What has changed in the outbreaking populations of the severe crop pest whitefly species in cassava in two decades?

High populations of African cassava whitefly (Bemisia tabaci) have been associated with epidemics of two viral diseases in Eastern Africa. We investigated population dynamics and genetic patterns by comparing whiteflies collected on cassava in 1997, during the first whitefly upsurges in Uganda, with collections made in 2017 from the same locations. Nuclear markers and mtCOI barcoding sequences were used on 662 samples. The composition of the SSA1 population changed significantly over the 20-year period with the SSA1-SG2 percentage increasing from 0.9 to 48.6%. SSA1-SG1 and SSA1-SG2 clearly interbreed, confirming that they are a single biological species called SSA1. The whitefly species composition changed: in 1997, SSA1, SSA2 and B. afer were present; in 2017, no SSA2 was found. These data and those of other publications do not support the ‘invader’ hypothesis. Our evidence shows that no new species or new population were found in 20 years, instead, the distribution of already present genetic clusters composing SSA1 species have changed over time and that this may be in response to several factors including the introduction of new cassava varieties or climate changes. The practical implications are that cassava genotypes possessing both whitefly and disease resistances are needed urgently

Genetic diversity of whitefly (Bemisia spp.) on crop and uncultivated plants in Uganda: implications for the control of this devastating pest species complex in Africa

Over the past three decades, highly increased whitefly (Bemisia tabaci) populations have been observed on the staple food crop cassava in eastern Africa and associated with ensuing viral disease pandemics and food insecurity. Increased whitefly numbers have also been observed in other key agricultural crops and weeds. Factors behind the population surges on different crops and their interrelationships are unclear, although in cassava they have been associated with specific populations within the Bemisia tabaci species complex known to infest cassava crops in Africa. This study carried out an in-depth survey to understand the distribution of B. tabaci populations infesting crops and uncultivated plant hosts in Uganda, a centre of origin for this pest complex. Whitefly samples were collected from 59 identified plant species and 25 unidentified weeds in a countrywide survey. Identities of 870 individual adult whiteflies were determined through mitochondrial cytochrome oxidase 1 sequences (651 bp) in the 3′ barcode region used for B. tabaci systematics. Sixteen B. tabaci and five related whitefly putative species were identified based on > 4.0% nucleotide divergence, of which three are proposed as novel B. tabaci putative species and four as novel closely related whitefly species. The most prevalent whiteflies were classified as B. tabaci MED-ASL (30.5% of samples), sub-Saharan Africa 1 (SSA1, 22.7%) and Bemisia Uganda1 (12.1%). These species were also indicated to be the most polyphagous occurring on 33, 40 and 25 identified plant species, respectively. Multiple (≥ 3) whitefly species occurred on specific crops (bean, eggplant, pumpkin and tomato) and weeds (Sida acuta and Ocimum gratissimum). These plants may have increased potential to act as reservoirs for mixed infections of whitefly-vectored viruses. Management of whitefly pest populations in eastern Africa will require an integration of approaches that consider their degree of polyphagy and a climate that enables the continuous presence of crop and uncultivated plant hosts

Review and guide to a future naming system of African Bemisia tabaci species

Once a pest has been correctly identified, its genus and species name can provide a link to valuable indications of its ecology, biology and life history that are critical for developing control strategies. Importantly, this link should exist even when the pest was known under other names (synonyms), or was not considered a pest at all (National Research Council, 1968). Many examples have shown that incorrect identification or classification of a pest has led to fruitless searches for biocontrol agents in the native range, incorrect assignments as disease vectors, and costly, yet misdirected, suppression measures. As new approaches for delimiting species based on molecular information become more widely used, the process of correctly identifying a species has become even more complex. Fortunately, we have good systematic frameworks and nomenclatural systems that are able to cope with these challenges. Here we review challenges associated with classification and identification within the Bemisia tabaci (Gennadius) species complex. These pests and the viruses they transmit have emerged in the past few decades as among the most damaging to food and fibre crops globally (Varma & Malathi, 2003; Pimental et al., 2005; Seal et al., 2006), especially in sub‐Saharan Africa (SSA). The systematics of the B. tabaci species group has been a highly debated topic for years (Boykin, 2014). Putative species are indistinguishable morphologically, so other biological data have been collected to investigate the species in the complex. Based on genetic differences (Colvin et al., 2004; Sseruwagi et al., 2005; Boykin et al., 2007; Boykin et al., 2013; Hsieh et al., 2014) and mating incompatibility (Colvin et al., 2004; Liu et al., 2007; Xu et al., 2010), B. tabaci is now recognized as a species complex that consists of at least 34 putative species (Boykin et al., 2012). The rapid discovery of significant species diversity has led to many changes in the informal names used over the last 10 years (Boykin, 2014), creating confusion in the literature

