656 Invasive Stink Bugs and Related Species (Pentatomoidea)
2011; Hosokawa et al. 2012b, 2016; Bistolas et al. 2014), which indicates frequent horizontal transmission
of the symbiotic bacteria and/or multiple evolutionary origins of the symbiotic associations.
Symbiotic bacteria of the superfamilies Coreoidea and Lygaeoidea belong to the genus Burkholderia
of the class Betaproteobacteria (Kikuchi et al. 2005, 2011; Olivier-Espejel et al. 2011; Boucias et al. 2012;
Itoh et al. 2014). Most of the Burkholderia species isolated from the coreoid and lygaeoid insects form a
monophyletic group in the genus Burkholderia, which is called the stink bug-associated beneficial and
environmental (SBE) group (Kikuchi et al. 2011, Itoh et al. 2014). In addition to the insect-associated
Burkholderia, this bacterial clade includes several strains from plant galls and environmental soils,
among which the insect-associated, plant-gall-associated, and environmentally isolated strains do not
form coherent groups (Kikuchi et al. 2011); this indicates frequent horizontal transmission between
them. In fact, as discussed in Section 14.1. 3.4, it has been reported that the coreoid and lygaeoid spe-
cies do not vertically transmit the Burkholderia symbionts but, rather, acquire the symbionts from the
environment in every generation (Kikuchi et al. 2007). Such a transmission mechanism may lead to the
development of the tangled phylogeny of the Burkholderia symbionts.
Bacteriocyte-associated symbionts of the families Lygaeidae and Blissidae belong to the
Enterobacteriaceae of the Gammaproteobacteria. These intracellular symbionts do not form a mono-
phyletic group within the bacterial group (Küechler et al. 2012), which strongly suggests their multiple
evolutionary origins.
In contrast to the simple, mono-associated gut microbiota in the superfamilies Pentatomoidea,
Coreoidea, and Lygaeoidea, the gut bacterial community in the family Pyrrhocoridae is relatively com-
plex, wherein Actinomyces, Firmicutes, and Proteobacteria are housed in the M3 section of the midgut,
which is swollen (Table 14.1) (Sudakaran et al. 2012). A broad survey of the gut community in diverse
pyrrhocorid species suggests that the Actinomyces-dominated, complex microbiota has evolved as the
common ancestor of this family (Sudakaran et al. 2015).
14.1.3.4 Transmission Mechanism of Symbiotic Bacteria
Diverse modes of mechanisms for symbiont transmission have been identified in several insect groups
(Buchner 1965, Kikuchi 2009, Salem et al. 2015). Endocellular symbionts such as Buchnera typically
are passed to the next generation via transovarial transmission, wherein the symbiont directly infects the
embryos in the maternal body (Mira and Moran 2002, Braendle et al. 2003, Miura et al. 2003, Frydman
et al. 2006, Koga et al. 2012). A similar mechanism has been reported in the intracellular symbioses
of the families Lygaeidae and Blissidae (Buchner 1965, Küechler et al. 2012, Matsuura et al. 2012).
On the other hand, insects harboring extracellular symbionts have evolved elaborate post-ovipositional
mechanisms for symbiont transmission such as superficial bacterial contamination of eggs (egg smear-
ing with excrement) and probing of parental bacteria-containing excrement (coprophagy). In the
Pentatomomorpha, the egg-smearing manner is possibly the most common and reported mechanism in
several species of the superfamilies Pentatomoidea and Pyrrhocoroidea (Abe et al. 1995, Prado et al. 2006,
Kaltenpoth et al. 2009, Kaiwa et al. 2010, Tada et al. 2011, Kikuchi et al. 2012, Hosokawa et al. 2013). In the
family Pentatomidae, female adults have enlarged crypts in the posterior end of M4, which are believed to
be symbiotic organs involved in the egg-smearing manner of symbiont transmission (Hayashi et al. 2015).
Acanthosomatid bugs bear closed crypts resulting in symbionts that never are excreted directly from the
crypts; these bugs develop a female-specific symbiotic organ called a “lubricating organ” along the repro-
ductive canal, which smears the symbiotic bacteria on the egg surfaces during oviposition (Rosenkranz
1939, Kikuchi et al. 2009). Mother stink bugs usually contaminate eggs during oviposition, except for
an exceptional case reported in a subsocial species, Parastrachia japonensis Scott (Parastrachiidae). In
P. japonensis, which is well known for maternal care of eggs and hatchlings, females smear their egg
clusters with symbiont-containing excrement immediately before egg hatching (Hosokawa et al. 2012a),
indicating they can determine when their eggs will hatch by an unrevealed sensing-mechanism.
In addition, a unique and elaborate transmission mechanism, called “capsule transmission,” has been
reported for the family Plataspidae, in which symbiont-filled particles, referred to as the “symbiont
capsules,” are deposited in association with eggs, and hatchlings probe the content of the capsules to acquire
the symbiont (Schneider 1940; Müller 1956, Fukatsu and Hosokawa 2002; Hosokawa et al. 2005, 2006)