Phylogenetic, Metabolic, and Taxonomic Diversities Shape Mediterranean Fruit Fly Microbiotas during Ontogeny

Aharon, Yael; Pasternak, Zohar; Yosef, Michael Ben; Behar, Adi; Lauzon, Carol R.; Yuval, Boaz; Jurkevitch, Édouard

doi:10.1128/aem.02761-12

Cited by 88 publications

(117 citation statements)

References 69 publications

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“…Similar findings of a predominantly vertical transmission with a low rate of horizontal transmission (that is, mixed transmission mode) in a range of other insects challenge the traditional view of a strict vertical transmission of most insect mutualists and instead highlight the importance of mixed transmission modes across a wide range of host taxa (Ebert, 2013). Examples for this mixed transmission mode include burying beetles (Kaltenpoth and Steiger 2014), fruit flies (Aharon et al, 2013), beewolves , termites (Schauer et al, 2012) and bumblebees (Koch and Schmid-Hempel, 2011).…”

Section: Mixed Transmission Mode and Partner Specificitymentioning

confidence: 61%

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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Section: Mixed Transmission Mode and Partner Specificitymentioning

confidence: 61%

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

et al. 2015

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“…In this study we found that B. dorsalis appears to have a relatively higher diversity of bacterial symbionts when compared to Ceratitis capitata and Drosophila melanogaster . High throughput analysis of bacteria population of the C. capitata revealed only 5–23 OTUs and 7–13 OTU of bacteria symbionts to be associated with the adult fly and larva respectively at 97% sequence identity21. Similarly 454 pyrosequencing of gut bacteria community associated with D. melanogaster yielded a total of 122 OTU at 97% sequencing identity22.…”

Section: Discussionmentioning

confidence: 99%

Pyrosequencing reveals a shift in symbiotic bacteria populations across life stages of Bactrocera dorsalis

Andongma

Wan

Dong

et al. 2015

Sci Rep

100

108

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Bactrocera dorsalis is one of the most economically important fruit flies around the world. In this study, 454 pyrosequencing was used to identify the bacteria associated with different developmental stages of B. dorsalis. At ≥ 97% nucleotide similarity, total reads could be assigned to 172 Operational Taxonomic Units belonging to six phyla. Proteobacteria dominated in immature stages while Firmicutes dominated in adult stages. The most abundant families were Enterococcaceae and Comamondaceae. The genus Comamonas was most abundant in pupae whereas completely absent in adults. Some identified species had low sequence similarity to reported species indicating the possibility of novel taxa. However, a majority sequence reads were similar to sequences previously identified to be associated with Bactrocera correcta, suggesting a characteristic microbial fauna for this insect genus. The type and abundance of different bacterial groups varied across the life stages of B. dorsalis. Selection pressure exerted by the host insect as a result of its habitat and diet choices could be the reason for the observed shift in the bacteria groups. These findings increase our understanding of the intricate symbiotic relationships between bacteria and B. dorsalis and provide clues to develop potential biocontrol techniques against this fruit fly.

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“…Aharon et al . () considered this finding in order to explain the increasing polyphyly of the Enterobacteriaceae during ontogeny in C. capitata . It could be hypothesized that the acquisition of endemic bacteria during the initial phases of invasion of a new region could lead to inflammatory disorders in the D. suzukii gut and generate transient enterobacterial blooms which, similarly, favor the reassortment of genetic material and confer habitat‐adapted fitness benefits to bacteria.…”

Section: Discussionmentioning

confidence: 99%

Metagenomic analysis reveals changes of the Drosophila suzukii microbiota in the newly colonized regions

Martinez‐Sañudo¹,

Simonato²,

Squartini³

et al. 2017

Insect Science

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The spotted wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) is a highly polyphagous pest of a wide variety of wild or cultivated berry and stone fruit. Originating from Southeast Asia, it has recently invaded a wide range of regions in Europe and North America. It is well known that insect microbiotas may significantly influence several aspects of the host biology and play an important role in invasive species introduction into new areas. However, in spite of the great economic importance of D. suzukii, a limited attention has been given so far to its microbiota. In this study, we present the first in-depth characterization of gut bacterial diversity from field (native and invasive range) and lab-reared populations of this insect. The gut bacterial communities of field insects were dominated, regardless of their origin, by 2 families of the phylum Proteobacteria: Acetobacteraceae and Enterobacteriaceae, while Firmicutes, mainly represented by the family Staphylococcaceae, prevailed in lab-reared population. Locality was the most significant factor in shaping the microbiota of wild flies. Moreover, a negative correlation between diversity and abundance of Enterobacteriaceae and the time elapsed since the establishment of D. suzukii in a new region was observed. Altogether our results indicate that habitat, food resources as well as the colonization phase of a new region contribute to shape the bacterial communities of the invasive species which, in turn, by evolving more quickly, could influence host adaptation in a new environment.

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Phylogenetic, Metabolic, and Taxonomic Diversities Shape Mediterranean Fruit Fly Microbiotas during Ontogeny

Cited by 88 publications

References 69 publications

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

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

Pyrosequencing reveals a shift in symbiotic bacteria populations across life stages of Bactrocera dorsalis

Metagenomic analysis reveals changes of the Drosophila suzukii microbiota in the newly colonized regions

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