Conserved Metallomics in Two Insect Families Evolving Separately for a Hundred Million Years

View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Crossref Biometals (2014) 27:1323–1335 DOI 10.1007/s10534-014-9793-9 Conserved metallomics in two insect families evolving separately for a hundred million years Polychronis Rempoulakis • Negar Afshar • Beatriz Osorio • Martha Barajas-Aceves • Joanna Szular • Sohel Ahmad • Thilakasiri Dammalage • Ulysses Sto Tomas • Esther Nemny-Lavy • Mor Salomon • Marc J. B. Vreysen • David Nestel • Fanis Missirlis Received: 11 July 2014 / Accepted: 14 September 2014 / Published online: 9 October 2014 Ó The Author(s) 2014. This article is published with open access at Springerlink.com Abstract Letal cofactors are required for enzymatic These fruit flies can be polyphagous (e.g., Ceratitis catalysis and structural stability of many proteins. capitata) or strictly monophagous (e.g., Bactrocera Physiological metal requirements underpin the evolu- oleae) or oligophagous (e.g., Anastrepha grandis)and tion of cellular and systemic regulatory mechanisms for were maintained in the laboratory on five distinct diets metal uptake, storage and excretion. Considering the based on olive oil, carrot, wheat bran, zucchini and role of metal biology in animal evolution, this paper molasses, respectively. The data indicate that overall asks whether metal content is conserved between metal content and distribution between the Tephritidae different fruit flies. A similar metal homeostasis was and Drosophilidae species was similar. Reduced metal previously observed in Drosophilidae flies cultivated on concentration was observed in B. oleae. Feeding the the same larval medium. Each species accumulated in polyphagous C. capitata with the diet of B. oleae the order of 200 lg iron and zinc and approximately resulted in a significant quantitative reduction of all ten-fold less manganese and copper per gram dry metals. Thus, dietary components affect metal content weight of the adult insect. In this paper, data on the in some Tephritidae. Nevertheless, although the evi- metal content in fourteen species of Tephritidae, which dence suggests some fruit fly species evolved prefer- are major agricultural pests worldwide, are presented. ences in the use or storage of particular metals, no metal P. Rempoulakis Á S. Ahmad Á T. Dammalage Á B. Osorio Á F. Missirlis (&) U. S. Tomas Á M. J. B. Vreysen Departamento de Fisiologıá, Biofı´sica y Neurociencias, IAEA Laboratories, Insect Pest Control Laboratory, Centro de Investigacioń y de Estudios Avanzados Joint FAO/IAEA Programme of Nuclear del Instituto Politećnico Nacional, Av. IPN 2508, Techniques in Food and Agriculture, Zacatenco, Mexico City, Mexico International Atomic Energy Agency, Seibersdorf, e-mail: fanis@fisio.cinvestav.mx Austria M. Barajas-Aceves P. Rempoulakis Á E. Nemny-Lavy Á D. Nestel Departamento de Biotecnologıá y Bioingenerıá, Department of Entomology, Institute of Plant Protection, Centro de Investigacioń y de Estudios Avanzados del Agricultural Research Organization (ARO), Instituto Politećnico Nacional, Av. IPN 2508, The Volcani Center, Beit Dagan, Israel Zacatenco, Mexico City, Mexico N. Afshar Á J. Szular M. Salomon School of Biological and Chemical Sciences, Citrus Division, The Israel Cohen Institute for Biological Queen Mary University of London, Mile End Road, Control, Plants Production and Marketing Board, London, UK Beit Dagan, Israel 123 1324 Biometals (2014) 27:1323–1335 concentration varied in order of magnitude between paper, we addressed the hypothesis that this relative these two families of Diptera that evolved indepen- stability of laboratory-maintained Drosophilidae met- dently for over 100 million years. allomes is also conserved in other fruit flies. Along with the family Drosophilidae, the family Keywords Physiology Á Evolution Á Genetics Á Tephritidae (true fruit flies) belongs to the insect order Nutrition Á Fruit flies of economic importance Á Diptera. The Tephritidae form a highly variable group Agriculture Á Mediterranean fruit fly of approximately five thousand described species belonging to five hundred genera (Aluja and Norrbom 1999; White and Elson-Harris 1994). The larvae in the majority of these species are phytophagous, feeding Introduction exclusively on plant tissues and pose a significant threat to agriculture in many regions of the world. The An obvious consideration in the evolution of flies and host range varies significantly among the different all organisms is the physiologic use of metals as species, with some being highly polyphagous, e.g., the cofactors in proteins (Cyert and Philpott 2013; God- Mediterranean fruit fly Ceratitis capitata has 356 frey and Glass 2011; Hansch and Mendel 2009). Metal recorded fruit and vegetable hosts (Liquido et al. 1991; homeostasis arises