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

ABSTRACT: 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.

SUBMITTER: Sudakaran S

PROVIDER: S-EPMC4817627 | biostudies-literature | 2015 Dec

REPOSITORIES: biostudies-literature

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

Sudakaran Sailendharan S Retz Franziska F Kikuchi Yoshitomo Y Kost Christian C Kaltenpoth Martin M

The ISME journal 20150529 12

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 vita ...[more]

PMID: 26023876

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Project description:Microbial consortia producing specific enzymatic cocktails are present in the gut of phytophagous and xylophagous insects; they are known to be the most efficient ecosystems to degrade lignocellulose. Here, the ability of these consortia to degrade ex vivo lignocellulosic biomass in anaerobic bioreactors was characterized in term of bioprocess performances, enzymatic activities and bacterial community structure. In a preliminary screening, guts of Ergates faber (beetle), Potosia cuprea (chafer), Gromphadorrhina portentosa (cockroach), Locusta migratoria (locust), and Gryllus bimaculatus (cricket) were inoculated in anaerobic batch reactors, in presence of grounded wheat straw at neutral pH. A short duration fermentation of less than 8 days was observed and was related to a drop of pH from 7 to below 4.5, leading to an interruption of gas and metabolites production. Consistently, a maximum of 180 mgeq.COD of metabolites accumulated in the medium, which was related to a low degradation of the lignocellulosic biomass, with a maximum of 5 and 2.2% observed for chafer and locust gut consortia. The initial cell-bound and extracellular enzyme activities, i.e., xylanase and β-endoglucanase, were similar to values observed in the literature. Wheat straw fermentation in bioreactors leads to an increase of cell-bounded enzyme activities, with an increase of 145% for cockroach xylanase activity. Bacterial community structures were insect dependent and mainly composed of Clostridia, Bacteroidia and Gammaproteobacteria. Improvement of lignocellulose biodegradation was operated in successive batch mode at pH 8 using the most interesting consortia, i.e., locust, cockroaches and chafer gut consortia. In these conditions, lignocellulose degradation increased significantly: 8.4, 10.5, and 21.0% of the initial COD were degraded for chafer, cockroaches and locusts, respectively in 15 days. Consistently, xylanase activity tripled for the three consortia, attesting the improvement of the process. Bacteroidia was the major bacterial class represented in the bacterial community for all consortia, followed by Clostridia and Gammaproteobacteria classes. This work demonstrates the possibility to maintain apart of insect gut biological activity ex vivo and shows that lignocellulose biodegradation can be improved by using a biomimetic approach. These results bring new insights for the optimization of lignocellulose degradation in bioreactors.

Project description:BackgroundDiet is a key component of a species ecological niche and plays critical roles in guiding the trajectories of evolutionary change. Previous studies suggest that dietary evolution can influence the rates and patterns of species diversification, with omnivorous (animal and plant, 'generalist') diets slowing down diversification compared to more restricted ('specialist') herbivorous and carnivorous diets. This hypothesis, here termed the "dietary macroevolutionary sink" hypothesis (DMS), predicts that transitions to omnivorous diets occur at higher rates than into any specialist diet, and omnivores are expected to have the lowest diversification rates, causing an evolutionary sink into a single type of diet. However, evidence for the DMS hypothesis remains conflicting. Here, we present the first test of the DMS hypothesis in a lineage of ectothermic tetrapods-the prolific Liolaemidae lizard radiation from South America.ResultsAncestral reconstructions suggest that the stem ancestor was probably insectivorous. The best supported trait model is a diet-dependent speciation rate, with independent extinction rates. Herbivory has the highest net diversification rate, omnivory ranks second, and insectivory has the lowest. The extinction rate is the same for all three diet types and is much lower than the speciation rates. The highest transition rate was from omnivory to insectivory, and the lowest transition rates were between insectivory and herbivory.ConclusionsOur findings challenge the core prediction of the DMS hypothesis that generalist diets represent an 'evolutionary sink'. Interestingly, liolaemid lizards have rapidly and successfully proliferated across some of the world's coldest climates (at high elevations and latitudes), where species have evolved mixed arthropod-plant (omnivore) or predominantly herbivore diets. This longstanding observation is consistent with the higher net diversification rates found in both herbivory and omnivory. Collectively, just like the evolution of viviparity has been regarded as a 'key adaptation' during the liolaemid radiation across cold climates, our findings suggest that transitions from insectivory to herbivory (bridged by omnivory) are likely to have played a role as an additional key adaptation underlying the exceptional diversification of these reptiles across extreme climates.

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

Publications

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

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