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Tracking Outbreak Populations of the Pepper Weevil Anthonomus Eugenii (Coleoptera; Curculionidae) Using Complete Mitochondrial Genomes

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Tracking Outbreak Populations of the Pepper Weevil Anthonomus Eugenii (Coleoptera; Curculionidae) Using Complete Mitochondrial Genomes RESEARCH ARTICLE Tracking outbreak populations of the pepper weevil Anthonomus eugenii (Coleoptera; Curculionidae) using complete mitochondrial genomes 1 1 2 Bart T. L. H. van de VossenbergID *, Tim Warbroek , Joseph Ingerson-Mahar , Cees Waalwijk3, Lucas P. van der Gouw1, Bernadette Eichinger2, Antoon J. M. Loomans1 1 National Reference Centre of plant health, Dutch National Plant Protection Organization, Wageningen, a1111111111 Gelderland, the Netherlands, 2 Department of Entomology, Rutgers University, New Brunswick, New Jersey, a1111111111 United States of America, 3 Biointeractions and Plant health, Wageningen University & Research, a1111111111 Wageningen, Gelderland, the Netherlands a1111111111 * [email protected] a1111111111 Abstract OPEN ACCESS The pepper weevil, Anthonomus eugenii, is a major pest on Capsicum species. Apart from natural spread, there is a risk of spread via international pepper trade. In the Netherlands, a Citation: van de Vossenberg BTLH, Warbroek T, Ingerson-Mahar J, Waalwijk C, van der Gouw LP, pepper weevil outbreak occurred in 2012 and affected six greenhouses producing different Eichinger B, et al. (2019) Tracking outbreak sweet pepper varieties. The following year, a pepper weevil outbreak occurred in Italy. To populations of the pepper weevil Anthonomus trace the origin of the Dutch outbreak and to establish if the Dutch and Italian outbreaks eugenii (Coleoptera; Curculionidae) using complete mitochondrial genomes. PLoS ONE 14(8): were linked, we determined the mitogenomes of A. eugenii specimens collected at outbreak e0221182. https://doi.org/10.1371/journal. locations, and compared these with specimens from the native area, and other areas where pone.0221182 the pest was introduced either by natural dispersal or via trade. The circular 17,257 bp A. Editor: Tzen-Yuh Chiang, National Cheng Kung eugenii mitogenome comprises thirteen mitochondrial genes typically found in insect spe- University, TAIWAN cies. Intra-species variation of these mitochondrial genes revealed four main mitochondrial Received: May 17, 2019 lineages encompassing 41 haplotypes. The highest diversity was observed for specimens Accepted: July 31, 2019 from its presumed native area (i.e. Mexico). The Dutch outbreak specimens represented three highly similar haplotypes, suggesting a single introduction of the pest. The major Published: August 14, 2019 Dutch haplotype was also found in two specimens from New Jersey. As the Netherlands Copyright: © 2019 van de Vossenberg et al. This is does not have pepper trade with New Jersey, it is likely that the specimens sampled in New an open access article distributed under the terms of the Creative Commons Attribution License, Jersey and those sampled in the Netherlands originate from a shared source that was not which permits unrestricted use, distribution, and included in this study. In addition, our analysis shows that the Italian and Dutch outbreaks reproduction in any medium, provided the original were not linked. The mitochondrial genome is a useful tool to trace outbreak populations author and source are credited. and the methodology presented in this paper could prove valuable for other invasive pest Data Availability Statement: Mitogenomes of the species, such as the African fruit moth Thaumatotibia leucotreta and emerald ash borer reference specimens were submitted in NCBI Agrilus planipennis. under accession numbers MK654676 (Anthonomus eugenii), MK654677 (Anthonomus pomorum), MK654678 (Anthonomus rectirostris), and MK654679 (Anthonomus rubi). Gene sequences of atp6, atp8, cytb, cox1, cox2, cox3, nad1, nad2, nad3, nad4, nad4L, nad5, and nad6 of the 137 Anthonomus spp. specimens included in PLOS ONE | https://doi.org/10.1371/journal.pone.0221182 August 14, 2019 1 / 15 Tracking Anthonomus eugenii outbreaks using complete mitogenomes the analysis were submitted in NCBI under Introduction accession numbers MK652895 to MK654675. The pepper weevil, Anthonomus eugenii Cano (Coleoptera: Curculionidae), is considered as Funding: This work was supported by the one of the most important pests on cultivated peppers (Capsicum spp.), because of damage Netherlands Food and Consumer Product Safety caused by direct feeding on the fruits [1]. Larvae feed on soft tissues inside the developing Authority grant OS_20141027 to Mr Bart T.L.H. van de Vossenberg and Mr. Cees Waalwijk. The fruit, whereas adults feed on flowers and young fruits. Presence of the pest results in malforma- funders had no role in study design, data collection tion, premature ripening and abscission of fruits [2], and losses of 33% to 100% have