Maria Navajas

The genome of Tetranychus urticae reveals herbivorous pest adaptations

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 90u2009megabases 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.

Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection

BackgroundThe 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 bees tolerance, as first steps toward unravelling mechanisms of host response and differences in susceptibility to Varroa parasitism.ResultsWe explored the transcriptional response to mite parasitism in two genetic stocks of A. mellifera which differ in susceptibility to Varroa, comparing parasitized and non-parasitized full-sister pupae from both stocks. Bee expression profiles were analyzed using microarrays derived from honey bee ESTs whose annotation has recently been enhanced by results from the honey bee genome sequence. We measured differences in gene expression in two colonies of Varroa-susceptible and two colonies of Varroa-tolerant bees. We identified a set of 148 genes with significantly different patterns of expression: 32 varied with the presence of Varroa, 116 varied with bee genotype, and 2 with both. Varroa parasitism caused changes in the expression of genes related to embryonic development, cell metabolism and immunity. Bees tolerant to Varroa were mainly characterized by differences in the expression of genes regulating neuronal development, neuronal sensitivity and olfaction. Differences in olfaction and sensitivity to stimuli are two parameters that could, at least in part, account for bee tolerance to Varroa; differences in olfaction may be related to increased grooming and hygienic behavior, important behaviors known to be involved in Varroa tolerance.ConclusionThese results suggest that differences in behavior, rather than in the immune system, underlie Varroa tolerance in honey bees, and give an indication of the specific physiological changes found in parasitized bees. They provide a first step toward better understanding molecular pathways involved in this important host-parasite relationship.

Social immunity in honeybees (Apis mellifera): transcriptome analysis of varroa‐hygienic behaviour

Honeybees have evolved a social immunity consisting of the cooperation of individuals to decrease disease in the hive. We identified a set of genes involved in this social immunity by analysing the brain transcriptome of highly varroa‐hygienic bees, who efficiently detect and remove brood infected with the Varroa destructor mite. The function of these candidate genes does not seem to support a higher olfactory sensitivity in hygienic bees, as previously hypothesized. However, comparing their genomic profile with those from other behaviours suggests a link with brood care and the highly varroa‐hygienic Africanized honeybees. These results represent a first step toward the identification of genes involved in social immunity and thus provide first insights into the evolution of social immunity.

A critical review on some closely related species of Tetranychus sensu stricto (Acari: Tetranychidae) in the public DNA sequences databases

Taxonomic misidentification of the specimens used to obtain DNA sequences is a growing problem reported for different groups of organisms, which threatens the utility of the deposited sequences in public DNA databases. This paper provides new evidence of misidentifications in molecular DNA public databases in phytophagous mites of the Tetranychidae family belonging to the group Tetranychus (Tetranychus). Several species in this group are of economic and quarantine importance in agriculture and among them Tetranychus urticae, a highly polyphagous mite causing outbreaks in many crops worldwide, is certainly the most studied. We analyzed and evaluated the identity of 105 GenBank accessions of ITS2 rDNA and 138 COI mtDNA sequences which were deposited as T. urticae and those of 14 other taxa morphologically closely related to Tetranychus sensu stricto. In addition, ITS2 and COI sequences of 18 T. urticae samples collected for this study and identified by morphological criteria, were generated and included in the analyzed dataset. Among the deposited sequences in the GenBank database, numerous cases of apparently mistaken identities were identified in the group Tetranychus s. str., especially between T. urticae, T. cinnabarinus, T. kanzawai and T. truncatus. Unreliable sequences (misidentified or dubious) were estimated at nearly 30%. In particular the analysis supports the invalidity of the controversial species status of T. cinnabarinus. More generally, it highlights the need of using combined morphological and molecular approaches to guarantee solid species diagnostics for reliable sequence accessions in public databases.

Modelling the potential distribution of the invasive tomato red spider mite, Tetranychus evansi (Acari: Tetranychidae)

Predicting the potential geographical distribution of a species is particularly important for pests with strong invasive abilities. Tetranychus evansi Baker & Pritchard, possibly native to South America, is a spider mite pest of solanaceous crops. This mite is considered an invasive species in Africa and Europe. A CLIMEX model was developed to predict its global distribution. The model results fitted the known records of T. evansi except for some records in dry locations. Dryness as well as excess moisture stresses play important roles in limiting the spread of the mite in the tropics. In North America and Eurasia its potential distribution appears to be essentially limited by cold stress. Detailed potential distribution maps are provided for T. evansi in the Mediterranean Basin and in Japan. These two regions correspond to climatic borders for the species. Mite establishment in these areas can be explained by their relatively mild winters. The Mediterranean region is also the main area where tomato is grown in open fields in Europe and where the pest represents a threat. According to the model, the whole Mediterranean region has the potential to be extensively colonized by the mite. Wide expansion of the mite to new areas in Africa is also predicted. Agricultural issues highlighted by the modelled distribution of the pest are discussed.

