Discussion
We found that the effects of intraspecific hybridization were neutral in
terms of fecundity and host acceptance. The reciprocal hybrids and the
parental populations laid eggs on all knotweeds showing little
preference towards any of the three species except for the Hokkaido
parent that preferred to lay a greater number of eggs on Bohemian
knotweed than Japanese knotweed. However, this host choice was
maladaptive because of low survival of eggs to adulthood. On the other
hand, the survival of the hybrid crosses was either intermediate between
the parental populations or higher than the survival of at least one of
the parents on given host plants. Thus, the sum effects of hybridization
appear to be either neutral or positive in this system.
We did not find evidence for hybrid vigor with regards to fecundity
since the reciprocal hybrid populations and the parental populations
laid similar number of eggs when summed up across knotweed species.
Heterosis is usually strongest in the first generation, and we used
second generation hybrids in our experiments where the effects may be
less pronounced. Yet, given that both parental populations have
undergone long-term laboratory rearing some increase in fitness was
expected upon hybridization, and second- and later-generation
intraspecific hybrids showed higher performance than their parents in
other insects as well (Hufbauer et al., 2013; Szűcs et al., 2012; Szűcs
et al., 2017). It is possible that because of the small body size, high
fecundity, and relative ease of rearing, A. itadori have been
kept at large enough population sizes that buffered them from genetic
problems, such as inbreeding or drift that hybridization could have
alleviated.
When presented with a choice between three knotweed species, both the
parental and hybrid A. itadori populations accepted all three
species for oviposition (Fig. 2). This indiscriminate egg laying
behavior was also observed in a recently collected distinct population
(Murakami) of A. itadori in paired-choice tests (Camargo et al.,
2022). Similarly, all three knotweed species were accepted for
oviposition in no-choice tests by both the Kyushu and Hokkaido
populations during host range testing (Grevstad et al., 2013). All the
above experiments were conducted in different geographical regions, the
one using the Murakami population in the Netherlands (Camargo et al.,
2022), the host range testing in Oregon and the United Kingdom (Grevstad
et al., 2013), and this study in Michigan, and they all used local
knotweed populations for the experiments. Thus, it appears that a
variety of genotypes of the three knotweed species are all recognized as
potential hosts by A. itadori . This can be beneficial for field
releases when mixed stands of different knotweed species co-occur,
however, some of these choices do not reflect survival probability of
psyllids.
The host choices of the Hokkaido population appear maladaptive since
females from this population lay most of their eggs on Bohemian knotweed
but can only develop on giant knotweed, which may be an artifact of over
a decade of laboratory rearing and lack of exposure to different
knotweed species. The developmental success of Hokkaido psyllids on
Bohemian and Japanese knotweeds were under 1% (Fig. 2). Such suboptimal
host choice behavior has been observed in many other herbivorous insects
(Alred, 2021; Badenes‐Perez et al., 2006; Berenbaum, 1981; Davis and
Cipollini, 2014; Faldyn et al., 2018; Ries and Fagan, 2003; Schlaepfer
et al., 2005). Notably, monarch butterflies (Danaus plexippus )
may lay up to a quarter of their eggs on invasive swallow-wort vines
(Vincetoxicum spp.) that are related to their milkweed hosts but
do not support larval development (Alred, 2021; Casagrande and Dacey,
2014). The Kyushu population does not discriminate among knotweed
species for oviposition, but it has relatively high development success
(40-62%) on all three species. Our results for survival of both the
Kyushu and Hokkaido populations on the different knotweed species are in
line with findings during host-specificity testing (Grevstad et al.,
2013).
Our development success results align with one other study by Fung et
al. (2020) that compared the survival of the F4 FemHOK cross and the
Kyushu parent on Japanese knotweed and found lower performance of the
hybrids. The conclusion made by Fung et al. was that hybridization would
not be beneficial for biological control in this system. However, we can
place the effects of hybridization of A. itadori in a better
context since we tested both reciprocal hybrids and compared their
performance to both parental populations on all three knotweed species.
We found that the survival of the reciprocal hybrids is somewhat
intermediate between those of the parental populations on all three
knotweed species (Fig. 2), which is a common outcome of intraspecific
hybridization (Dingle et al., 1982; He et al., 2021; Szűcs et al., 2012;
Tauber et al., 1986). This means that overall, hybridization improved
performance compared to one parent and decreased performance compared to
another parent. However, an intermediate developmental success is better
than no development at all (see Hokkaido psyllids on Japanese and
Bohemian knotweeds).
