A study of the super-abundant Bemisia tabaci (Gennadius) species complex (Hemiptera: Aleyrodidae) in cassava mosaic disease pandemic areas in Tanzania

Abstract

Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is a cryptic species complex comprising morphologically indistinguishable but genetically variable populations. It is the vector of cassava mosaic geminiviruses (CMGs) causing cassava mosaic (CMD) disease to cassava (Manihot esculenta Crantz). After the outbreak and spread of a severe CMD from Uganda to several East and Central African countries, the production of cassava has been impaired. The severe CMD pandemic is mainly characterized by high disease severity and super-abundant populations of B. tabaci. This research sought to study the super-abundant populations in Tanzania. The main objectives were to assess the genetic diversity and distribution of cassava-associated B. tabaci, to assess the endosymbiont fauna, and to investigate the population structure of B. tabaci populations found in Tanzania. Hence, whiteflies collected through several field surveys were analysed using mitochondrial and nuclear markers. The four B. tabaci putative species found to be present in the study area based on mitochondrial data were sub-Saharan Africa 1 (SSA1), Mediterranean (MED), Indian Ocean (IO) and East Africa 1 (EA1). There were four sub-groups (SG) under SSA1 which included SSA1-SG1, SSA1-SG2, SSA1-SG1-2 and SSA1-SG3. SSA1-SG1 was found to be the pandemic-associated B. tabaci in Tanzania, being found predominantly in the pandemic affected north-western part of the country. The SSA1-SG2 was shown to be present in the pandemic-unaffected central part while SSA1-SG3 was exclusively found confined to the coastal parts. Microsatellite data also identified SSA1, MED and IO B. tabaci putative species as well as B. afer. It further revealed two sub-clusters within SSA1, which were each dominating different geographic areas across the sampling zones. One type predominated in the north-western pandemic affected part of Tanzania but diminishing in frequency towards the south-east, whilst the other became increasingly common until it becomes almost the only type present in the coastal area. The central part was a mix of the two sub-clusters. The CMD pandemic front was estimated to lie in Geita Region located in north-western Tanzania and to be spreading from the north-west to the south-east at ca 26 km per year. The different sub-groups and putative species in the study area exhibited contrasting endosymbionts profiles. Although no particular endosymbiont was found to be associated only with the pandemic-associated SSA1-SG1, the most remarkable feature was the absence of secondary symbiont infection for more than a third of the population. Multiple infection was very common in the remaining SSA1 sub-groups as well as in MED, IO and EA1 putative species. Finally, the extended presence of the pandemic-associated SSA1-SG1 in areas of up to 180 km to the south-east of the pandemic front is not entirely surprising, as changes in whitefly populations precede changes in disease status. However, the advancement of this pandemic-associated sub-group further into the non-pandemic central part coupled with the possibilities of gene flow and hybridization observed with other sub-groups poses an on-going threat to cassava production in the region. Therefore, future studies should focus towards understanding the exact nature of secondary symbionts on these insects in the wider region of East and Central Africa. This work was the first study that provided baseline information on the contrasting endosymbiont patterns and that confirmed the association of a distinct genetic sub group to the severe CMD pandemic in Tanzania more than a decade after similar associations were first made in Uganda.