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.