The spider mite Tetranychus urticae is a cosmopolitan agricultural pest with an extensive host plant range and an extreme record of pesticide resistance. Here we present the completely sequenced and annotated spider mite genome, representing the first complete chelicerate genome. At 90 megabases T. urticae has the smallest sequenced arthropod genome. Compared with other arthropods, the spider mite genome shows unique changes in the hormonal environment and organization of the Hox complex, and also reveals evolutionary innovation of silk production. We find strong signatures of polyphagy and detoxification in gene families associated with feeding on different hosts and in new gene families acquired by lateral gene transfer. Deep transcriptome analysis of mites feeding on different plants shows how this pest responds to a changing host environment. The T. urticae genome thus offers new insights into arthropod evolution and plant–herbivore interactions, and provides unique opportunities for developing novel plant protection strategies.

The availability of new genetic technologies has positioned the field of biological control as a test bed for theories in evolutionary biology and for understanding practical aspects of the release of genetically manipulated material. Purposeful introductions of pathogens, parasites, predators and herbivores, when considered as replicated semi-natural field experiments, show the unpredictable nature of biological colonization. The characteristics of organisms and their environments that determine this variation in the establishment and success of biological control can now be explored using genetic tools. Lessons from studies of classical biological control can help inform researchers and policy makers about the risks that are associated with the release of genetically modified organisms, particularly with respect to long-term evolutionary changes.

Background: The parasitic mite, Varroa destructor, is the most serious pest of the western honey bee, Apis mellifera, and has caused the death of millions of colonies worldwide. This mite reproduces in brood cells and parasitizes immature and adult bees. We investigated whether Varroa infestation induces changes in Apis mellifera gene expression, and whether there are genotypic differences that affect gene expression relevant to the bee's tolerance, as first steps toward unravelling mechanisms of host response and differences in susceptibility to Varroa parasitism.

We compared patterns of intraspecific polymorphism of two markers with contrasted modes of evolution, nuclear ribosomal DNA (rDNA) and mitochondrial DNA (mtDNA), in the phytophagous mite Tetranychus urticae Koch. The second internal transcribed spacer (ITS2) of rDNA and a fragment in the mtDNA gene coding for Cytochrome Oxidase I (COI), were PCR-amplified and sequenced in samples of various geographical origins distributed worldwide. The 15 COI haplotypes found fell into two major phylogenetic lineages differing by an average of 5% nucleotide divergence. Samples from the Mediterranean basin were represented in both lineages, and showed no phylogeographical structure. The other samples, from temperate regions of the northern hemisphere, were clustered in one of the lineages and displayed little variation, indicating a recent colonization of this region. In contrast, no variation at all was found at the ITS2 in this species. We sequenced both COI and ITS2 in four other species of the genus Tetranychus and found that, despite the absence of intraspecific polymorphism, ITS appears to evolve 2.5 times faster than COI. We argue that rDNA homogeneity over the species range of T. urticae results from the high colonization potential of this species, preventing long-term differentiation. Preliminary data on two other mite species (Amphitetranychus viennensis Zacher and Mononychellus progresivus Doreste) with stricter ecological requirements and more restricted colonization potential revealed substantial and concordant geographical differentiation for both ITS2 and COI.

Varroa destructor , now a major pest of the Western honeybee, Apis mellifera , switched from its original host, the Eastern honeybee, A. cerana , ca . 50 years ago. So far, only two out of several known mitochondrial haplotypes of V. destructor have been found to be capable of reproducing on A. mellifera (Korea and Japan). These haplotypes are associated in almost complete cytonuclear disequilibrium to diagnostic alleles at 11 microsatellite loci. By contrast, microsatellite polymorphism within each type is virtually absent, because of a severe bottleneck at the time of host change. Accordingly, 12 mitochondrial sequences of 5185 nucleotides displayed 0.40% of nucleotide divergence between haplotypes and no intra haplotype variation. Hence, each type has a quasi–clonal structure. The nascent intratype variability is subsequent to the clone formation 50 years ago: in both types the variant alleles differ from the most common by one (in 10 cases), two (five cases) or three (one case) repeated motifs. In addition to individuals of the two ‘pure’ types, five F 1 hybrids and 19 recombinant individuals (Japan alleles introgressed into the Korea genetic background) were detected. The existence of F 1 and recombinant individuals in admixed populations requires that double infestations of honeybee cells occur in a high proportion but the persistence of pure types suggests a post–zygotic isolation between the two clones.

