Mothers never miss the moment: a fine-tuned mechanism for vertical symbiont transmission in a subsocial insect

Hosokawa, Takahiro; Hironaka, Mantaro; Mukai, Hiromi; Inadomi, Koichi; Suzuki, N.; Fukatsu, Takema

doi:10.1016/j.anbehav.2011.11.006

Cited by 58 publications

(64 citation statements)

References 34 publications

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“…(14,22,26,27). In this study, although less conspicuous, we found that several rows of crypts at the posterior end region of the symbiotic midgut are morphologically differentiated and conspicuously enlarged specifically in adult females of P. splendens (Fig.…”

Section: Discussionmentioning

confidence: 63%

“…4). Such obligate symbiotic bacteria associated with the midgut symbiotic organs have been described from a variety of stinkbugs of the families Pentatomidae (15,17,18,20,21,34,44), Scutelleridae (16,45,46), Cydnidae (19), Plataspidae (24,25,47,48), Acanthosomatidae (14), Parastrachiidae (22), Urostylididae (26), and others. As are the cases of the gut symbiotic bacteria associated with the stinkbugs representing the superfamily Pentatomoidea (21,49,50), the gut symbiont of P. splendens was placed within the Enterobacteriaceae of the Gammaproteobacteria, in contrast to the betaproteobacterial gut symbionts widely found across the superfamilies Lygaeoidea and Coreoidea (5).…”

Section: Discussionmentioning

confidence: 99%

“…In urostylidid stinkbugs, the basal region of the ovarioles is enlarged and distended for jelly production, and novel paired organs for symbiont transmission are formed in association with the female genital chamber (26). In a parastrachiid stinkbug, upon egg hatching, behaviors of adult females and their newborn nymphs are finely synchronized for vertical symbiont transmission, and a posterior region of the symbiotic midgut is hypertrophied in a female-specific manner for production of a copious amount of symbiont-containing materials (22). In acanthosomatid stinkbugs, novel paired organs for symbiont transmission, which are similar to but anatomically distinct from those of urostylidid stinkbugs, are present near the female genital chamber (14).…”

mentioning

confidence: 99%

“…Most commonly, as observed in the families Pentatomidae, Scutelleridae, Acanthosomatidae, and Cydnidae, vertical symbiont transmission is set up upon oviposition by egg surface contamination with symbiont-containing materials and establishes upon egg hatching by nymphal oral exploitation of the egg surface (1,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21). In several presocial stinkbugs of the families Parastrachiidae and Cydnidae, adult females continuously attend and take care of their eggs and excrete symbiont-containing materials just before or after egg hatching, which newborns consume and establish vertical symbiont transmission (22,23). In the family Plataspidae, uniquely, adult females produce brown-colored particles encasing symbiont-containing materials, so-called symbiont capsules, upon oviposition, and hatchlings suck the content of the capsules for establishing vertical transmission of the symbiont (24,25).…”

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confidence: 99%

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Female-Specific Specialization of a Posterior End Region of the Midgut Symbiotic Organ in Plautia splendens and Allied Stinkbugs

