Portiera gives new clues on the evolutionary history of whiteflies

Abstract

Whiteflies (Hemiptera: Sternorrhyncha: Aleyrodidae) are a superfamily of small phloem-feeding insects. Their taxonomy is currently based on the morphology of nymphal stages that display phenotypic plasticity, which produces inconsistencies. To overcome this limitation, we developed a new phylogenetic framework that targets five genes of Candidatus Portiera aleyrodidarum, the primary endosymbiont of whiteflies. Portiera lineages have been co-diverging with whiteflies since their origin and therefore reflect their host evolutionary history. We also studied the origin of stability and instability in Portiera genomes by testing for the presence of two alternative gene rearrangements and the loss of a functional polymerase proofreading subunit (dnaQ), previously associated with genome instability. We present two phylogenetic reconstructions. One using the sequences of all five target genes from 22 whitefly species belonging to 17 genera. The second uses only two genes to include additional published Portiera sequences of 21 whitefly species, increasing our sampling size to 42 species from 25 genera. The developed framework showed low signal saturation, specificity to whitefly samples, and efficiency in solving inter-genera relationships and standing inconsistencies in the current taxonomy of the superfamily. Genome instability was found to be present only in the Aleurolobini tribe containing the Singhiella, Aleurolobus and Bemisia genera. This suggests that Portiera genome instability likely arose in the Aleurolobini tribes common ancestor, around 70 Mya. We propose a link between the switch from multi-bacteriocyte to a single-bacteriocyte mode of inheritance in the Aleurolobini tribe and the appearance of genome instability in Portiera.