Data from: Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts

Symbiotic associations with bacteria have facilitated important evolutionary transitions in insects and resulted in long-term obligate interactions. Recent evidence suggests that these associations are not always evolutionarily stable and that symbiont replacement and/or supplementation of an obligate symbiosis by an additional bacterium has occurred during the history of many insect groups. Yet, the factors favoring one symbiont over another in this evolutionary dynamic are not well understood; progress has been hindered by our incomplete understanding of the distribution of symbionts across phylogenetic and ecological contexts. While many aphids are engaged into an obligate symbiosis with a single Gammaproteobacterium, Buchnera aphidicola, in species of the Lachninae subfamily, this relationship has evolved into a “ménage à trois”, in which Buchnera is complemented by a co-symbiont, usually Serratia symbiotica. Using deep sequencing of 16S rRNA bacterial genes from 128 species of Cinara (the most diverse Lachninae genus), we reveal a highly dynamic dual symbiotic system in this aphid lineage. Most species host both Serratia and Buchnera but, in several clades, endosymbionts related to Sodalis, Erwinia or an unnamed member of the Enterobacteriaceae have replaced Serratia. Endosymbiont genome sequences from four aphid species confirm that these co-resident symbionts fulfill essential metabolic functions not ensured by Buchnera. We further demonstrate through comparative phylogenetic analyses that co-symbiont replacement is not associated with the adaptation of aphids to new ecological conditions. We propose that symbiont succession was driven by factors intrinsic to the phenomenon of endosymbiosis, such as rapid genome deterioration or competitive interactions between bacteria with similar metabolic capabilities.

与细菌建立的共生关系，推动了昆虫演化历程中的关键过渡事件，并促成了长期的专性共生互作。新近研究证据表明，这类共生关系并非始终在演化上保持稳定；诸多昆虫类群的演化历史中，均发生过共生体替换事件，或是通过额外细菌对专性共生关系进行补充的情况。然而，在这一演化动态中，偏向某一类共生体而非其他的驱动因素仍未得到充分阐释；我们对共生体在系统发育与生态环境中的分布认知不足，这一短板阻碍了相关研究进展。尽管多数蚜虫与单一的γ-变形菌门（Gammaproteobacterium）细菌布氏蚜虫菌（Buchnera aphidicola）形成专性共生，但在长角蚜亚科（Lachninae）的物种中，这一关系已演变为“三方共生体系（ménage à trois）”，即布氏蚜虫菌会由一种共共生体（通常为共生沙雷氏菌（Serratia symbiotica））予以补充。本研究通过对128种大蚜属（Cinara，长角蚜亚科中物种多样性最高的类群）的细菌16S rRNA基因进行深度测序，揭示了该蚜虫支系中高度动态的双重共生体系。多数物种同时宿主共生沙雷氏菌与布氏蚜虫菌，但在多个演化支中，与索氏菌属（Sodalis）、欧文氏菌属（Erwinia）或肠杆菌科（Enterobacteriaceae）未命名类群相关的内共生体，已取代了共生沙雷氏菌的位置。对4种蚜虫的内共生体基因组进行测序的结果证实，这些共存的共生体能够完成布氏蚜虫菌无法承担的关键代谢功能。本研究进一步通过比较系统发育分析证实，共共生体的替换与蚜虫对新生态环境的适应并无关联。本研究提出，共生体的演替是由内共生现象本身的内在因素驱动的，例如基因组快速退化，或是代谢能力相近的细菌之间的竞争互作。