Global patterns in genomic diversity underpinning the evolution of insecticide resistance in the aphid crop pest Myzus persicae

Abstract

The aphid Myzus persicae is a destructive agricultural pest that displays an exceptional ability to develop resistance to both natural and synthetic insecticides. To investigate the evolution of resistance in this species we generated a chromosome-scale genome assembly and living panel of >110 fully sequenced globally sampled clonal lines. Our analyses reveal a remarkable diversity of resistance mutations segregating in global populations of M. persicae. We show that the emergence and spread of these mechanisms is influenced by host-plant associations, uncovering the widespread co-option of a host-plant adaptation that also offers resistance against synthetic insecticides. We identify both the repeated evolution of independent resistance mutations at the same locus, and multiple instances of the evolution of novel resistance mechanisms against key insecticides. Our findings provide fundamental insights into the genomic responses of global insect populations to strong selective forces, and hold practical relevance for the control of pests and parasites.

Fig. 1. New biological and genomic resources for the aphid Myzus persicae reveal the genome-wide patterns of genetic variation in clones sampled from across the world.

a Chromosome-scale genome assembly of M. persicae clone G006. Heatmap shows frequency of HiC contacts along the genome assembly. Blue lines indicate super scaffolds and green lines show contigs, with the X axis showing cumulative length in millions of base pairs (Mb). b Geographic origin and sequence coverage of the 127 resequenced clones of M. persicae used in this study. c Circular plot of genome-wide genetic variation in a global sample of 127 M. persicae clones. The outermost circle represents the 6 chromosome-sized super-scaffolds of the genome assembly, with scaffold 1 the X chromosome. Moving inwards the circles represent: gene density, SNP density, GC and AT% over 100 kb non-overlapping windows.

Fig. 2. Phylogenetic relationship and population structure of 127 M. persicae clones.

a Maximum likelihood phylogeny based on >1 M biallelic SNPs. Data from two samples of Myzus cerasi were used as an outgroup. The geographic origin of clones and the host plant from which they were collected are indicated by coloured circles and squares respectively. Clone identification numbers (corresponding to Supplementary Data 1) are also included. For a representation of the tree as a phylogram see Fig. S1. b, c Principal component analysis of genetic diversity between clonal lines with samples coloured by host plant (b) or geographic origin (c). d Coancestry heatmap of the sampled clones derived from fineSTRUCTURE analysis. The scale shows the degree of shared genetic chunks between the lines (lower, yellow, to higher, blue). The maximum a posteriori (MAP) tree generated by fineSTRUCTURE showing the relationship between samples is shown above the heatmap. The geographic origin of clones and the host plant from which they were collected are indicated by the outer and inner coloured rectangles respectively (see PCA keys for interpretation of colours).

Fig. 3. Genetic structure in globally sampled M. persicae.

a Admixture analysis of genetic structure and individual ancestry. Colours in each column represent the inferred proportion of ancestry when K is varied from 2 to 12, the most likely number of predicted genetic clusters (K = 12) is indicated by a box. The geographic origin of clones and the host plant from which they were collected are indicated above and below the structure plot by coloured circles and squares respectively. b Geographic representation of genetic structure in the clones when grouped by country of origin (K = 12).

Fig. 4. Genomic divergence and signatures of selection associated with host plant use in M. persicae.

Panels from bottom to top display nucleotide diversity (π), Tajima’s D, F_ST, and H12 values across the 5 autosomal chromosomes of M. persicae for the main host plant groups (oilseed rape (OSR), peach, tobacco, pepper and potato), see Supplementary Data 1 for sample sizes. H12 scan: Each data point represents the H12 value calculated based on a 1000 SNP window. Red points highlight the top 15 peaks at each scaffold. Fixation index (F_ST), Tajima’s D, and nucleotide diversity (π): smoothed lines were estimated based on a 10 kb chromosomal window.

Fig. 5. Insecticide resistance mechanisms in global M. persicae.

a, b Frequency of eight resistance mutations in M. persicae collected from different countries (a) and host plants (b). Significant (p < 0.05) associations between specific resistance mutations and host-differentiated populations are denoted using a star (Fisher’s exact test). Significance applying to a specific codon is indicated in brackets. See Supplementary Data 1 for sample sizes. c Identification of novel resistance mutations in domain II of the voltage-gated sodium channel (VGSC) in M. persicae that confer resistance to pyrethroid insecticides. A schematic of the VGSC is shown above a nucleotide alignment illustrating the nature and position of two new mutations that both result in the same M918I substitution. For reference the wildtype sequence and the mutations leading to the amino acid substitutions reported previously at this position in resistant M. persicae are also displayed in the alignment.

Fig. 6. Population genomics of variation in sensitivity to a recently introduced insecticide.

a Sensitivity of 110 clones of M. persicae to two concentrations (0.25 ppm and 0.5 ppm) of the insecticide spirotetramat. Error bars display 95% confidence intervals (n = 4 biological replicates, each comprising 10 aphids). b, c Identification of a novel resistance mutation in a highly conserved region of the acetyl-CoA carboxylase (ACC) enzyme carboxyltransferase (CT) domain in M. persicae that confers resistance to spirotetratmat. A schematic of the ACC enzyme is shown above an amino acid alignment illustrating the position of an alanine to valine substitution in clone 20 (that exhibits marked resistance to spirotetramat) that was not observed in any of the other M. persicae clones. To illustrate the conserved nature of the alanine at this position across insects the sequences of several other insect species are included in the alignment.

Fig. 7. Average long-range linkage disequilibrium (LD) and LD decay over distance for all autosomes of M. persicae from peach and tobacco in Italy and Greece.

Distribution of r is plotted separately for all autosomes in clones from a peach-Greece, b peach-Italy, c tobacco-Greece and d tobacco-Italy. See Supplementary Data 1 for sample sizes. Individual points in the box plot represent mean r² values in 100 KB windows along the entire length of autosomes. r² values are plotted as a function of distance (LD decay) across all autosomes in e peach-Greece, f peach-Italy, g tobacco-Greece and h tobacco-Italy clones.