Whole-genome single nucleotide polymorphism and mating compatibility studies reveal the presence of distinct species in sub-Saharan Africa Bemisia tabaci whiteflies

Abstract

In sub-Saharan Africa cassava growing areas, two members of the Bemisia tabaci species complex termed sub-Saharan Africa 1 (SSA1) and SSA2 have been reported as the prevalent whiteflies associated with the spread of viruses that cause cassava mosaic disease (CMD) and cassava brown streak disease (CBSD) pandemics. At the peak of CMD pandemic in the late 1990s, SSA2 was the prevalent whitefly, although its numbers have diminished over the last two decades with the resurgence of SSA1 whiteflies. Three SSA1 subgroups (SG1 to SG3) are the predominant whiteflies in East Africa and vary in distribution and biological properties. Mating compatibility between SSA1 subgroups and SSA2 whiteflies was reported as the possible driver for the resurgence of SSA1 whiteflies. In this study, a combination of both phylogenomic methods and reciprocal crossing experiments were applied to determine species status of SSA1 subgroups and SSA2 whitefly populations. Phylogenomic analyses conducted with 26 548 205 bp whole genome single nucleotide polymorphisms (SNPs) and the full mitogenomes clustered SSA1 subgroups together and separate from SSA2 species. Mating incompatibility between SSA1 subgroups and SSA2 further demonstrated their distinctiveness from each other. Phylogenomic analyses conducted with SNPs and mitogenomes also revealed different genetic relationships among SSA1 subgroups. The former clustered SSA1-SG1 and SSA1-SG2 together but separate from SSA1-SG3, while the latter clustered SSA1-SG2 and SSA1-SG3 together but separate from SSA1-SG1. Mating compatibility was observed between SSA1-SG1 and SSA1-SG2, while incompatibility occurred between SSA1-SG1 and SSA1-SG3, and SSA1-SG2 and SSA1-SG3. Mating results among SSA1 subgroups were coherent with phylogenomics results based on SNPs but not the full mitogenomes. Furthermore, this study revealed that the secondary endosymbiont-Wolbachia-did not mediate reproductive success in the crossing assays carried out. Overall, using genome wide SNPs together with reciprocal crossings assays, this study established accurate genetic relationships among cassava-colonizing populations, illustrating that SSA1 and SSA2 are distinct species while at least two species occur within SSA1 species.

Keywords: Bemisia tabaci; phylogenomics; reciprocal crossing; sub-Saharan Africa species.