title: Adaptation of a polyphagous herbivore to a novel host plant extensively shapes the transcriptome of herbivore and host.
abstract: Generalist arthropod herbivores rapidly adapt to a broad range of host plants. However, the extent of transcriptional reprogramming in the herbivore and its hosts associated with adaptation remains poorly understood. Using the spider mite Tetranychus urticae and tomato as models with available genomic resources, we investigated the reciprocal genomewide transcriptional changes in both spider mite and tomato as a consequence of mite's adaptation to tomato. We transferred a genetically diverse mite population from bean to tomato where triplicated populations were allowed to propagate for 30 generations. Evolving populations greatly increased their reproductive performance on tomato relative to their progenitors when reared under identical conditions, indicative of genetic adaptation. Analysis of transcriptional changes associated with mite adaptation to tomato revealed two main components. First, adaptation resulted in a set of mite genes that were constitutively downregulated, independently of the host. These genes were mostly of an unknown function. Second, adapted mites mounted an altered transcriptional response that had greater amplitude of changes when re-exposed to tomato, relative to nonadapted mites. This gene set was enriched in genes encoding detoxifying enzymes and xenobiotic transporters. Besides the direct effects on mite gene expression, adaptation also indirectly affected the tomato transcriptional responses, which were attenuated upon feeding of adapted mites, relative to the induced responses by nonadapted mite feeding. Thus, constitutive downregulation and increased transcriptional plasticity of genes in a herbivore may play a central role in adaptation to host plants, leading to both a higher detoxification potential and reduced production of plant defence compounds.
authors.affiliation: Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 9424, 1090 GE, Amsterdam, The Netherlands.
authors.forename: Nicky
authors.initials: N
authors.lastname: Wybouw
authors.affiliation: Department of Biology, University of Western Ontario, London, N6A 5B7, ON, Canada.
authors.forename: Vladimir
authors.initials: V
authors.lastname: Zhurov
authors.affiliation: Department of Biology, University of Western Ontario, London, N6A 5B7, ON, Canada.
authors.forename: Catherine
authors.initials: C
authors.lastname: Martel
authors.affiliation: Department of Biology, University of Western Ontario, London, N6A 5B7, ON, Canada.
authors.forename: Kristie A
authors.initials: KA
authors.lastname: Bruinsma
authors.affiliation: Royal Belgian Institute of Natural Sciences, Vautierstraat 29, B-1000, Brussel, Belgium.|Terrestrial Ecology Unit, Biology Department, Ghent University, K. L. Ledeganckstraat 35, B-9000, Gent, Belgium.
authors.forename: Frederik
authors.initials: F
authors.lastname: Hendrickx
authors.affiliation: Department of Biology, University of Western Ontario, London, N6A 5B7, ON, Canada.|Instituto de Ciencias de la Vid y el Vino, 26006, Logroño, Spain.
authors.forename: Vojislava
authors.initials: V
authors.lastname: Grbić
authors.affiliation: Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 9424, 1090 GE, Amsterdam, The Netherlands.|Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, B-9000, Ghent, Belgium.
authors.forename: Thomas
authors.initials: T
authors.lastname: Van Leeuwen
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D005075:Biological Evolution; D005828:Genetics, Population; D060434:Herbivory / Q000235:genetics*; D018551:Solanum lycopersicum / Q000235:genetics* / Q000502:physiology; D040102:Tetranychidae / Q000201:enzymology / Q000235:genetics*; D059467:Transcriptome
keywords: adaptation; genetic accommodation; herbivory; plant defence; transcriptomics; xenobiotic metabolism