from the combination of regulating Hancock et al. 2000; De Meyer et al. 2002). Other dietary absorption and organismal storage and excre- species are strictly monophagous, e.g., the olive fruit tion to ensure tissues and cells have sufficient metal fly Bactrocera oleae, which feeds only on the olive ions available for biological use (Mandilaras et al. fruit mesocarp (Tzanakakis 2003), or oligophagous, 2013; Southon et al. 2013; Tang and Zhou 2013). feeding on a small range of hosts, e.g., the South Dietary absorption, in turn, is under continuous American cucurbit fruit fly Anastrepha grandis. environmental influence forming a key ecological Colonies of fruit flies were maintained at the Insect factor defining each species’ niche (Forbes et al. 2009; Pest Control Laboratory (IPCL) of the joint Food and Lang et al. 2012; Sharon et al. 2010). The extent to Agriculture Organization–International Atomic which specialized diets and natural selection affect the Energy Agency (FAO-IAEA) program of Nuclear metal homeostasis systems in different insect orders Techniques in Food and Agriculture of the United has not been investigated. Nations. Appropriate artificial larval diets provide all Previous research has indicated that genetic change the necessary nutrients for the development of the can influence metal homeostasis in Drosophila mel- flies. Rearing of the polyphagous and oligophagous anogaster, a commonly used fly in basic research. flies on a common artificial medium is possible, but Mutations in the X-chromosome of D. melanogaster certain species have unique requirements and the use can cause dramatic changes in total body zinc of natural hosts as rearing medium is still unavoidable. accumulation (Afshar et al. 2013) and mutations in This is the case with species attacking Cucurbitaceae, an iron transporter (Bettedi et al. 2011), or flies like A. grandis (Gomes Silva and Malavasi 1993) and heterozygous for mutations in the iron storage protein the African fruit fly Dacus ciliatus (Zur et al. 2009), ferritin (Gutierrez et al. 2013), accumulate less iron in which have both been maintained on their natural their bodies. Similarly, flies heterozygous for muta- hosts (zucchinis) for a number of generations. tions in Syntaxin 5 accumulate less copper (Norgate In this study, the metal contents in the bodies of et al. 2010). Changes in metal concentrations can also newly emerged adults belonging to 14 different arise by RNA interference (Bahadorani et al. 2010; species of fruit fly, representing the major pests, were Soriano et al. 2013; Xiao et al. 2014). Furthermore, measured. With the exception of D. ciliatus and one when nine species of Drosophilidae, chosen for their population of C. capitata all other insects were differences in ecology and behavior and because their maintained at the IPCL facilities. Whereas previous full genomes had been available (Clark et al. 2007), studies have compared species only within a single were raised on the same larval medium, they showed a family representing perhaps 10–12 million years of similar metal profile, suggesting that evolutionary separation, this resource was used to evaluate evolu- mechanisms exist that shape, and conserve, metal tionary mechanisms operating on insect metal homeo- homeostasis (Sadraie and Missirlis 2011). In this stasis over a much longer period by comparing the 123 Biometals (2014) 27:1323–1335 1325 families Drosophilidae and Tephritidae, which are quarantine pest in Austria and hence, the IPCL has a estimated to have been divergent for 100 million years unique collection of fruit fly strains and species that (Beverley and Wilson 1984; Wulbeck and Simpson allows for parallel and comparative studies of many 2000). In addition, a dietary variable (an olive oil different species. The origin and typical hosts of all supplement) was introduced experimentally to test its strains used in this study are listed in Table 1. The effect on metal accumulations and address the theory number of generations the colonies were maintained at that the oil reduces tissue metal content. Only few the IPCL and the history of each line are shown. Fruit previous studies have addressed whether olive oil flies representing four genera (Bactrocera, Anastre- might have metal chelating properties, and none of pha, Dacus and Ceratitis) were selected for analysis these involved tests with experimental animals (Bri- and experimentation. Bactrocera was represented ante et al. 2003; Paiva-Martins and Gordon 2005; with nine species, Anastrepha with three species, Visioli and Galli 2002). and Ceratitis and Dacus with one species each. The fly colonies were maintained in controlled bioclimatic rooms at a temperature of 25 ± 2 °C, humidity at Materials and methods 65 ± 5 %, and a photoperiod of light to dark

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