Serial Invasions of the Winter Moth, Operophtera Brumata, to North America

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Serial Invasions of the Winter Moth, Operophtera Brumata, to North America Received: 21 December 2020 | Revised: 7 May 2021 | Accepted: 10 May 2021 DOI: 10.1111/mec.15983 ORIGINAL ARTICLE Four times out of Europe: Serial invasions of the winter moth, Operophtera brumata, to North America Jeremy C. Andersen1 | Nathan P. Havill2 | Adalgisa Caccone3 | Joseph S. Elkinton1 1Department of Environmental Conservation, University of Abstract Massachusetts, Amherst, MA, USA Reconstructing the geographic origins of non- native species is important for study- 2Northern Research Station, USDA Forest Service, Hamden, CT, USA ing the factors that influence invasion success, however; these analyses can be con- 3Department of Ecology & Evolutionary strained by the amount of diversity present in the native and invaded regions, and by Biology, Yale University, New Haven, CT, changes in the genetic background of the invading population following bottlenecks USA and/or hybridization events. Here we explore the geographical origins of the invasive Correspondence winter moth (Operopthera brumata L.) that has caused widespread defoliation to for- Jeremy C. Andersen, Department of Environmental Conservation, University of ests, orchards, and crops in Nova Scotia, British Columbia, Oregon, and the northeast- Massachusetts, Amherst, MA, USA. ern United States. It is not known whether these represent independent introductions Email: [email protected] to North America, or a “stepping stone” spread among regions. Using a combination of Funding information Bayesian assignment and approximate Bayesian computation methods, we analysed a U.S. Forest Service, Grant/Award Number: 17- CR- 11242303- 066; Animal and population genetic data set of 24 microsatellite loci. We estimate that winter moth was Plant Health Inspection Service, Grant/ introduced to North America on at least four occasions, with the Nova Scotian and Award Number: AP17PPQS&T00C068, AP18PPQS&T00C070 and British Columbian populations probably being introduced from France and Sweden, AP19PPQFO000C125 respectively; the Oregonian population probably being introduced from either the British Isles or northern Fennoscandia; and the population in the northeastern United States probably being introduced from somewhere in Central Europe. We discuss the impact of genetic bottlenecks on analyses meant to determine region of origin. KEYWORDS approximate Bayesian computation, biosecurity, invasion routes, microsatellites invasive species, Operopthera brumata, population genetics 1 | INTRODUCTION it is often unclear whether the species is a serial invader (i.e., each population was introduced independently) or whether the separate In light of the unprecedented number of introductions of non- native populations represent establishment from within the invasive re- species (Mack et al., 2000), one of the most pressing research needs gions under a “stepping stone” model (see Cerwenka et al., 2014; for evolutionary biologists and ecologists is to identify the factors Lombaert et al., 2010; Oficialdegui et al., 2019; Tonione et al., 2011 that influence the establishment of species that have negative eco- for examples). Identifying which mode of introduction occurred (se- logical and economic impacts (Suarez & Tsutsui, 2008). Multiple rial invader or stepping stone) is therefore necessary for the study introductions (Dlugosch & Parker, 2008), including cryptic ones of genetic and ecological factors that drive invasion success as inde- (Roman, 2006), are thought to play an important role in providing pendent populations are required for robust hypothesis- based test- the diversity required to overcome genetic bottlenecks associated ing (Kang et al., 2007) – information that is also crucial for focusing with the establishment of populations in novel ecosystems (Darling management efforts (Floerl et al., 2009). et al., 2008; Facon et al., 2008). However, when multiple geographi- When reconstructing regions of origins, and determining the cally disjunct populations of an invasive species become established, numbers of introductions of a focal organism, historical records Molecular Ecology. 