Expansion of the cassava brown streak pandemic in Uganda revealed by annual field survey data for 2004 to 2017

Funder: Uganda Government Association for Strengthening Agricultural Research in Eastern and Central AfricaFunder: Bill and Melinda Gates Foundation (Bill & Melinda Gates Foundation)Abstract: Cassava brown streak disease (CBSD) is currently the most devastating cassava disease in eastern, central and southern Africa affecting a staple crop for over 700 million people on the continent. A major outbreak of CBSD in 2004 near Kampala rapidly spread across Uganda. In the following years, similar CBSD outbreaks were noted in countries across eastern and central Africa, and now the disease poses a threat to West Africa including Nigeria - the biggest cassava producer in the world. A comprehensive dataset with 7,627 locations, annually and consistently sampled between 2004 and 2017 was collated from historic paper and electronic records stored in Uganda. The survey comprises multiple variables including data for incidence and symptom severity of CBSD and abundance of the whitefly vector (Bemisia tabaci). This dataset provides a unique basis to characterize the epidemiology and dynamics of CBSD spread in order to inform disease surveillance and management. We also describe methods used to integrate and verify extensive field records for surveys typical of emerging epidemics in subsistence crops

Endemism and Reemergence Potential of the Ipomovirus Sweet Potato Mild Mottle Virus (Family Potyviridae) in Eastern Africa: Half a Century of Mystery

Viruses have the ability to frequently colonize new hosts and ecological niches because of their inherently high genetic and evolutionary plasticity. However, a virus may emerge and remain of no or less economic importance until changes in viral or environmental factors dictate its epidemiological status. An example is sweet potato mild mottle virus (SPMMV), which was first reported in the 1970s on sweetpotato in eastern Africa. SPMMV has remained endemic in the region and poorly understood, yet accounting for 60 to 95% of losses, especially in mixed infections. Unlike other sweetpotato viruses which have global incidences, SPMMV has never been confirmed outside eastern Africa. This implicates the region as its center of origin but does not fully account for SPMMV's exclusive geographic delimitation to eastern Africa. Despite its importance, several mysteries and research gaps surround SPMMV, which decelerate efforts for effective virus disease management in sweetpotato. The aim of this review is to articulate research gaps, propose pivotal scientific directions, and stimulate knowledge generation for better management of virus diseases in sweetpotato. Vector-mediated transmission of SPMMV remains enigmatic. Here, we postulate testable hypotheses to explain SPMMV transmission. Comparisons between SPMMV and cassava brown streak ipomoviruses demonstrate epidemiological “hallmarks” for monitoring SPMMV. Evolutionary forces on SPMMV coupled with the virus' broad host range imply a “silent build up” of more fit variants in a changing climate, and this could explode into a worse disease conundrum. These information gaps need urgent filling to ease future management of virus disease emergences in sweetpotato. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license

African cassava whitefly, Bemisia tabaci, resistance in African and South American cassava genotypes

The whitefly, Bemisia tabaci, is a major pest of cassava, particularly in Africa where it is responsible both for the transmission of plant viruses and, increasingly, for direct damage due to feeding by high populations. To date, there have been no practical solutions to combat this emerging problem, due to the inability of the subsistence farmers that grow cassava to afford expensive inputs such as insecticides. A programme of research was carried out linking institutes in Africa, the UK and South America, to identify possible resistance sources in cassava to the whitefly, Bemisia tabaci. The South American genotype MEcu 72 and several Ugandan cassava landraces including Ofumba Chai, Nabwire 1 and Mercury showed good levels of resistance to B. tabaci. Field and screen-house experiments showed that all of the improved, high-yielding cassava mosaic disease (CMD) resistant cassava genotypes assessed were highly susceptible to B. tabaci and supported high populations of all life stages. These data support the hypothesis that the continuing high populations of cassava B. tabaci in Uganda are due, in part, to the widespread adoption of CMD-resistant cassava varieties during the CMD pandemic. They also show that the whitefly, Aleurotrachelus socialis, resistance present in the South American cassava genotypes could have broader applicability in the Old World

Expansion of the cassava brown streak pandemic in Uganda revealed by annual field survey data for 2004 to 2017.

