Seed preferences of Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae): Are there specialized trophic populations?

Kristenová, Marta; Exnerová, Alice; Štys, Pavel

doi:10.14411/eje.2011.075

Cited by 23 publications

(15 citation statements)

References 17 publications

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“…; Abou‐Donia ; Kristenová et al . ). Our comparative analysis of the different gut regions and the microbiota of the ingested food material suggest that specific symbiotic bacteria are restricted to the M3 region, where the food particles also remain for the longest period of time (Silva & Terra ; Kodrík et al .…”

Section: Discussionmentioning

confidence: 97%

“…Pyrrhocorid bugs preferentially feed on seeds of Malvales plants, which are generally avoided by other phytophagus insects due to the detrimental effects of their phytochemical defences such as gossypol and cyclopropenoic fatty acids, which can interfere with the digestion of food materials, cause retarded growth and lead to sterility (Allen et al 1967;Abou-Donia 1976;Kristenová et al 2011). Our comparative analysis of the different gut regions and the microbiota of the ingested food material suggest that specific symbiotic bacteria are restricted to the M3 region, where the food particles also remain for the longest period of time (Silva & Terra 1994;Kodrík et al 2012).…”

Section: Comparison Of Methods For the Characterization Of Microbial mentioning

confidence: 99%

“…Pyrrhocoris apterus predominantly utilizes dry ripe seeds of linden trees (Tilia cordata and T. platyphyllos) as a food source. However, during limited access to linden seeds, P. apterus has been shown to easily adapt to seeds of other Malvales (Kristenová et al 2011) as well as host plants from different families (Socha 1993;Tischler 1959). Additionally, firebugs are opportunistic scavengers feeding occasionally on dead insects, and they even attack and consume freshly moulted conspecifics (Henrici 1938;Southwood & Leston 1959).…”

Section: Introductionmentioning

confidence: 99%

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Geographical and ecological stability of the symbiotic mid‐gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae)

et al. 2012

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Symbiotic bacteria often play an essential nutritional role for insects, thereby allowing them to exploit novel food sources and expand into otherwise inaccessible ecological niches. Although many insects are inhabited by complex microbial communities, most studies on insect mutualists so far have focused on single endosymbionts and their interactions with the host. Here, we provide a comprehensive characterization of the gut microbiota of the red firebug (Pyrrhocoris apterus, Hemiptera, Pyrrhocoridae), a model organism for physiological and endocrinological research. A combination of several culture-independent techniques (454 pyrosequencing, quantitative PCR and cloning/sequencing) revealed a diverse community of likely transient bacterial taxa in the mid-gut regions M1, M2 and M4. However, the completely anoxic M3 region harboured a distinct microbiota consisting of facultative and obligate anaerobes including Actinobacteria (Coriobacterium glomerans and Gordonibacter sp.), Firmicutes (Clostri-dium sp. and Lactococcus lactis) and Proteobacteria (Klebsiella sp. and a previously undescribed Rickettsiales bacterium). Characterization of the M3 microbiota in different life stages of P. apterus indicated that the symbiotic bacterial community is vertically transmitted and becomes well defined between the second and third nymphal instar, which coincides with the initiation of feeding. Comparing the mid-gut M3 microbial communities of P. apterus individuals from five different populations and after feeding on three different diets revealed that the community composition is qualitatively and quantitatively very stable, with the six predominant taxa being consistently abundant. Our findings suggest that the firebug mid-gut microbiota constitutes a functionally important and possibly coevolved symbiotic community.

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Section: Discussionmentioning

confidence: 97%

Section: Comparison Of Methods For the Characterization Of Microbial mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Geographical and ecological stability of the symbiotic mid‐gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae)

et al. 2012

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“…(Salem et al, 2014). As the predominant food source of Pyrrhocoridae, that is, seeds of the plant order Malvales (Kristenová et al, 2011), is deficient in B vitamins, this symbiont-mediated nutritional upgrading plays an important role by allowing the hosts to exploit a nutritionally inadequate diet (Salem et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Evolutionary transition in symbiotic syndromes enabled diversification of phytophagous insects on an imbalanced diet