Review of the invasion of Tetranychus evansi : biology, colonization pathways, potential expansion and prospects for biological control

In the last two decades the subtropical red tomato spider mite, Tetranychus evansi, has expanded its geographical distribution and emerged as a major invasive agricultural pest. The mite is considered to be native to South America. Since its first report from north-eastern Brazil in 1952, it has been reported from different continents. This paper reviews literature on several aspects of the biology of T. evansi related to its status as an invasive species. It addresses taxonomical issues, occurrences, life history traits, host-plant interactions, genetic diversity of geographical isolates and worldwide colonisation pathways. It also presents updated data which allowed the assessment of the actual worldwide distribution of this species, from its discovery to the latest reports. As T. evansi is considered an emerging agricultural pest, we also present data based on modelling of the potential of T. evansi to colonize new geographical areas. In addition, this review presents past and current research on natural enemies of T. evansi potentially useful for its biological control. While summarizing the knowledge on T. evansi, the review emphasizes research possibilities that are worth pursuing, mainly concerning the ability of T. evansi to establish new populations and to detect new promising natural enemies.

Test of colonisation scenarios reveals complex invasion history of the red tomato spider mite Tetranychus evansi.

The spider mite Tetranychus evansi is an emerging pest of solanaceous crops worldwide. Like many other emerging pests, its small size, confusing taxonomy, complex history of associations with humans, and propensity to start new populations from small inocula, make the study of its invasion biology difficult. Here, we use recent developments in Approximate Bayesian Computation (ABC) and variation in multi-locus genetic markers to reconstruct the complex historical demography of this cryptic invasive pest. By distinguishing among multiple pathways and timing of introductions, we find evidence for the “bridgehead effect”, in which one invasion serves as source for subsequent invasions. Tetranychus evansi populations in Europe and Africa resulted from at least three independent introductions from South America and involved mites from two distinct sources in Brazil, corresponding to highly divergent mitochondrial DNA lineages. Mites from southwest Brazil (BR-SW) colonized the African continent, and from there Europe through two pathways in a “bridgehead” type pattern. One pathway resulted in a widespread invasion, not only to Europe, but also to other regions in Africa, southern Europe and eastern Asia. The second pathway involved the mixture with a second introduction from BR-SW leading to an admixed population in southern Spain. Admixture was also detected between invasive populations in Portugal. A third introduction from the Brazilian Atlantic region resulted in only a limited invasion in Europe. This study illustrates that ABC methods can provide insights into, and distinguish among, complex invasion scenarios. These processes are critical not only in understanding the biology of invasions, but also in refining management strategies for invasive species. For example, while reported observations of the mite and outbreaks in the invaded areas were largely consistent with estimates of geographical expansion from the ABC approach, historical observations failed to recognize the complex pathways involved and the corresponding effects on genetic diversity.

New Asian types of Varroa destructor: a potential new threat for world apiculture

