Introduction
Hymenoptera (bees, wasps, and ants) are arguably the most species-rich
group of animals on earth, in large part due to the sheer diversity of
parasitoid wasps within the order as driven by the close associations
these wasps have with their host arthropods (Forbes, Bagley, Beer,
Hippee, & Widmayer, 2018). Parasitoid wasps lay their eggs eitheron (ectoparasitoids) or in their hosts (endoparasitoids),
with some arresting the development of their hosts upon oviposition
(idiobionts), whereas others allow their host to continue development
during wasp larval growth (koinobionts) (Askew & Shaw, 1986). The level
of host specialization varies among parasitoid wasps. Some species are
monophagous, specializing on a single arthropod host species
(oligophagous), while others utilize a wider, albeit often closely
related, range of arthropod hosts, (host-flexible), Koinobiont
endoparasitoids are likely to be more specialized because developing
wasp larvae must survive through host development and must successfully
defend against the host’s immune response to parasitism(Beckage &
Gelman, 2004; Vinson & Iwantsch, 1980).
As a host is required for parasitoid survival and reproduction, there
are direct fitness consequences to selecting a host (Charnov & Skinner,
1984; Kouamé & Mackauer, 1991; Wang & Messing, 2004). Further, the
process of selecting and locating a host differs depending on the level
of host specialization of the parasitoid wasp (Bertoldi, Rondoni,
Brodeur, & Conti, 2019; Vet & Dicke, 1992; Vinson, 1976).
Although there are many factors
that may influence host selection in parasitoids (Price, 1971), for
host-flexible parasitoids some host species may provide a fitness
advantage relative to others. This begs the question: where a host
preference exists, how do host-flexible parasitoids locate and select
their preferred hosts?
Semiochemical cues (infochemicals) emitted from the host herbivore or
plants, also referred to as the plant host complex (PHC), are one way
parasitoid wasps may locate a viable host (Tumlinson, Lewis, & Vet,
1993; Vet & Dicke, 1992). Among infochemicals, there are three main
classifications: (1) Kairomones that benefit the receiver, (2) allomones
which benefit the sender, and (3) synomones that benefit both the sender
and receiver (Brown Jr, Eisner, & Whittaker, 1970). For parasitoids,
kairomones are often in the form of non-volatile oral secretions or
feces from the host (Rutledge, 1996), although volatile pheromones may
also be utilized. Synomones are typically plant-emitted volatiles and
may be either herbivore-induced or constitutively produced (Hilker &
McNeil, 2008; McCormick, Unsicker, & Gershenzon, 2012; Paré &
Tumlinson, 1999; Tumlinson, Lewis, et al., 1993). The detection of these
infochemicals by parasitoids can be innate or learned, although there
are still relatively few studies documenting how host-flexible
parasitoids use infochemicals for foraging and host acceptance (Steidle
& Van Loon, 2003).
Vet and Dicke (1992) hypothesized that not all infochemicals are equal,
and instead suffer from what they term the ‘reliability-detectability
problem’. Under this paradigm, host kairomones have high reliability
because they are excellent indicators of host presence. However, they
also have low detectability because they are typically localized and not
detectable at a distance (Vet & Dicke, 1992). Due to their reliability,
these infochemicals likely play an important role as a dependable
indicator of the presence a specific host for monophagous parasitoids
(Vet & Dicke, 1992). Vet and Dicke (1992) also contend that
plant-emitted synomones travel much farther than host compounds making
them more likely to be detected at a distance by foraging parasitoids,
but are likely poor indicators of host presence and therefore
unreliable. One hypothesized solution to the reliability-detectability
problem is herbivore-induced synomones, infochemicals released from the
plant in response to damage from herbivory termed the plant-host complex
(PHC). Vet and Dicke (1992) proposed that parasitoids would have strong
responses to these synomones if the parasitoid was a specialist on one
host species found on a single plant species, or parasitoids that can
utilize multiple hosts on a single plant species. In these cases,
herbivore-induced synomones of the PHC are not only detectable over a
long distance but also reliable indicators of host presence.
