Abstract
Whiteflies (Hemiptera: Sternorrhyncha: Aleyrodidae) are a superfamily of small phloem-feeding insects. They rely on their primary endosymbionts "Candidatus Portiera aleyrodidarum" to produce essential amino acids not present in their diet. Portiera has been codiverging with whiteflies since their origin and therefore reflects its host’s evolutionary history. Like in most primary endosymbionts, the genome of Portiera stays stable across the Aleyrodidae superfamily after millions of years of codivergence. However, Portiera of the whitefly Bemisia tabaci has lost the ancestral genome order, reflecting a rare event in the endosymbiont evolution: the appearance of genome instability. To gain a better understanding of Portiera genome evolution, identify the time point in which genome instability appeared and contribute to the reconstruction of whitefly phylogeny, we developed a new phylogenetic framework. It targeted five Portiera genes and determined the presence of the DNA polymerase proofreading subunit (dnaQ) gene, previously associated with genome instability, and two alternative gene rearrangements. Our results indicated that Portiera gene sequences provide a robust tool for studying intergenera phylogenetic relationships in whiteflies. Using these new framework, we found that whitefly species from the Singhiella, Aleurolobus, and Bemisia genera form a monophyletic tribe, the Aleurolobini, and that their Portiera exhibit genome instability. This instability likely arose once in the common ancestor of the Aleurolobini tribe (at least 70 Ma), drawing a link between the appearance of genome instability in Portiera and the switch from multibacteriocyte to a single-bacteriocyte mode of inheritance in this tribe.
Highlights
Whiteflies are small phloem-feeding insects, which, together with aphids, scale insects, and psyllids, form the Sternorrhyncha suborder (Grimaldi and Engel 2005)
We found that Portiera of Aleurolobus and Singhiella whitefly species form a monophyletic clade together with Portiera of Bemisia, the Aleurolobini tribe
We discovered that whitefly species from the Singhiella, Aleurolobus, and Bemisia genera form a monophyletic tribe, the Aleurolobini
Summary
Whiteflies are small phloem-feeding insects, which, together with aphids, scale insects, and psyllids, form the Sternorrhyncha suborder (Grimaldi and Engel 2005). The Aleyrodidae consist of three extant subfamilies, the Udamoselinae, the Aleurodicinae, and the Aleyrodinae, and an extinct one, the Bernaeinae. The Aleurodicinae subfamily contains 21 extant genera, mainly distributed in Neotropical/Australasian regions (Charles 2010; Ouvrard and Martin 2020). The Aleyrodinae, with at least 142 described genera, is the most diverse and globally distributed subfamily and includes the major pest species Bemisia tabaci and Trialeurodes vaporariorum (Manzari and Quicke 2006; Ouvrard and Martin 2020). The extant whitefly subfamilies were reported to originate in the Middle Cretaceous (Campbell et al 1994), the first fossils of the Aleurodicinae and Aleyrodinae subfamilies were dated to the Lower Cretaceous (Drohojowska and Szwedo 2015). It is assumed that the emergence of angiosperms in the Lower Cretaceous opened new environmental niches and has promoted diversification and speciation of whiteflies along with their angiosperm hosts (Middle–Upper Cretaceous), leading to the emergence of the modern whitefly species (Drohojowska and Szwedo 2015)
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