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The association between Bemisia tabaci mitotypes and cotton leaf curl outbreaks in Pakistan was investigated using the mitochondria cytochrome oxidase I gene (COI) as a molecular marker. The 3′-651 base fragment has been used to resolve B. tabaci phylogenies. However, the 5′-618 base fragment was nearly unexplored. Phylogenetic analysis for 829 whiteflies from 11 districts in two provinces of Pakistan, indicated all haplotypes grouped on the Asia II major clade, with Asia II-1 mitotype predominating, at 84%, compared to Asia II-5 and II-7, at ~16%, combined. The 3′- and 5′-fragment tree topologies were similar, while the concatenated topology was unique in some respects. Comparisons of segregating sites within the 3′- and 5′-loci, at third codon positions, 71 and 47, and of transitions to transversions (Ti/Tv) ratio of 2.93 and 5.9, respectively, showed the 3′-locus was most informative, while nucleotide diversity (π) was highest for the 5′-end, indicating both fragments contributed to concatenated tree structure. The extent of haplotype diversity, measured by Tajima's D, R 2, and Fu's F analyses, revealed significant demographic expansion for Asia II-1 and II-7 mitotypes. The bottleneck that preceded the expansions was evident in the temporal changes in mtCOI polymorphisms beginning in ~1990s, a timeframe known to have coincided with the adoption of a high-yield whitefly-susceptible cultivar in 1988, followed by pesticide overuse. These two cooperating phenomena appear to have exerted selection on the cotton leaf curl disease (CLCuD)-whitefly complex, resulting in the emergence of a resistance-breaking begomovirus as the polyphagous Asia II-1 mitotype underwent a genetic expansion that led to 'a perfect storm'. [ABSTRACT FROM AUTHOR]

Simple Summary: The whitefly Bemisia tabaci taxon consists of an undefined number of morphologically identical genetic variants of which only a few, including the B, harbor invasive haplotypes. These haplotypes have potential to upsurge and become important pests and plant virus vectors in irrigated agroecosystems worldwide. In the 1980s, unprecedented outbreaks associated with the B variant were reported worldwide, however, the precise origin(s) of the invasive haplotypes has not been determined. In this study, available B. tabaci mitochondrial gene sequences were examined for patterns of conserved single nucleotide changes (SNPs). The whitefly sequence records represented North Africa-Middle Eastern habitats, the proposed B variant center of origin, and distant locales recently invaded by haplotype(s) of the B variant. Unexpectedly, the analysis revealed eight SNPs groups (haplotypes) demonstrating that the genetic architecture of the B mitoype is more complex than previously recognized. Also, the distribution patterns of the eight B haplotypes were tightly linked to well-defined eco-geographic regions, suggesting the different groups have diversified by geographic isolation. Contrary to claims that collectively, the B variant is invasive, only two of the eight haplotypic groups have established in geographical locations outside of their zone of endemism. The Bemisia tabaci cryptic species contains 39 known mitotypes of which the B and Q are best recognized for having established outside their extant endemic range. In the 1980s, previously uncharacterized haplotype(s) of the B mitotype rapidly established in tropical and subtropical locales distant from their presumed center of origin, leading to displacement of several native mitotypes and extreme damage to crops and other vegetation particularly in irrigated agroecosystems. To trace the natural and evolutionary history of the invasive B haplotypes, a phylo-biogeographic study was undertaken. Patterns of single nucleotide polymorphisms (SNPs) and signatures potentially indicative of geographic isolation were investigated using a globally representative mitochondrial cytochrome oxidase I gene (mtCOI) sequence database. Eight haplotype groups within the North Africa-Middle East (NAFME) region were differentiated, NAFME 1–8. The NAFME 1–3 haplotypes were members of the same population that is associated with warm desert climate niches of the Arabian Peninsula and east coastal Africa-Ethiopia. The NAFME 4 and 5 haplotypes are endemic to warm and cold semi-arid niches delimited by the Irano-Turanian floristic region, itself harboring extensive biodiversity. Haplotypes 6 and 7 co-occurred in the Middle East along eastern Mediterranean Sea landmasses, while NAFME 8 was found to be endemic to Cyprus, Turkey, and desert micro-niches throughout Egypt and Israel. Contrary to claims that collectively, the B mitotype is invasive, NAFME 6 and 8 are the only haplotypes to have established in geographical locations outside of their zone of endemism. [ABSTRACT FROM AUTHOR]