Coevolution and synchronized evolutionary rates in aphid dual endosymbiosis

Many insects rely on obligate bacterial endosymbionts for essential nutrients. However, long-term endosymbiosis drives genome erosion, frequently resulting in the acquisition of additional symbionts that complement or replace ancestral partners. In aphids, the primary nutritional symbiont Buchnera aphidicola can be supplemented by a co-obligate symbiont, most commonly Serratia symbiotica. The long-term evolutionary trajectory of this newly acquired symbiont and its impact on Buchnera remain unknown. Here, we assembled host mitochondrial and endosymbiont genomes from thirteen aphid species belonging to a clade in which Serratia has functioned as a co-obligate symbiont for approximately 25 million years. Phylogenomic analyses reveal that Serratia has undergone extensive genome reduction followed by strict codivergence with aphids and Buchnera. Bayesian molecular dating shows that substitution rates in Serratia and Buchnera are tightly correlated and fall within the range previously reported for Buchnera. Genome-wide analyses indicate pervasive purifying selection in both symbionts. Homologous host-provisioning genes retained in both symbionts did not exhibit elevated evolutionary rates. However, unlike other functional categories, their dN/dS values were not correlated between symbionts, suggesting that they no longer evolve under shared selective regimes, consistent with progressive metabolic specialization. Intraspecific patterns of polymorphism and phylogenies mirror macroevolutionary patterns across the clade. Fluorescence in situ hybridization shows that Serratia and Buchnera occupy distinct bacteriocytes, suggesting that similar demographic processes may contribute to their parallel evolution. Our findings demonstrate that, once integrated into an obligate partnership, newly acquired nutritional symbionts can converge on the long-term evolutionary dynamics of ancient obligate symbionts while undergoing functional specialization.