Introduction
Classical biological control aims to introduce and establish exotic
natural enemies to reduce populations of invasive species. It can
provide long-term and sustainable control of invasive species; however,
low establishment success and variable or low impact of the introduced
agents are ongoing problems during the implementation of biocontrol
programs (Cock et al., 2016; Schwarzländer et al., 2018; Van Driesche et
al., 2020). This could be due to a variety of factors, including reduced
genetic diversity because of long-term laboratory rearing that can limit
the ability of the biocontrol agents to adapt to their new environment
(Szűcs et al., 2019). The use of intentional intraspecific hybridization
as a tool, and in general, a better integration of evolutionary
principles into the practice of biological control are emerging new
directions to enhance the fitness and adaptive ability of biocontrol
agents (Leung et al., 2020; Moffat et al.; Sentis et al., 2022; Szűcs et
al., 2019).
Hybridization can promote rapid evolutionary change and facilitate
adaptations, since it can increase genetic variation, which serves as
the raw material for evolution (Dlugosch et al., 2016; Schierenbeck and
Ellstrand, 2009; Stebbins, 1959). Inter- and intraspecific hybridization
can also create novel genotypes that may exhibit unique traits and
adaptations that are not found in the parental populations (Arnold,
1997; Rieseberg and Willis, 2007; Stebbins, 1959). Early-generation
hybrids can exhibit hybrid vigor, or heterosis, whereby the fitness of
hybrids is higher than that of the parents (Edmands, 2007; Lynch, 1991).
However, recombination in later-generation hybrids can erase heterosis,
disrupt co-adapted gene complexes (hybrid breakdown), and outbreeding
depression may ensue that can result in lower fitness of hybrids than
their parents (Edmands, 2007; Lynch, 1991).
In the context of biological control,
promoting rapid adaptation to
novel and changing climates is desirable, but there are concerns that
hybridization may lead to rapid evolutionary changes in the host range
of agents. Upon hybridization many traits may show intermediate values
compared to the parents, which may be due to the high additive genetic
variance that governs many life history traits (Danilevskii, 1965;
Dingle et al., 1982; Hoy, 1975; Tauber et al., 1986). However, there can
also be sex-linkage and maternal effects in the expression of traits in
hybrids, which can result in resemblance towards either parent, but more
often the maternal parent (Hard et al., 1993; Mousseau and Dingle, 1991;
Tauber et al., 1986). From the few studies that investigated the effects
of hybridization on host use it appears that hybridization can have
immediate effects on host-specificity of herbivorous insects. When the
strains or species that are crossed have different host preferences the
hybrids may exhibit specificity towards either of the parental host
species and preference can change as hybridization progresses in later
generations (Bitume et al., 2017; Hoffmann et al., 2002; Mathenge et
al., 2010). However, when the parental strains that are crossed have
similar host ranges hybridization do not necessarily alter the
preference or performance of hybrids on suboptimal non-target species
(Szűcs et al., 2021). Little is known of how intraspecific hybridization
may influence host and climate adaptations in herbivorous insects used
as biocontrol agents and without a better understanding of these basic
processes, we cannot integrate evolutionary principles into biocontrol
to improve the outcomes of programs.
The current study explores whether intraspecific hybridization could be
used as a tool to improve the establishment and the impact of biological
control agents against invasive knotweeds. Three species of invasive
knotweeds, Japanese knotweed (Fallopia japonica ), giant knotweed
(F. sachalinensis ) and their hybrid Bohemian knotweeds (F.
x bohemica ) have been targeted for biological control by the psyllidAphalara itadori (Hemiptera: Aphalaridae) for over a decade in
the United Kingdom, since 2014 in Canada and since 2020 in the USA and
the Netherlands (Camargo et al., 2022; Grevstad et al., 2022). Despite
large scale, repeated introductions of A. itadori using thousands
of individuals locally, long-term establishment, population growth and
control of knotweeds have not been successful at any locations to date
(Fung et al., 2020; Grevstad et al., 2018; Grevstad et al., 2022; Jones
et al., 2021). The lack of establishment can be due to multiple factors,
including climate mismatch, predation, or low fitness of the agents
because of long term laboratory rearing (Andersen and Elkinton, 2022;
Grevstad et al., 2022; Jones et al., 2021; Jones et al., 2020). Given
that currently two populations of A. itadori are available for
introduction in Michigan which are specific to different knotweed
species and that the populations have distinct climate adaptations,
intraspecific hybridization between them could increase genetic
diversity, improve fitness, adaptive potential to different climates,
and alter host preference. These outcomes would be desirable in Michigan
where only the long-term laboratory-reared populations are available for
introduction, and where releases face the problem of matching either the
best fitting host-race on existing knotweed infestations or the best
climate match of A. itadori .
In southern Michigan, where a humid continental climate prevails, large
populations of Japanese and Bohemian knotweeds are present
(misin.msu.edu). The southern population of A. itadori which was
collected on the island of Kyushu in Japan has the best performance on
these two knotweed species (Grevstad et al., 2013). However, Kyushu has
a subtropical climate. The northern population of A. itadori was
collected from a similar climate as southern Michigan, on the island of
Hokkaido in Japan, but they have the best performance on giant knotweeds
and low fitness on Japanese and Bohemian knotweeds (Grevstad et al.,
2013). Thus, there appears to be no optimal release approach in southern
Michigan using either population of A. itadori .
Hence, we explored the effects of hybridization on fitness, host choice
and developmental success of A. itadori on different knotweed
species to evaluate the biocontrol potential of hybrids. We created
reciprocal hybrids between the southern and northern populations and
compared their fecundity and their host choices between the three
knotweed species with those of the parental populations in multiple
choice tests. We also assessed developmental success of the hybrid and
parental populations on the three knotweed species. We hypothesized that
hybrids would show intermediate traits between the parental populations
regarding host choice and developmental success on the different
knotweed species. In addition, we predicted that hybridization would
lead to heterosis, possibly increasing fecundity of either or both
reciprocal hybrid crosses.