data INRAE (https://doi.org/10.15454/ETBWEP). The Genbank accession numbers for the mitochondrial haplotypes reported in this paper are OK489329:OK489334.

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Acknowledgements

We would like to thank Richard Bellanger, Jared Bernard, Jean-Baptiste Daubrée, Jacques Deleuze, Massimo Faccoli, Steve Frank, Lei Gao (Shanghai Academy of Landscape Architecture Science and Planning), Benjamin Gey, Federica Giarruzzo, Fabrice Pinard, and Giovanna Tropea for sending specimens. We also would like to thank Anne Loiseau for the laboratory work. We are grateful to MGX-Montpellier GenomiX for sequencing the RAD libraries and to the Genotoul bioinformatics platform Toulouse Occitanie (Bioinfo Genotoul, https://doi.org/10.15454/1.5572369328961167E12) for providing computing and storage resources. We are also grateful to the Sino-French Joint Laboratory for Invasive Forest Pests in Eurasia (IFOPE) for its support.

Funding

This work was supported by the LIFE project SAMFIX (SAving Mediterranean Forests from Invasions of Xylosandrus beetles and associated pathogenic fungi, LIFE17 NAT/IT/000609, https://www.lifesamfix.eu/) which received funding from the European Union’s LIFE Nature and Biodiversity programme. JH and AJJ were supported by the US Forest Service, the USDA APHIS, and the National Science Foundation.

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The authors declare no conflict of interests. Specimens sampled did not involve endangered nor protected species.

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Urvois, T., Perrier, C., Roques, A. et al. A first inference of the phylogeography of the worldwide invader Xylosandrus compactus. J Pest Sci (2021). https://doi.org/10.1007/s10340-021-01443-7

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Keywords

  • Bioinvasion
  • Invasion route
  • Black twig borer
  • COI
  • RAD sequencing
  • Ambrosia beetle