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 has occurred during the history of many insect groups. This provides us with opportunities to investigate the factors favoring one symbiont over another, but progress has been hindered by our incomplete understanding of the distribution of symbionts across phylogenetic and ecological contexts. The association of aphids with Buchnera aphidicola, established 150 Mya, is one of the most persistent obligate symbioses known to date. However, in a few species of the genus Cinara, this relationship has evolved into a “ménage à trois”, in which a former facultative endosymbiont, Serratia symbiotica, performs some of the functions usually fulfilled by Buchnera. Using deep sequencing of 16S rRNA bacterial genes from 128 Cinara species and a robust phylogeny, we show that dual symbiosis has evolved repeatedly in Cinara. 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. These findings confirm that the species of this genus require a co-resident symbiont to complement Buchnera in its nutritional role. We further demonstrate that cosymbiont 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
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