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Uva-DARE (Digital Academic Repository) UvA-DARE (Digital Academic Repository) The role of horizontally transferred genes in the xenobiotic adaptations of the spider mite Tetranychus urticae Wybouw, N.R. Publication date 2015 Document Version Final published version Link to publication Citation for published version (APA): Wybouw, N. R. (2015). The role of horizontally transferred genes in the xenobiotic adaptations of the spider mite Tetranychus urticae. General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:29 Sep 2021 Nicky-ch1_Vera-ch1.qxd 18/08/2015 14:32 Page 11 1 General Introduction Nicky-ch1_Vera-ch1.qxd 18/08/2015 14:32 Page 12 General Introduction 1.1. ARTHROPOD HERBIVORY ased on fossil records dating back to the Late Silurian era (420 million years Bago), arthropods were the first terrestrial animals that showed signs of her- bivory (or feeding exclusively on plant material) (Labandeira, 2002, 2006). Arthropods are characterized by the presence of articulated appendages (arthropod means ‘jointed foot’) and a chitinous exoskeleton, which necessi- tates ecdysis for growth. This phylum contains four living subphyla: Myriapoda, Crustacea, Hexapoda and Chelicerata (FIGURE 1.1) and represents a great majority of all currently living plant-feeding animal species (Schoonhoven et al., 2006; Strong et al., 1984). Although every subphylum harbors phytophagous species, only the Hexapoda and Chelicerata lineages will be discussed. Arthropod herbivory within these subphyla can be divided into four differ- ent feeding guilds: (1) external feeding (chewing, snipping or tearing), (2) pierc- ing-sucking (cell-content, xylem or phloem), (3) internal feeding by creating tunnels between upper and lower plant surfaces in a process called mining, and (4) feeding through gall formation or other plant distortions. Typically, a phy- tophagous arthropod lineage is characterized by one particular mode of feed- ing. For instance, within insects, beetles and caterpillars are chewing herbivores, while some true bugs (or Hemiptera) pierce and suck plant tissue. Within Chelicerata, plant-feeding mites typically pierce and suck cell content (Labandeira, 2005; Lindquist, 1998; Schoonhoven et al., 2006). 1.1.1. THE CHALLENGES OF ARTHROPOD HERBIVORY Remarkably, even though plants represent the most readily available and abun- dant food source in terrestrial ecosystems, only a limited number of chelicerate and hexapod lineages adopted a phytophagous lifestyle. Within Hexapoda, her- bivory is only detected in nine living orders (Labandeira, 2002; Schoonhoven et al., 2006; Strong et al., 1984), while in Chelicerata, and more specifically, in the terrestrial class of the Arachnida, adaptations to obligate phytophagy mainly occurred in the order of the Trombidiformes which belongs to the subclass of mites and ticks (or the Acari) (Krantz & Lindquist, 1979; Lindquist, 1998) (FIGURE 1.1). It is argued that only a restricted number of arthropod lineages were able to develop a phytophagous lifestyle because the unique composition of land plants makes them arduous and unfavorable food. First, plant cells are enclosed in a recalcitrant cell wall which arthropods can find hard to penetrate due to its 12 Nicky-ch1_Vera-ch1.qxd 18/08/201514:32Page13 13 FIGURE 1.1. Dated evolutionary history of the Arthropoda phylum. Time line and phylogeny are based on a combination of sources Chapter 1 (Dabert et al., 2010; Hedges & Kumar, 2009; Lindquist, 1998; Regier et al., 2010; Yeates et al., 2012). Divergence times within Acariformes are still under much debate. Lineages within the Hexapoda and Chelicerata subphyla are marked in blue. Clades possess- ing phytophagous species have their names printed in bold green font. Nicky-ch1_Vera-ch1.qxd 18/08/2015 14:32 Page 14 General Introduction mechanical strength as well as to digest due to an inherently inadequate battery of enzymes to break down cellulose, lignin or pectin (Carpita & Gibeaut, 1993; Heredia, 2003; Sorensen et al., 2010; Whetten & Sederoff, 1995). Second, arthropods and plants have a distinctly different chemical composition, charac- terized by a relative high protein and carbohydrate content, respectively (Mattson, 1980; Strong et al., 1984). Another evolutionary hurdle for plant feed- ing arthropods is thus to elevate between what they nutritionally need for their own development and what