The ability for parasitoids wasps to utilize volatile compounds has been
well established, but most studies have either focused on specialists
(Colazza, McElfresh, & Millar, 2004; de Moraes, Lewis, Pare, Alborn, &
Tumlinson, 1998; Du, Poppy, Powell, & Wadhams, 1997; Gols, Bullock,
Dicke, Bukovinszky, & Harvey, 2011; McCall, Turlings, Lewis, &
Tumlinson, 1993; Röse, Lewis, & Tumlinson, 1998; Tumlinson, Turlings,
& Lewis, 1993; Xiu et al., 2019), or on a single host-flexible species
(D’Alessandro, Brunner, von Mérey, & Turlings, 2009; Ponzio et al.,
2016; Röse et al., 1998; Tumlinson, Lewis, et al., 1993; Turlings,
Tumlinson, & Lewis, 1990; Wei et al., 2007) and no other related
species. Although Vet and Dicke’s (1992) hypotheses may hold true for
parasitoids that specialize on a single host species, it is likely that
host-flexible parasitoids utilize these cues differently. An overarching
issue with each one of these hypotheses is that they approach the system
from a bottom-up perspective, describing infochemical use between the
third and second trophic level (parasitoid and host herbivore), and how
interactions between the second and first (host herbivore and plant)
could impact infochemical use by the third. In doing so, these
hypotheses downplay the potential for infochemical cues from the first
trophic level, outside of herbivore-induced infochemicals, to function
as reliable indicators for the location of a suitable host herbivore. In
this study we examine how infochemicals from the plant impact host
selection in parasitoids, and whether closely related host-flexible
parasitoids exhibit a differential preference for different plant
volatile profiles.
An excellent group for testing this question is Eadya Huddleston
& Short, 1978 (Hymenoptera: Braconidae: Euphorinae), a small genus of
parasitoid wasps endemic to Australia. These wasps attack paropsine
leaf-beetles (Coleoptera: Chyrsomelidae: Chrysomelinae) that feed onEucalyptus L’Héritier, 1789 (Myrtales: Myrtaceae). Eadyais currently comprised of 6 described species (Huddleston & Short,
1978; Ridenbaugh, Barbeau, & Sharanowski, 2018), all of which are host
flexible to varying degrees. Species such as Eadya daenerysRidenbaugh, 2018 and Eadya spitzer Ridenbaugh, 2018 were
documented from four different hosts, while E. paropsidisHuddleston & Short, 1978 has been documented on three hosts between
Tasmania and mainland Australia, but only reared from Paropsis
tasmanica Baly, 1866 in Tasmania (Peixoto et al., 2018).
Species of Eadya are also of interest as biological control
agents targeting invasive paropsine beetles infesting Eucalyptusplantations in New Zealand, with E. daenerys approved to controlP. charybdis Stål, 1860 (T. M. Withers, Allen, Todoroki, Pugh, &
Gresham, 2020) and E. annleckieae Ridenbaugh, 2018 as a potential
agent to control Paropsisterna (=Pst. variicollis(Chapuis) in Peixoto et al., 2018) (Nahrung et al., 2020). Leschen et
al. (2020) recently synonymized Pst. variicollis under Pst.
cloelia (Stål) but referenced no type material.
Given the host flexibility observed within Eadya , plant
infochemicals may play a more important role than host cues in host
selection. To assess this, we perform cophylogenetic analyses to test
for evidence of cospeciation between Eadya and their hosts. If
the parasitoids show strong evidence of cospeciation with their hosts,
we expect that host infochemicals would have a strong impact on host
location and selection. To examine how infochemicals from the plant
potentially impact host location and selection in closely related
host-flexible parasitoids, we test for distinct chemoprofiles inEucalyptus species and test whether these profiles are different
for damaged versus undamaged leaves, suggesting an herbivore-induced
response. Then we ask if these plant chemoprofiles are good predictors
of parasitoid and/or host species, which would indicate that plants have
a strong influence on host location and selection in the parasitoid.