Revisiting the first case of insect-bacteria cospeciation: phylogenetic incongruence between aphids and their obligate endosymbiont at subfamily level

It has been widely accepted that aphids and their primary endosymbiotic bacteria Buchnera have strictly parallel diversification relationship. As the first reported case of insect-bacteria cospeciation, this parallel diversification hypothesis has been prevalent, in spite of its basis of limited taxonomic sampling and recent doubts. Here we revisit the evolutionary relationships between aphids and Buchnera by using much more taxa and genomic data (16S rDNA, ATP synthase β-subunit gene, and gluconate-6-phosphate dehydrogenase gene) to reconstruct the Buchnera phylogeny and test its congruence with the host phylogeny. Comparisons of the Buchnera phylogeny with morphology- and molecular-based aphid phylogenies indicate phylogenetic incongruence between aphids and Buchnera at subfamily level. Current empirical and theoretical evidence indicate two potential mechanisms underlying this incongruence: one is variation in evolutionary rates of Buchnera genomes among different aphid lineages; the other is horizontal transmission of Buchnera during the radiation of extant aphid subfamilies and tribes from their common ancestor.