been and analysis, decision to publish, or preparation of reported [3, 4]. Cultivated peppers are the main host for A. eugenii, but the pest can also com- the manuscript. plete its lifecycle on several other solanaceous species, such as: Solanum melongena (egg- Competing interests: The authors have declared plant), Solanum rostratum (buffalobur nightshade) and Solanum nigrum (black nightshade) that no competing interests exist. [5]. Because of its impact, A. eugenii is listed as quarantine pest in several European, South- American and African countries [6]. Based on the earliest reports of the pepper weevil and its hosts, it is generally believed that the species originates from Mexico or surrounding regions in Central America [7]. Today, A. eugenii is a major pest species on peppers in Mexico, the southern United States, central Amer- ica, and the Caribbean [8]. Apart from its natural range, the pest has been found outdoors in Hawaii in 1933 [1], French Polynesia pre-1986 [9], Puerto Rico in 1982 [10], and the Domini- can Republic in 2006 [11]. The pest was also encountered in greenhouses in southern Canada in 1992 [12] and again in 2009 and 2010 [13]. Similarly, the pest was found in greenhouses in the Netherlands (2012) [14] and Italy (2013) [15], where in the latter country the pest was also found outdoors. In these cases, the infestations are believed to be associated with the import of Capsicum and/or Solanum fruits, or plants for planting. For the European Union the risk of infestation from the import of Capsicum and Solanum fruits was initially regarded as low (but with a high uncertainty), as import of host fruits from countries in which the pest is endemic occurs since at least 1988 and no outbreaks had taken place since [16]. In the Netherlands, A. eugenii was first intercepted on eggplant fruits from the Dominican Republic in 1999 [17], and since then the pest has been intercepted numerous times from Mexico and the Dominican Republic at import inspections. The first and only out- break of A. eugenii in the Netherlands was in July 2012 when the pest was found in four green- houses producing sweet pepper (Capsicum annuum) fruit in the province of Zuid-Holland [14]. In October and November of the same year, two additional greenhouses were found to be infested. All infested greenhouses were situated close to each other (2 km radius) and a surveil- lance program was initiated. Eradication measures were taken against A. eugenii which included the application of pesticides, and the destruction and secured removal of plants and growing medium in all infested greenhouses. The National Plant Protection Organization declared that the pest was successfully eradicated in the Netherlands in December 2013 [18]. In Italy, the pest was declared eradicated in 2018 [19]. The mitochondrial genome is frequently used in phylogenetic [20, 21] and population-level studies [22, 23] as it typically represents a single maternally inherited molecule with low levels of recombination while being present in high copy numbers [24, 25]. With the introduction of next generation sequencing technology, the number of annotated complete mitogenomes has increased tremendously [26]. For instance, higher level phylogenetic relationships in the weevils (Curculionoidea), were determined by generating and analyzing close to one hundred (near) complete mitochondrial genomes from a single Illumina MiSeq run [27]. For the weevil tribe Anthonomini, one complete mitogenome, namely that of Bradybatus kellneri (KX087247), and two partial mitogenomes, those of Anthonomus pomorum (JN163951) and Anthonomus grandis (MG253256) are present in the public domain. To place the A. eugenii intraspecies variation in the context of other Anthonomus species, the mitogenomes of specimens of A. pomorum, Anthonomus rectirostris and Anthonomus rubi were assembled and included in this study. PLOS ONE | https://doi.org/10.1371/journal.pone.0221182 August 14, 2019 2 / 15 Tracking Anthonomus eugenii outbreaks using complete mitogenomes Material and methods Insect specimens Following the Dutch 2012 outbreak, 32 specimens of A. eugenii were obtained from the affected greenhouses. Over fifty production sites of sweet pepper (C. annuum) fruit in an area of 4 x 9 km around the infested facilities were included in a follow-up survey in which pheromone traps (male aggregation pheromone in combination with a yellow sticky trap) were placed in primary production locations. These traps were also placed in greenhouses producing tomatoes, egg- plants or ornamental Solanaceae within an area of 2 x 3 km around the infested sites. In addition, specimens from regular import inspections performed by the Dutch National Plant Protection Organization (NPPO-NL), and from collections as well as and specimens obtained from external contacts were included to create a reference panel of 135 A. eugenii specimens. Three A. piri, six A. pomorum, three
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