2021;30:3439–3452. wileyonlinelibrary.com/journal/mec © 2021 John Wiley & Sons Ltd | 3439 3440 | ANDERSEN ET AL. should be referenced and robust genetic analyses performed (e.g., was introduced to North America, and when possible, determine Lynch & Saltonstall, 2002; Schwenk et al., 2008). Unfortunately, the specific source location. Lastly, we comment on the effects of historical records may not exist for all introduced species, and it is genetic bottlenecks on the establishment of invasive winter moth not uncommon for an introduced species to go unnoticed for long populations. periods of time before becoming an invasive pest. Genetic analyses have the ability to independently reconstruct regions of origins, and in some instances provide estimates for the times of introductions 2 | MATERIALS AND METHODS (Auger- Rozenberg et al., 2012; Barker et al., 2017; Javal et al., 2019; Lesieur et al., 2019; Lombaert et al., 2010; Oficialdegui et al., 2019; 2.1 | Sample collection Zardus & Hadfield, 2005). However, the power of these analyses is constrained by numerous factors including the underlying genetic Winter moth males were collected using pheromone- baited traps structure of the species, the number of generations since the intro- (Elkinton et al., 2010, 2011) from locations in Europe, North Africa, duction, the effective size of the founding population(s), the strength and western Asia, as well as from the four regions in North America, of the bottleneck the population(s) experienced, and/or the pres- where established winter moth populations have been recorded ence of differing selective pressures in the native and introduced (Nova Scotia, British Columbia, Oregon, and the northeastern United regions. As such, one common finding is for introduced populations States). In addition, larval individuals and adult females, which are to be reconstructed as genetically “distinct” from all sampled source wingless and do not fly, were opportunistically collected (see Table populations (e.g., Barker et al., 2017; Wu et al., 2015). This result S1 for complete collection information, including life stages, and could be due to the tendency for commonly implemented Bayesian Figure 1). genetic clustering algorithms to over- split populations (Frantz et al., After collection, adult moths were placed in glassine envelopes 2009) or an artefact generated during the interpretation of results (Uline Corporation) and stored at either – 20 or – 80°C, and larval (Lawson et al., 2018). caterpillars were placed in 95% ethanol and stored at – 20°C. For Here, we explore the invasion history of the economically many of the moths included in our analysis (1361 out of 1839), col- damaging defoliator the winter moth, Operophtera brumata L. lection and genotype information have been previously reported by (Lepidoptera: Geometridae). In its native distribution across Europe, us in studies of winter moth population structure in the native or in- North Africa, and western Asia, winter moth defoliates a wide troduced ranges (Andersen et al., 2017; Andersen, Havill, Broadley, range of tree and shrub species (Ferguson, 1978). Populations of et al., 2019; Andersen, Havill, Mannai, et al., 2019; Andersen et al., winter moth in Europe have been used as a model for the study of 2021; see Table S1). population ecology (Varley et al., 1973), and this species has been critically important for understanding the importance of spatial- synchrony (Jepsen et al., 2009) and synchrony of hatch with host 2.2 | Microsatellite genotyping tree bud- burst (Varley & Gradwell, 1960; Visser & Holleman, 2001) – a factor studied in other invasive defoliator populations as well Genomic DNA was extracted using the EZNA Tissue DNA extrac- (e.g., Hunter & Elkinton, 2000). The invasion history of winter moth tion kit (Omega Bio- tek), following the manufacturer's protocols. in North America has been well documented, with populations of For adult males, prior to extraction, the wings and genitalia were winter moth first reported in the 1930s in Nova Scotia (Embree, removed and stored as vouchers. For adults and larvae, the remain- 1967; MacPhee, 1967; MacPhee et al., 1988), the 1950s in Oregon ing body parts were then homogenized, using 3/16” stainless steel (Kimberling et al., 1986), the 1970s in British Columbia (Gillespie beads (GlenMills Inc.) with a FastPrep- 24 sample homogenizer (MP et al., 1978), and in the 1990s in coastal regions of northeastern Biomedicals). After extraction, 24 microsatellites including 15 dinu- United States (Elkinton et al., 2010, 2014). These populations are cleotide, 14 trinucletotide, two tetranucelotide, and one pentanu- thought to have been introduced by the movement of infected nurs- cleotide loci (see Havill et al., 2017 for sequence information and ery stocks (Ferguson, 1978). However, where in Eurasia these popu- amplification methods) were genotyped at the DNA Analysis Facility lations were introduced from, and whether these represent a single on Science Hill at Yale University, using a Thermo Fisher Scientific introduction that was then spread across North America, or multiple 3730xl DNA analyser. Fragment lengths were determined using introductions (or some combination of these) is unclear. A genetic the microsatellite plugin in the software program GENEIOUS v. R11 examination of the invasion history of winter moth in North America (https://www.genei ous.com) in comparison to the GeneScan 500 was previously conducted, but was
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