Introduction:
In light of the unprecedented number of introductions of nonnative
species (Mack et al., 2000), one of the most pressing research needs for
evolutionary biologists and ecologists is to identify the factors that
influence the establishment of species that have negative ecological and
economic impacts (Suarez & Tsutsui, 2008). Multiple introductions
(Dlugosch & Parker, 2008), including cryptic ones (Roman, 2006), are
thought to play an important role in providing the diversity required to
overcome genetic bottlenecks associated with the establishment of
populations in novel ecosystems (Darling, Bagley, Roman, Tepolt, &
Geller, 2008; Facon, Pointier, Jarne, Sarda, & David, 2008). However,
when multiple geographically disjunct populations of an invasive species
become established, it is often unclear whether the species is a serial
invader (i.e., each population was introduced independently) or whether
the separate populations represent establishment from within the
invasive regions under a “stepping stone” model (see Cerwenka,
Alibert, Brandner, Geist, & Schliewen, 2014; Lombaert, Guillemaud,
Cornuet, Malausa, Facon, & Estoup, 2010; Oficialdegui et al., 2019;
Tonione, Reeder, & Moritz, 2011 for examples). Identifying which mode
of introduction occurred (serial invader or stepping stone) is necessary
for the study of genetic and ecological factors that drive invasion
success as independent populations are necessary for robust
hypothesis-based testing (Kang, Buckley, & Lowe, 2007), and this
information is also crucial for focusing management efforts (Floerl,
Inglis, Dey, & Smith, 2009).
When reconstructing regions of origins, and determining the numbers of
introductions of a focal organism, ideally historical records should be
observed and robust genetic analyses performed (e.g., Lynch &
Saltonstall, 2002; Schwenk, Brede, & Streit, 2008). Unfortunately,
historical records may not exist for all introduced species, and it is
not uncommon for an introduced species to go unnoticed for long 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
(Auger-Rozenberg et al., 2012; Barker, Andonian, Swope, Luster, &
Dlugosch, 2017; Javal et al., 2019; Lesieur et al., 2019; Lombaert et
al., 2010; Oficialdegui et al., 2019; Zardus & Hadfield, 2005).
However, the power of these analyses are constrained by numerous factors
including the underlying genetic structure of the species, the number of
generations since the introduction, the effective size of the founding
population(s), the strength of the bottleneck the population(s)
experienced, and/or the presence of differing selective pressures in the
native and introduced regions. As such, one common finding is for
introduced populations to be reconstructed as genetically “distinct”
from all sampled source populations (e.g., Barker et al., 2017; Wu et
al., 2015). This result could be due to the tendency for commonly
implemented Bayesian genetic clustering algorithms to over-split
populations (Frantz, Cellina, Krier, Schley, & Burke, 2009) or an
artifact generated during the interpretation of results (Lawson, Van
Dorp, & Falush, 2018).
Here we explore the invasion history of the economically damaging
defoliator the winter moth, Operophtera brumata L. (Lepidoptera:
Geometridae). In its native distribution across Europe, North Africa,
and western Asia, winter moth defoliates a wide range of tree and shrub
species (Ferguson, 1978). Populations of winter moth in Europe have been
used as a model for the study of population ecology (Varley, Gradwell,
& Hassell, 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 tree bud-burst (Embree, 1965 ,Varley &
Gradwell, 1960, Visser & Holleman, 2001) – a factor studied in other
invasive defoliator populations as well (e.g. Hunter & Elkinton, 2000).
The invasion history of winter moth in North America has been well
documented, with populations of winter moth first reported in the 1930’s
in Nova Scotia (Embree, 1967; MacPhee, 1967; MacPhee, Newton, & McRae,
1988), the 1950’s in Oregon (Kimberling, Miller, & Penrose, 1986), the
1970’s in British Columbia (Gillespie, Finlayson, Tonks, & Ross, 1978),
and in the 1990’s in coastal regions of northeastern United States
(Elkinton et al., 2010; Elkinton, Liebhold, Boettner, & Sremac, 2014).
These populations are thought to have been introduced by the movement of
infected nursery stocks (Ferguson, 1978). However, where in Eurasia
these populations were introduced from, and whether these represent a
single introduction that was then spread across North America, or
multiple introductions (or some combination of these) is unclear.
Previously, a genetic examination of the invasion history of winter moth
in North America was conducted, but was unable to discern these patterns
due to low levels of mitochondrial DNA diversity in both introduced and
native samples (Gwiazdowski, Elkinton, DeWaard, & Sremac, 2013).
To overcome this limitation, we examine the invasion history of winter
moth in North America using polymorphic microsatellite loci amplified
from individuals collected across its native and introduced regions. We
specifically examine how many times winter moth was introduced to North
America, and when possible, determine the specific source location.
Lastly, we comment on the role of hybridization between winter moth and
a North American congener the Bruce spanworm (O. bruceata Hulst),
and the effects of genetic bottlenecks on the establishment of invasive
winter moth populations.