Genetic analysis of the tomato russet mite provides evidence of oligophagy and a widespread pestiferous haplotype.

Worldwide, the tomato russet mite (TRM), Aculops lycopersici (Eriophyidae), is a key pest on cultivated tomato in addition to infesting other cultivated and wild Solanaceae; however, basic information on TRM supporting effective control strategies is still lacking, mainly regarding its taxonomic status and genetic diversity and structure. As A. lycopersici is reported on different species and genera of host plants, populations associated with different host plants may constitute specialized cryptic species, as shown for other eriophyids previously considered generalists. The main aims of this study were to (i) confirm the TRM taxonomic unity of populations from different host plants and localities as well as the species' oligophagy, and (ii) to advance the understanding of TRM host relationship and invasion history. For this purpose, we evaluated the genetic variability and structure of populations from different host plants along crucial areas of occurrence, including the area of potential origin, based on DNA sequences of mitochondrial (cytochrome c oxidase subunit I) and nuclear (internal transcribed spacer, D2 28S) genomic regions. Specimens from South America (Brazil) and Europe (France, Italy, Poland, The Netherlands) were collected from tomato and other solanaceous species from the genera Solanum and Physalis. Final TRM datasets were composed of 101, 82 and 50 sequences from the COI (672 bp), ITS (553 bp) and D2 (605 bp) regions, respectively. Distributions and frequencies of haplotypes (COI) and genotypes (D2 and ITS1) were inferred; pairwise genetic distance comparisons, and phylogenetic analysis were performed, including Bayesian Inference (BI) combined analysis. Our results showed that genetic divergences for mitochondrial and nuclear genomic regions from TRM associated with different host plants were lower than those observed in other eriophyid taxa, confirming conspecificity of TRM populations and oligophagy of this eriophyid mite. Four haplotypes (cH) were identified from the COI sequences with cH1 being the most frequent, representing 90% of all sequences occurring in all host plants studied (Brazil, France, The Netherlands); the other haplotypes were present exclusively in Brazilian populations. Six variants (I) were identified from the ITS sequences: I-1 was the most frequent (76.5% of all sequences), spread in all countries and associated with all host plants, except S. nigrum. Just one D2 sequence variant was found in all studied countries. The genetic homogeneity among populations highlights the occurrence of a highly invasive and oligophagous haplotype. These results failed to corroborate the hypothesis that differential symptomatology or damage intensity among tomato varieties and solanaceous host plants could be due to the genetic diversity of the associated mite populations. The genetic evidence, along with the history of spread of cultivated tomato, corroborates the hypothesis of a South American origin of TRM.