The two-spotted spider mite Tetranychus urticae is one of the most significant mite pests in agriculture, feeding on more than 1,100 plant hosts, including model plants Arabidopsis thaliana and tomato, Solanum lycopersicum. Here, we describe timecourse tomato transcriptional responses to spider mite feeding and compare them with Arabidopsis in order to determine conserved and divergent defense responses to this pest. To refine the involvement of jasmonic acid (JA) in mite-induced responses and to improve tomato Gene Ontology annotations, we analyzed transcriptional changes in the tomato JA-signaling mutant defenseless1 (def-1) upon JA treatment and spider mite herbivory. Overlay of differentially expressed genes (DEG) identified in def-1 onto those from the timecourse experiment established that JA controls expression of the majority of genes differentially regulated by herbivory. Comparison of defense responses between tomato and Arabidopsis highlighted 96 orthologous genes (of 2,133 DEG) that were recruited for defense against spider mites in both species. These genes, involved in biosynthesis of JA, phenylpropanoids, flavonoids, and terpenoids, represent the conserved core of induced defenses. The remaining tomato DEG support the establishment of tomato-specific defenses, indicating profound divergence of spider mite-induced responses between tomato and Arabidopsis.

The invasion of the Western honey bee, Apis mellifera, by Varroa destructor is attributed to two mitochondrial haplotypes (K and J) that shifted last century from their primary host the Eastern honey bee, A. cerana, in north-east Asia. Here, mitochondrial DNA sequences (cox1, cox3, atp6 and cytb: 2700 base pairs) were obtained from mites infesting both Eastern and Western honeybees (respectively 21 and 11 colonies) from Asia including regions where the shifts first occurred. A total of eighteen haplotypes were uncovered in Asia (11 on A. cerana and 7 on A. mellifera). Two new variants of the K haplotype and two of the J haplotype were found on Western honeybees in what appeared to be well-established infestations. New haplotypes may represent a potential threat to A. mellifera worldwide. The extreme lack of polymorphism in the K and J haplotypes outside of Asia, can now be plausibly explained as being due to genetic 'bottlenecks' that occurred in Asia before and after mites shifted from their original Eastern honeybee host. Apis mellifera / Apis cerana / Varroa / mitochondrial DNA/diversity

Spider mites, Tetranychidae, represent one of the most cosmopolitan and economically important groups of terrestrial arthropods; however, many aspects of their evolutionary relationships remain uncertain. We sequenced part of the mitochondrial cytochrome oxidase subunit I (COI) gene in 20 species of phytophagous mites belonging to nine genera and two families (Tetranychidae and Tenuipalpidae), including several agricultural pests. As reported in insects, the sequences were extremely rich in A + T (75% on average), especially in the third codon position (95%). However, one of the genera we studied had a significantly lower A+T content (69% on average, 78% in the third codon position), showing that base composition can change substantially over short periods of time. Most interspecific differences were transversions and their number increased steadily with the number of non-synonymous differences, while the number of transitions remained constant. The phylogeny based on COI sequences was inferred using the maximum likelihood method. The results are compatible as a whole with the traditional classification based on morphological characters, but call for some minor taxonomic revisions. Some morphological characters and life history traits (mode of reproduction, adaptation to the host plant) were also analysed within this phylogenetic framework. At the family level, one can see a trend towards thelytoky becoming rarer compared to the general mode of reproduction of the group, arrhenotoky. There is also an evolutionary tendency towards a more complex mode of life, with the production of silk webs and correlated changes of the locomotion apparatus. However, in the Tetranychidae there seems to have been convergent evolution of these morphological characters together with independent development of a common adaptation to this mode of life in different genera.