Hayashi

Hosokawa

Meng

et al. 2015

Appl Environ Microbiol

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dMany stinkbugs (Insecta: Hemiptera: Heteroptera) are associated with bacterial symbionts in a posterior region of the midgut. In these stinkbugs, adult females excrete symbiont-containing materials from the anus for transmission of the beneficial symbionts to their offspring. For ensuring the vertical symbiont transmission, a variety of female-specific elaborate traits at the cellular, morphological, developmental, and behavioral levels have been reported from diverse stinkbugs of the families Plataspidae, Urostylididae, Parastrachiidae, etc. Meanwhile, such elaborate female-specific traits for vertical symbiont transmission have been poorly characterized for the largest and economically important stinkbug family Pentatomidae. Here, we investigated the midgut symbiotic system of a pentatomid stinkbug, Plautia splendens. A specific gammaproteobacterial symbiont was consistently present extracellularly in the cavity of numerous crypts arranged in four rows on the midgut fourth section. The symbiont was smeared on the egg surface upon oviposition by adult females, orally acquired by newborn nymphs, and thereby transmitted vertically to the next generation and important for growth and survival of the host insects. We found that, specifically in adult females, several rows of crypts at the posterior end region of the symbiotic midgut were morphologically differentiated and conspicuously enlarged, often discharging the symbiotic bacteria from the crypt cavity to the main tract of the symbiotic midgut. The female-specific enlarged end crypts were also found in other pentatomid stinkbugs Plautia stali and Carbula crassiventris. These results suggest that the enlarged end crypts represent a female-specific specialized morphological trait for vertical symbiont transmission commonly found among stinkbugs of the family Pentatomidae. Many insects are associated with microbial mutualists in the gut lumen, inside the body cavity, or within the cells (1, 2). For ecological and evolutionary persistence of such mutualistic associations, vertical symbiont transmission through host generations is among the pivotal processes, although nonvertical (i.e., horizontal or environmental) symbiont transmission may also be prevalent in marine invertebrates, plants, and some insects (3-5).In intracellular associations such as Buchnera in aphids and Wigglesworthia in tsetse flies, vertical symbiont transmission usually occurs prenatally to developing eggs or embryos within maternal bodies (1,(6)(7)(8). In extracellular associations such as gut microbes in termites and stinkbugs, by contrast, vertical symbiont transmission tends to occur postnatally outside the maternal bodies via nymphal feeding of symbiont-containing excrements (1, 9, 10).The majority of plant-sucking stinkbugs (order Hemiptera: suborder Heteroptera: infraorder Pentatomomorpha: superfamily Pentatomoidea) are associated with bacterial symbionts of a beneficial nature in a posterior region of the midgut, where numerous crypts develop and harbor specific symbiotic bacteria the...

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Section: Discussionmentioning

confidence: 63%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Female-Specific Specialization of a Posterior End Region of the Midgut Symbiotic Organ in Plautia splendens and Allied Stinkbugs

Hayashi

Hosokawa

Meng

et al. 2015

Appl Environ Microbiol

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“…Many cydnid species of the subfamily Sehirinae are known as subsocial, in which adult females guard and take care of their eggs and nymphs in the nest (1, 3, 18). Hence, the gut symbiotic associations in the Cydnidae would provide intriguing opportunities to investigate the evolutionary connections between symbiosis and sociality (8,22).…”

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confidence: 99%

Polyphyly of Gut Symbionts in Stinkbugs of the Family Cydnidae

Hosokawa

Kikuchi

Nikoh

et al. 2012

Appl Environ Microbiol

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c Symbiotic bacteria associated with midgut crypts of stinkbugs of the family Cydnidae, representing seven species and 13 populations, were investigated. All of the symbionts were species specific, and constituted at least four distinct lineages in the Gammaproteobacteria, indicating multiple evolutionary origins of the gut symbionts among the burrower bugs.T he majority of plant-sucking stinkbugs are associated with symbiotic bacteria harbored in the lumen of a specialized region of the midgut (2,4,12). Previous studies have revealed remarkable diversity in the evolutionary host-symbiont relationships among major stinkbug groups. In the superfamily Pentatomoidea, the gut symbionts consist of a number of distinct lineages in the Gammaproteobacteria, and the host insects generally transmit their symbiont vertically by either of the posthatch transmission mechanisms, including egg surface contamination, coprophagy, symbiont capsule provisioning, etc. (12). Notably, different pentatomoid families may exhibit distinct patterns in their host-symbiont evolutionary intimacy. In the families Plataspidae and Acanthosomatidae, the symbiont phylogeny was highly congruent with the host phylogeny, and the symbiont genomes exhibit highly degenerative features such as AT-biased nucleotide compositions, accelerated molecular evolutionary rates,

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