Considering developmental success
alone we concur with Grevstad et al. (2013) that the Kyushu population
is best suited for release on Bohemian and Japanese knotweeds and the
Hokkaido population should only be used for releases on giant knotweed.
However, the Kyushu population could also be used on giant knotweeds if
the Hokkaido population is not available since they have relatively high
developmental success on this species. In cases where cold adaptation
traits from the Hokkaido population may be desirable, such as in
Michigan, the release of hybrids might increase chances of overwintering
success and should be considered as a viable alternative to either
parental population.
An additional climate factor is photoperiod, which combined with
temperature is used by most insects, including A. itadori to
decide when to enter diapause (Danilevskii, 1965; Grevstad et al.,
2022). Native species are locally adapted to use the cues from
shortening daylength to prepare for winter and they will switch from a
reproductive phase to a non-reproductive phase at a critical photoperiod
(Danilevskii, 1965; Masaki, 1999). The Hokkaido population that was
derived from collections made at 42.6° latitude enters its
non-reproductive stage at a longer critical photoperiod than the Kyushu
psyllids originating from a latitude of 32.8° N. This means that
Hokkaido psyllids will diapause earlier than their Kyushu counterparts
in the field (Grevstad et al., 2022). This appears to be a desirable
trait in southern Michigan that is located at the same latitude as
Hokkaido. However, the Hokkaido population will have low survival on the
prevailing Japanese and Bohemian knotweeds in southern Michigan. On the
other hand, because of their shorter critical photoperiod, Kyushu
psyllids may start a new generation later in the season that they cannot
complete before cold temperatures set in.
In sum, based on mismatches in temperature, photoperiod, and host plant
availability neither the Kyushu nor the Hokkaido population may be ideal
for releases in southern Michigan. Given that the hybrids between these
two populations are able to develop and lay eggs on any of the three
knotweed species and that they will have a mix of genotypes from both
parental populations it is likely that there will be individuals with
traits that can confer better survival and performance than those of
either parent. Hybrids could also adapt faster to altered climates and
photoperiod regimes because of their likely higher genetic diversity. We
know from other weed biocontrol systems that critical daylength can
evolve rapidly and that hybridization can alter the timing of diapause
(Bean et al., 2012; Szűcs et al., 2012). For example, rapid evolution of
the critical photoperiod was found in Diorhabda carinulata that
allowed the southward expansion of this agent used to controlTamarix spp. In the USA (Bean et al., 2012). In ragwort flea
beetles (Longitarsus jacobaeae ) used against the invasiveJacobaea vulgaris intraspecific hybridization altered the summer
diapause response (Szűcs et al., 2012) and increased the biocontrol
potential of hybrids in the field (Szűcs et al., 2019).
Additionally, as a hybrid species, Bohemian knotweeds can possess a
greater degree of genetic diversity, which has been proposed as a main
characteristic in this species’ invasive potential (Clements et al.,
2016; Parepa et al., 2014). In such a case where genotypes of a target
species are diverse, hybrids may be well suited in that they maintain a
greater degree of diversity of their own compared to the parental
populations, potentially benefitting establishment probability through
the increased likelihood of adaptive evolution (Szűcs et al., 2017).
The release program of A. itadori in North America is still in
its early stages, so monitoring of initial Kyushu and Hokkaido field
populations will be essential to assess the establishment success and
control potential of these two parental populations. In addition, a new
population of A. itadori was collected in Niigata prefecture in
Japan on the island of Honshu in 2019, called the Murakami population
(Camargo et al., 2022). This population performs best on Bohemian
knotweed and based on collection location its climate adaptation may be
somewhat intermediate between the Kyushu and Hokkaido populations
(Camargo et al., 2022). The first releases of the Murakami population
were conducted in the Netherlands in 2020 (Camargo et al. 2022).
However, it may take years before this population is approved for field
release in the United States, therefore, releases for the foreseeable
future have to focus on the populations that are currently available.
Hybridization between the two populations already approved for
biocontrol release might prove to be a relatively simple and efficient
method of increasing rates of establishment.
Data Archiving Statement: Data for this study is available as
Supplementary Information.
Acknowledgements: We are grateful to F. Grevstad for providing
us with the Hokkaido and Kyushu psyllid populations. We thank B. Blossey
and Zs. Szendrei for comments on an earlier version of the manuscript.
This work was supported by the Michigan Department of Natural Resources
Michigan Invasive Species Grant Proposal (award # IS19-5003). M. S. was
supported by the United States Department of Agriculture National
Institute of Food and Agriculture (USDA NIFA) Hatch projects 1017601 and
1018568.