Genetic diversity of the tomato russet mite supporting oligophagy and evidencing widespread of an invasive haplotype

Abstract

Worldwide, the tomato russet mite (TRM), Aculops lycopersici (Eriophyidae), is a key pest on grown tomatoes besides infesting other cultivated and wild Solanaceae; however, information on TRM basics aspects supporting effective control strategies still lacking, mainly regarding its taxonomic unit and genetic diversity and structure. As A. lycopersici is reported on different species and genera of host plants maybe, populations associated with different host plants constitute specialized cryptic species, such as showed 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; ii) to advance the understanding on TRM host relationship and invasion history. For this purpose it was evaluated the genetic variability and structure of populations from different host plants along crucial areas of occurrence, including that potentially of origin and the invaded ones, 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 Solanum and Physalis genera. Final TRM datasets were composed by 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 sequence variants (D2 and ITS1) were inferred; pairwise genetic distances, and phylogenetic analysis were performed, including Bayesian Inference (BI) combined analysis. Genetic divergences for mitochondrial and nuclear genomic regions from TRM associated with different host plants were even lower than those observed in other eriophyid taxa confirming co-specific of TRM populations and oligophagy of this eriophyid mite. Four haplotypes (cH) were identified from the COI sequences being cH1 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 for S. nigrum. Just one D2 sequence variant was found in all studied countries. The genetic homogeneity among populations highlights occurrence of a highly invasive and not host-specific haplotype. These results also do not corroborate the hypothesis that differential symptomatology/damage intensity by tomato varieties and solanaceous host plants could be due to the genetic diversity of the associated mite populations. Even this contribution was not primarily aimed to trace TRM invasion routes, genetic evidence, jointly with the main host plant history, corroborate the hypothesis of a TRM South American origin.