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

Abstract

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.

Figure 1

Rooted posterior probability phylogenetic tree generated by MrBayes using the Markov chain Monte Carlo method for all the different mtDNA COI haplotype sequences (651 bp) of 1997 and 2017 samples together (n = 14) with reference sequences (n = 12, in bold) obtained from GenBank for comparison. Numbers associated with nodes indicate the posterior probability for those nodes. Horizontal bars represent genetic distances as indicated by the scale bar, vertical distances are arbitrary.

Figure 2

STRUCTURE bar plots for SSA1 and SSA2 populations collected from Uganda (a) for 33 populations of SSA1 arranged by subgroup, site and year at K = 2 and 3, e.g., K2(a) and K3(a) with recessive allele option turned on, and K2(b) and K3(b) without the option turned on. (b) For 102 randomly selected SSA1-SG1 and SSA1-SG2 together with 17 individuals of SSA2 at K = 3 and 4. The black line within SSA1 separates individuals of SSA1-SG1 and SSA1-SG2 for 2017 and SSA1-SG1 for 1997.

Figure 3

Principal component analysis of B. tabaci (SSA1-SG1 and SSA1-SG2) populations from Uganda. Colours show the genetic clusters found with the Bayesian analysis of structure at K = 3. Each dot represents one individual. The pink cluster is dominated by the 1997 population, whereas the blue and orange clusters are dominated by the 2017 population. In each cluster there are few individuals of different years represented by green, brown and black dots.

Figure 4

Geographical locations of sampling surveys conducted in (a) Uganda as a whole and (b) part of the central region in which sampling was conducted. Red and black circles are sample sites for whitefly collections made in February 1997 and February 2017.