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.ZusammenfassungDie Varroamilbe, Varroa destructor, ist ein gut adaptierter Parasit der Östlichen Honigbiene (Apis cerana), insbesondere in den nördlichen Regionen des asiatischen Festlands. Mit ihrem Wechsel auf die Westliche Honigbiene (A. mellifera) im letzen Jahrhundert kam es zu einer dramatischen Ausbreitung dieser Milbe. Als verantwortlich für den Parasitenübergang werden zwei mitochondriale (mt) Haplotypen (K1 und J1) von Varroa angesehen. Bereits erhobene molekulare Daten deuten darauf hin, dass es sich hierbei, aufgrund der zeitlichen Zusammenhänge dieser Wirtswechsel, um zwei partiell isolierte Klone handelt. Mittels Genotypisierung von V. destructor Isolaten aus Regionen, in denen die Wirtswechsel der J1 und K1 Milben zuerst stattgefunden hatten, sowie einer weiträumigeren Untersuchung des natürlichen Ausbreitungsgebiets von V. destructor in Asien, versuchten wir in der vorliegenden Studie ein genaueres Bild über den Befall von A. mellifera durch V. destructor zu erhalten. Jede Milbenprobe wurde zunächst anhand des publizierten 458 Basenpaarfragments des mitochondrialen Gens Cytochromoxidase 1 (cox1) genetisch charakterisiert, um neue Varianten bereits bekannten Haplotypen zuordnen zu können. Um die genetische Variabilität der Milben besser erfassen zu können, wurde im nächsten Schritt ein 2700 Nukleotide langes Fragment sequenziert, das vier mitochondriale Gene beinhaltet: cox1, Cytochromoxidase III (cox3), ATP Synthase 6 (atp6) und Cytochrom b (cytb). Wir untersuchten Varroamilben aus Asien, die sowohl die Östliche (21 Völker) als auch die Westliche Honigbiene (11 Völker) befallen hatten (Tab. I). Milben mit identischer Sequenz des 458 Basenpaare (bp) langen cox1 Fragments wurden als Mitglieder jeweils einer der sieben Haplogruppen (K1, J1, V1, C1, C2, C3, L1) betrachtet. Insgesamt fanden wir 18 mt Haplotypen (Varianten der zusammenhängenden Sequenzen innerhalb einer Haplogruppe (Tab. III). Von diesen fanden wir 12 auf A. cerana und 6 auf A. mellifera (Tab. I, Abb. 1). Obwohl wir nur eine neue Haplogruppe fanden (C3 in Tab. I und III), konnten wir 12 neue Haplotypen innerhalb der Haplogruppen erkennen, für die bisher keine genetische Variation bekannt war. Dies zeigt, dass Varroamilben in Asien genetisch wesentlich variabler sind, als bisher angenommen. Unsere Untersuchung zeigt des weiteren, dass die weltweit auf A. mellifera gefundenden ursprünglichen K1 und J1 Haplotypen von V. destructor aus zwei unterschiedlichen Milbenpopulationen stammen. Diese sind jeweils durch die K1 und die J1 Haplogruppenzuordnung definiert (Abb. 2), die im nordöstlichen Asien A. cerana befallen. Beide Populationen sind genetisch wesentlich variabler, als bisher angenommen, und die hier neubeschriebenen Haplotypen dieser Populationen haben A. mellifera in Asien zwar befallen, sich aber noch außerhalb dieser Region verbreitet. Diese neuen Haplotypen stellen nun neue potentielle Bedrohungen für A. mellifera außerhalb Asiens dar. Außerdem stellen diese Beobachtungen eine Warnung gegen die freie Verfrachtung von Honigbienen dar und zeigen die Notwendigkeit einer strengen und korrekten Quarantäne für den internationalen Handel mit lebenden Honigbienen.

DNA-based methods for eriophyoid mite studies: review, critical aspects, prospects and challenges.

Besides their potential for species identification, DNA-based methods are also routinely used for addressing ecological, evolutionary, phylogenetic and genetic questions to study several groups of Acari. However, in contrast to other plant-feeding mites and despite the economical relevance of many species of Eriophyoidea, very few scientists have dared so far to use DNA methods for the study of this group of mites; their very small size certainly has influenced this. In this review we examine the main techniques that have been used to study eriophyoid mites and discuss the results from the literature where DNA methods have provided significant advances to address several essential questions of the eriophyoid biology, e.g., to clarify suspect synonymies, to test hypothesis of cryptic species, to examine the occurrence of biotypes, especially in relation to virus ability or host-plant associations, to understand colonization patterns of invasive species, and for uses as biological control agents against invasive plants. We discuss these questions which might be related to agricultural issues, together with more fundamental aspects as the revision of the phylogeny of the Eriophyoidea. We discuss on the advantages as well as limitations of the most commonly used genetic markers and emphasize prospects and challenges of new molecular approaches. Much is now expected from molecular techniques in many fields of biology and for virtually all taxa. Eriophyoids should not be the exception.

Pyrethroid resistance in the tomato red spider mite, Tetranychus evansi, is associated with mutation of the para‐type sodium channel

BACKGROUNDnThe tomato red spider mite, Tetranychus evansi (Baker and Pritchard), is a serious pest of solanaceous crops in many African countries. In this study an investigation has been conducted to establish whether mutation of the para-type sodium channel underlies pyrethroid resistance in T. evansi strains collected in Southern Malawi.nnnRESULTSnTwo T. evansi strains from Malawi showed tolerance to the organophosphate chlorpyrifos and resistance (20-40-fold) to the pyrethroid bifenthrin, but were susceptible to two contemporary acaricides (abamectin and fenpyroximate) in insecticide bioassays. Cloning of a 3.1 kb fragment (domains IIS5 to IVS5) of the T. evansi para gene from pyrethroid-resistant and pyrethroid-susceptible strains revealed a single non-synonymous mutation in the resistant strains that results in an amino acid substitution (M918T) within the domain II region of the channel. Although novel to mites, this mutation confers high levels of resistance to pyrethroids in several insect species where it has always been associated with another mutation (L1014F). This is the first report of the M918T mutation in the absence of L1014F in any arthropod species. Diagnostic tools were developed that allow sensitive detection of this mutation in individual mites.nnnCONCLUSIONnThis is the first study of pyrethroid resistance in T. evansi and provides contemporary information for resistance management of this pest in Southern Malawi.