Discussion:
Documenting the establishment and formation of new hybrid zones in real
time is critical for understanding the spatial and temporal nature of
these regions of genetic interchange (Abbott et al., 2013; Mallet,
2005). In addition, understanding the dynamics of hybridization between
native and non-native species may be particularly important for
understanding how invasive species become established and spread,
because reproducing with a native species could alleviate Allee effects
that limit the establishment of small populations due to stochastic
disturbances and mate-finding (Ellstrand & Schierenbeck, 2000;
Espeland, 2013; Mesgaran et al., 2016; Pfennig, Kelly, & Pierce, 2016;
Yamaguchi, Yamanaka, & Liebhold, 2019). Here, we document the real time
formation of a clinal (sensu Taylor et al., 2015) hybrid zone, following
the introduction of the invasive winter moth to the northeastern United
States. Our analyses suggest that the location of the center of this
hybrid zone might not be regulated primarily by environmental variables,
but appears to be behaving as a tension hybrid zone. Tension hybrid
zones are characterized by their independence from environmental
variables, narrow geographic width, low frequencies of hybridization,
and with the geographic location determined by a balance between
dispersal (dependent on population density) and selection against
hybrids (Barton & Hewitt, 1985; Key, 1968; Smith, Hale, Kearney,
Austin, & Melville, 2013). As shown by examining our two transects, the
hybrid zone is narrow, with a mean of ~ 40 km across all
years in both transects, and hybridization rate is low
(~ 6 % in both transects). The location of the hybrid
zone also appears to be dependent on population size, which would
influence dispersal rate because the center of the hybrid zone is near
the region where the population size of winter moth drops to where it is
similar to the endemic Bruce spanworm populations (Figures 7 and 8). The
final feature of a tension zone, low hybrid fitness, has also been
demonstrated in this system. Laboratory rearing of winter moth and Bruce
spanworm produced 93.5 and 94.1% viable eggs, respectively, while
crosses between winter moth females and Bruce spanworm males produced
60.8% viable eggs and crosses between Bruce spanworm females and winter
moth males produced just 22.1% viable eggs (Havill et al., 2017). The
near complete lack of Bruce spanworm backcrosses also indicates low
hybrid fitness in this system (Havill et al., 2017; Andersen et al.,
2019; this study). Interestingly, these two species appear to have few
pre-zygotic barriers to hybridization since they share the same sex
pheromone (Elkinton et al., 2011) and have overlapping mating flight
periods (Andersen, unpublished data). The barriers to hybridization in
this system, therefore, appear to be almost entirely made up of
post-zygotic incompatibilities resulting from > 500,000
years of allopatric divergence (based on an averaged observed
mitochondrial percent divergence between these two species of 7.5%
documented in Gwiazdowski, Elkinton, DeWaard, & Sremac, 2013; and the
newly calibrated mitochondrial mutation rate of approximately 14.5% per
million years for insects presented in Key, Frederick, & Schul, 2018).
Separating environmental factors (e.g., climate, land use, etc.) from
population factors (e.g., dispersal, abundance, hybrid fitness, etc.),
may not always be entirely feasible, and could, in part, explain why
there is a paucity of documented examples of this type of hybrid zone
between an introduced and a native species. However, by comparing our
two transects that differed in extreme minimum temperatures
(Massachusetts from -20°C to -24°C, and Connecticut ~
-17°C), our results indicate that extreme minimum winter temperatures
are not constraining the geographic location or width of the winter moth
x Bruce spanworm hybrid zone. That said, it should be noted that
researchers in Europe have observed that populations of winter moth can
rapidly adapt to changes in environmental conditions (van Asch, Salis,
Holleman, van Lith, & Visser, 2013), and as such the winter moth x
Bruce spanworm hybrid zone presents an exciting system to study the
combined roles of local adaptation and hybridization in the
establishment an invasive species under changing climate regimes.
In contrast to direct environmental constraints on the location of the
hybrid zone, we believe that population factors are more important for
explaining the differences in relative population densities of these two
species and therefore the stability and dynamics of the hybrid zone. One
such constraint might be top-down pressure by natural enemies of both
species. The biological control of winter moth in North America is one
of the best-known examples of the successful use of importation
biological control (Van Driesche et al., 2010) to reduce the ecological
and economic impacts of a non-native forest defoliator with a broad host
range (Elkinton et al., 2015; Embree, 1966; Kimberling et al., 1986;
Roland & Embree, 1995). Recently, Elkinton et al. (2021) showed
that the introduction of a single specialist natural enemy to the
Northeast was able to convert winter moth to non-pest status. These
introduced natural enemies have been incredibly effective at reducing
the abundance of winter moth in high density locations, but at low
densities, numerous authors have found that native pupal parasitoids
play an important role in regulating winter moth population sizes
(Frank, 1967a, 1967b; Horgan, 2005; Horgan & Myers, 2004; Latto &
Hassell, 1987; Raymond et al., 2002; Roland, 1994; Roland & Embree,
1995, Broadley 2018). For example, in the Northeast, Broadley (2018)
found that mortality caused by native generalist pupal parasitoids was
lowest in the eastern coastal regions and increased as she sampled
locations into the western interior portions of this region. Pupal
parasitism could therefore play an important role in limiting the
population sizes of both species, and as a result providing the
necessary balance for a tension hybrid zone to exist in this system (see
Taylor et al., 2015). It will be interesting to observe whether the
location of the hybrid zone shifts east as the population density of
winter moth continues to decrease due to the impacts of biological
control. Indeed, the eastward retreat of the hybrid zone in 2018, the
last year of our study (Figures 7 and 8), may indicate that this has
begun.
It is commonly acknowledged that during the invasion process, the
probability of establishment of non-native species can be influenced by
native predators, parasitoids, competitors, and/or microbial communities
through a process known as biotic resistance (Alpert, 2006; Dawkins &
Esiobu, 2016; Kimbro, Cheng, & Grosholz, 2013; Levine, Adler, &
Yelenik, 2004). For several decades there has been considerable concern
expressed in the literature about the risk of hybridization between
native and introduced species resulting in the “hybridization to
extinction” of the native species (Allendorf et al., 2001; Ayres,
Zaremba, & Strong, 2004; Hinton, 1975; Levin, 2002; Levin,
Francisco-Ortega, & Jansen, 1996; Prentis, White, Radford, Lowe, &
Clarke, 2007; Rhymer & Simberloff, 1996; Todesco et al., 2016; Wolf,
Takebayashi, & Rieseberg, 2001). Under a tension hybrid zone model,
however, the continued exchange of genetic material and the resulting
production of low-fitness hybrids, could result in a reduction in the
rate of spread of the introduced species by stabilizing the geographic
center of the hybrid zone, creating what we believe is an
underappreciated form of biotic resistance to invasion (sensuLevine et al., 2004). As such, we encourage additional research into the
possible role of hybridization for limiting the establishment and spread
of non-native species.