et al. 2015

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Evolutionary adaptations for the exploitation of nutritionally challenging or toxic host plants represent a major force driving the diversification of phytophagous insects. Although symbiotic bacteria are known to have essential nutritional roles for insects, examples of radiations into novel ecological niches following the acquisition of specific symbionts remain scarce. Here we characterized the microbiota across bugs of the family Pyrrhocoridae and investigated whether the acquisition of vitamin-supplementing symbionts enabled the hosts to diversify into the nutritionally imbalanced and chemically well-defended seeds of Malvales plants as a food source. Our results indicate that vitamin-provisioning Actinobacteria (Coriobacterium and Gordonibacter), as well as Firmicutes (Clostridium) and Proteobacteria (Klebsiella) are widespread across Pyrrhocoridae, but absent from the sister family Largidae and other outgroup taxa. Despite the consistent association with a specific microbiota, the Pyrrhocoridae phylogeny is neither congruent with a dendrogram based on the hosts' microbial community profiles nor phylogenies of individual symbiont strains, indicating frequent horizontal exchange of symbiotic partners. Phylogenetic dating analyses based on the fossil record reveal an origin of the Pyrrhocoridae core microbiota in the late Cretaceous (81.2-86.5 million years ago), following the transition from crypt-associated beta-proteobacterial symbionts to an anaerobic community localized in the M3 region of the midgut. The change in symbiotic syndromes (that is, symbiont identity and localization) and the acquisition of the pyrrhocorid core microbiota followed the evolution of their preferred host plants (Malvales), suggesting that the symbionts facilitated their hosts' adaptation to this imbalanced nutritional resource and enabled the subsequent diversification in a competition-poor ecological niche.

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“…Additionally, feeding by puncturing young cotton bolls usually results in the reduction of boll size (Pearson, 1958). Pyrrhocoris apterus also specializes on seeds of the plant order Malvales, particularly dry seeds of linden trees (Tilia cordata and T. platyphyllos) (Socha, 1993;Kristenova et al, 2011). However, some studies also reported on the exploitation of seeds of other plants groups within and -to a more limited extent -also beyond this plant order, as well as on the occasional feeding of firebugs on dead or weakened arthro-pods (Kershaw and Kirkaldy, 1908;Ahmad and Schaefer, 1987;Kristenova et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae)

Salem

Kreutzer

Sudakaran

et al. 2012

Environmental Microbiology

118

113

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Actinobacteria engage in defensive symbioses with several insect taxa, but reports of nutritional contributions to their hosts have been exceptionally rare. Cotton stainers (Dysdercus fasciatus) and red firebugs (Pyrrhocoris apterus) (both Hemiptera, Pyrrhocoridae) harbour the actinobacterial symbionts Coriobacterium glomerans and Gordonibacter sp. as well as Firmicutes (Clostridium sp. and Lactococcus sp.) and Proteobacteria (Klebsiella sp. and a Rickettsiales bacterium) in the M3 region of their mid-gut. We combined experimental manipulation with community-level analyses to elucidate the function of the gut symbionts in both pyrrhocorid species. Elimination of symbionts by egg-surface sterilization resulted in significantly higher mortality and reduced growth rates, indicating that the microbial community plays an important role for host nutrition. Fitness of symbiont-deprived bugs could be completely restored by re-infection with the original microbiota, while reciprocal cross-infections of microbial communities across both pyrrhocorid species only partially rescued fitness, demonstrating a high degree of host-symbiont specificity. Community-level analyses by quantitative PCRs targeting the dominant bacterial strains allowed us to link the observed fitness effects to the abundance of the two actinobacterial symbionts. The nutritional mutualism with Actinobacteria may have enabled pyrrhocorid bugs to exploit Malvales seeds as a food source and thereby possibly allowed them to occupy and diversify in this ecological niche.

show abstract

Seed preferences of Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae): Are there specialized trophic populations?

Cited by 23 publications

References 17 publications

Geographical and ecological stability of the symbiotic mid‐gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae)

Geographical and ecological stability of the symbiotic mid‐gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae)

Evolutionary transition in symbiotic syndromes enabled diversification of phytophagous insects on an imbalanced diet

Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae)

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