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
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DOI:
10.1038/ismej.2015.75
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发表时间:
2015-05
期刊:
The ISME Journal
影响因子:
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通讯作者:
S. Sudakaran;Franziska Retz;Y. Kikuchi;Christian Kost;Martin Kaltenpoth
S. Sudakaran;Franziska Retz;Y. Kikuchi;Christian Kost;Martin Kaltenpoth
中科院分区:
其他
文献类型:
--
作者:
S. Sudakaran;Franziska Retz;Y. Kikuchi;Christian Kost;Martin Kaltenpoth

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利用营养挑战或有毒寄主植物的进化适应是推动植食性昆虫多样化的主要力量。虽然共生细菌是已知的昆虫具有重要的营养作用,辐射到新的生态位后,收购特定的共生体的例子仍然很少。在这里,我们表征了Pyrrhocoridae家族昆虫的微生物群,并调查了补充维生素的共生体的获得是否使宿主能够多样化为营养不平衡和化学防御良好的锦葵属植物种子作为食物来源。我们的研究结果表明,维生素供应放线菌(CoriobacteriumandGordonibacter),以及厚壁菌门(梭菌属)和变形菌门(克雷伯氏菌属)是广泛的Pyrrhocoridae,但没有从姐妹家庭Largidae和其他外群类群。尽管与特定的微生物群的一致关联,Pyrrhocoridae的共生性既不与基于宿主微生物群落特征的树状图一致,也不与单个共生体菌株的共生性一致,表明共生伙伴的频繁水平交换。基于化石记录的系统发育年代分析揭示了Pyrrhocoridae核心微生物群在白垩纪晚期(8120 - 8650万年前)的起源,随后从与隐窝相关的β-变形菌共生体过渡到位于中肠M3区域的厌氧群落。在共生综合征(即共生体的身份和本地化)的变化和收购的pyrrhocorid核心微生物群遵循其首选的宿主植物(锦葵属)的进化,这表明共生体促进其主机的适应这种不平衡的营养资源,并使随后的多样化在竞争贫乏的生态位。
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 (CoriobacteriumandGordonibacter), 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.