plant tissues offer in terms of nutrients. Third, once arthropods (and other organisms) evolved to access and feed on plant tissue, host plants counteracted by developing anti-herbivore defenses. Plant resistance to herbivores is achieved by physical barriers (which include tri- chomes, spines and rough leaves) and/or by producing chemical defenses (Howe & Jander, 2008). These defensive phytochemicals (or ‘plant allelochem- icals’) can both repulse and poison herbivores or interfere with the assimilation of plant nutrients inside the herbivore’s gut (Whittaker & Feeny, 1971). These are only a few of many evolutionary obstacles arthropods face on their road to herbivory. However, once an arthropod species successively underwent the necessary adaptive breakthroughs (or key innovations), it is thought that the acquired ability to colonize a new plant or plant family can pro- mote massive species diversifications (Mitter et al., 1988). Indeed, within the Hexapoda subphylum, the herbivorous lineages belong to the most species rich orders, with the Coleoptera and Lepidoptera (349,000 and 119,000 species, respectively) on top (Labandeira, 2002; Schoonhoven et al., 2006; Strong et al., 1984). In parallel, two obligate phytophagous Acari superfamilies (Tetrany - choidea and Eriophyoidea) are also exceptionally species rich (Krantz & Lindquist, 1979; Lindquist, 1998). 1.1.2. HOST PLANT RANGE OF ARTHROPOD HERBIVORES Depending on the potential host plant species range, arthropod herbivores are traditionally divided into specialists (which exhibit mono- and oligophagy) and generalists (which are polyphagous). FIGURE 1.2 depicts some example species along the scale from being strictly monophagous to polyphagous. In contrast to specialists, generalist herbivores are able to feed and develop on plants belong- ing to unrelated, phylogenetically distinct plant families. Within arthropods, there has been an evolutionary trend to specialize to specific host plants (Nosil, 2002; Schoonhoven et al., 2006), making true polyphagous herbivores scarce. Indeed, less than 10% of all phytophagous insects are able to feed on plants of 14 Nicky-ch1_Vera-ch1.qxd 18/08/2015 14:32 Page 15 Chapter 1 more than three plant families (Bernays & Graham, 1988). However, these rare polyphagous herbivores can be found in diverse orders, both within Hexapoda and Chelicerata (Krantz & Lindquist, 1979; Lindquist, 1998; Schoonhoven et al., 2006; Strong et al., 1984). 1.2. PHYTOPHAGOUS MITES Mites are placed in the Acari subclass within the largest chelicerate class of the Arachnida. They can be distinguished from their closest chelicerate and arachnid relatives by their unique body plan, small size (never exceeding a few centimeters) and great diversity in life styles. The mite body consists of one single segment and is artificially divided into the gnathosoma, the feeding region holding the primary organs of food acquisition (e.g. chelicerae and pedipalps), and the idiosoma, which is the site for all other life functions, e.g. locomotion, post-oral digestion, and reproduction. Mites adapted to a diverse range of ecological niches and diversified the structure of their chelicerae allowing them to feed on plants, bac- teria, animals and fungi (Walter & Proctor, 1999). Although a handful of mite species in the Sarcoptiformes order can be classified as herbivores, adaptations to obligate phytophagy predominantly occurred in the order of the Trombidiformes and have led to three major phytophagous mite clades: Eriophyoidea, Tetrany - choidea, and Tarsonemidae of which the latter belongs to the Heterostigmata lin- eage (Krantz & Lindquist, 1979; Lindquist, 1998) (FIGURE 1.1). 1.2.1. BIOLOGY AND MORPHOLOGY OF PHYTOPHAGOUS MITES The chelicerae of phytophagous mites are modified into a stylet-like structure allowing the mites to feed from plants by piercing plant cells and sucking up cell- content. Tarsonemid, tetranychoid and eriophyoid mites are morphologically distinguishable from one another. While tetranychoid mites exceed 400 µm, the size of eriophyoid and tarsonemid mites only ranges between 90 and 350 µm. Adult eriophyoid mites have a more elongated worm-like body with only two pairs of legs, while adult tetranychoid and tarsonemid mites have four pairs. In tarsonemid males, the fourth pair of legs is extensively modified and used to carry a quiescent
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