Cassava brown streak disease (CBSD) is currently the most devastating cassava disease in eastern, central and southern Africa affecting a staple crop for over 700 million people on the continent. A major outbreak of CBSD in 2004 near Kampala rapidly spread across Uganda. In the following years, similar CBSD outbreaks were noted in countries across eastern and central Africa, and now the disease poses a threat to West Africa including Nigeria - the biggest cassava producer in the world. A comprehensive dataset with 7,627 locations, annually and consistently sampled between 2004 and 2017 was collated from historic paper and electronic records stored in Uganda. The survey comprises multiple variables including data for incidence and symptom severity of CBSD and abundance of the whitefly vector (Bemisia tabaci). This dataset provides a unique basis to characterize the epidemiology and dynamics of CBSD spread in order to inform disease surveillance and management. We also describe methods used to integrate and verify extensive field records for surveys typical of emerging epidemics in subsistence crops

Comparative evolutionary analyses of eight whitefly Bemisia tabaci sensu lato genomes: cryptic species, agricultural pests and plant-virus vectors

The genomes, transcriptomes, and predicted protein-coding sequences are available from Ensembl Metazoa (http://metazoa.ensembl.org) and are included within the references. Raw RNA-Seq datasets generated and/or analyzed during the current study are available from the European Nucleotide Archive database repository (https://www.ebi.ac.uk/ena) under the parent project accessions: PRJEB28507, PRJEB36965, PRJEB35304, PRJEB39408. All data generated during the analyses of these datasets are included in this published article, supplementary information files, and figshare repository (https://doi.org/10.6084/m9.figshare.23666799; https://doi.org/10.6084/m9.figshare.23666832.v4; https://doi.org/10.6084/m9.figshare.23666844).International audienceBackground: The group of > 40 cryptic whitefly species called Bemisia tabaci sensu lato are amongst the world's worst agricultural pests and plant-virus vectors. Outbreaks of B. tabaci s.l. and the associated plant-virus diseases continue to contribute to global food insecurity and social instability, particularly in sub-Saharan Africa and Asia. Published B. tabaci s.l. genomes have limited use for studying African cassava B. tabaci SSA1 species, due to the high genetic divergences between them. Genomic annotations presented here were performed using the 'Ensembl gene annotation system' , to ensure that comparative analyses and conclusions reflect biological differences, as opposed to arising from different methodologies underpinning transcript model identification. Results: We present here six new B. tabaci s.l. genomes from Africa and Asia, and two re-annotated previously published genomes, to provide evolutionary insights into these globally distributed pests. Genome sizes ranged between 616-658 Mb and exhibited some of the highest coverage of transposable elements reported within Arthropoda. Many fewer total protein coding genes (PCG) were recovered compared to the previously published B. tabaci s.l. genomes and structural annotations generated via the uniform methodology strongly supported a repertoire of between 12.8-13.2 × 10 3 PCG. An integrative systematics approach incorporating phylogenomic analysis of nuclear and mitochondrial markers supported a monophyletic Aleyrodidae and the basal positioning of B. tabaci Uganda-1 to the sub-Saharan group of species. Reciprocal cross-mating data and the co-cladogenesis pattern of the primary obligate endosymbiont 'Candidatus Portiera aleyrodidarum' from 11 Bemisia genomes further supported the phylogenetic reconstruction to show that African cassava B. tabaci populations consist of just three biological species. We include comparative analyses of gene families related to detoxification, sugar metabolism, vector competency and evaluate the presence and function of horizontally transferred genes, essential for understanding the evolution and unique biology of constituent B. tabaci. s.l species.Conclusions: These genomic resources have provided new and critical insights into the genetics underlying B. tabaci s.l. biology. They also provide a rich foundation for post-genomic research, including the selection of candidate gene-targets for innovative whitefly and virus-control strategies