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Evaluating DNA Barcoding for Species Identification And Evaluating DNA Barcoding for Species Identification and Discovery in European Gracillariid Moths Carlos Lopez-Vaamonde, Natalia Kirichenko, Alain Cama, Camiel Doorenweerd, H. Charles J. Godfray, Antoine Guiguet, Stanislav Gomboc, Peter Huemer, Jean-François Landry, Ales Laštůvka, et al. To cite this version: Carlos Lopez-Vaamonde, Natalia Kirichenko, Alain Cama, Camiel Doorenweerd, H. Charles J. Godfray, et al.. Evaluating DNA Barcoding for Species Identification and Discovery in Euro- pean Gracillariid Moths. Frontiers in Ecology and Evolution, Frontiers Media S.A, 2021, 9, 10.3389/fevo.2021.626752. hal-03149644 HAL Id: hal-03149644 https://hal.sorbonne-universite.fr/hal-03149644 Submitted on 23 Feb 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. fevo-09-626752 February 14, 2021 Time: 16:51 # 1 ORIGINAL RESEARCH published: 18 February 2021 doi: 10.3389/fevo.2021.626752 Evaluating DNA Barcoding for Species Identification and Discovery in European Gracillariid Moths Carlos Lopez-Vaamonde1,2*, Natalia Kirichenko3,4, Alain Cama5, Camiel Doorenweerd6,7, H. Charles J. Godfray8, Antoine Guiguet9, Stanislav Gomboc10, Peter Huemer11, Jean-François Landry12, Ales Lašt ˚uvka13, Zdenek Lašt ˚uvka14, Kyung Min Lee15, David C. Lees16, Marko Mutanen15, Erik J. van Nieukerken7, Andreas H. Segerer17, Paolo Triberti18, Christian Wieser19 and Rodolphe Rougerie20 1 INRAE, URZF, Orléans, France, 2 IRBI, UMR 7261, CNRS-Université de Tours, Tours, France, 3 Sukachev Institute of Forest, Siberian Branch of Russian Academy of Sciences, Federal Research Center “Krasnoyarsk Science Center SB RAS,” Krasnoyarsk, Russia, 4 Siberian Federal University, Krasnoyarsk, Russia, 5 La Chapelle sur Loire, France, 6 Department Edited by: of Plant and Environmental Protection Sciences, College of Tropical Agriculture and Human Resources, University of Hawaii, 7 8 Bernd Schierwater, Honolulu, HI, United States, Naturalis Biodiversity Center, Leiden, Netherlands, Department of Zoology, University 9 University of Veterinary Medicine of Oxford, Oxford, United Kingdom, Department of Biology, The Pennsylvania State University, University Park, PA, 10 11 Hannover, Germany United States, Gancani, Beltinci, Slovenia, Tiroler Landesmuseen Betriebsges.m.b.H., Sammlungs- und Forschungszentrum, Hall in Tirol, Austria, 12 Agriculture and Agri-Food Canada, Ottawa Research and Development Centre, Reviewed by: Ottawa, ON, Canada, 13 Prostejov,ˇ Czechia, 14 Faculty of Agronomy, Mendel University, Brno, Czechia, 15 Ecology Felix David, and Genetics Research Unit, University of Oulu, Oulu, Finland, 16 Department of Life Sciences, Natural History Museum, University of Veterinary Medicine London, United Kingdom, 17 Staatliche Naturwissenschaftliche Sammlungen Bayerns, Zoologische Staatssammlung Hannover, Germany München (SNSB-ZSM), Munich, Germany, 18 Museo Civico di Storia Naturale, Zoologia, Verona, Italy, 19 Landesmuseum für Wiebke Feindt, Kärnten, Abteilung Zoologie, Sammlungs- und Wissenschaftszentrum, Klagenfurt, Austria, 20 Institut de Systématique, Tierärztliche Hochschule Hannover, Evolution, Biodiversité (ISYEB), Muséum national d’Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Germany Antilles, Paris, France *Correspondence: Carlos Lopez-Vaamonde [email protected] Gracillariidae is the most species-rich leaf-mining moth family with over 2,000 described species worldwide. In Europe, there are 263 valid named species recognized, many of Specialty section: which are difficult to identify using morphology only. Here we explore the use of DNA This article was submitted to Phylogenetics, Phylogenomics, barcodes as a tool for identification and species discovery in European gracillariids. and Systematics, We present a barcode library including 6,791 COI sequences representing 242 of the a section of the journal Frontiers in Ecology and Evolution 263 (92%) resident species. Our results indicate high congruence between morphology Received: 06 November 2020 and barcodes with 91.3% (221/242) of European species forming monophyletic clades Accepted: 27 January 2021 that can be identified accurately using barcodes alone. The remaining 8.7% represent Published: 18 February 2021 cases of non-monophyly making their identification uncertain using barcodes. Species Citation: discrimination based on the Barcode Index Number system (BIN) was successful Lopez-Vaamonde C, Kirichenko N, Cama A, for 93% of species with 7% of species sharing BINs. We discovered as many as Doorenweerd C, Godfray HCJ, 21 undescribed candidate species, of which six were confirmed from an integrative Guiguet A, Gomboc S, Huemer P, Landry J-F, Lašt ˚uvkaA, Lašt ˚uvkaZ, approach; the other 15 require additional material and study to confirm preliminary Lee KM, Lees DC, Mutanen M, evidence. Most of these new candidate species are found in mountainous regions of van Nieukerken EJ, Segerer AH, Mediterranean countries, the South-Eastern Alps and the Balkans, with nine candidate Triberti P, Wieser C and Rougerie R (2021) Evaluating DNA Barcoding species found only on islands. In addition, 13 species were classified as deep for Species Identification conspecific lineages, comprising a total of 27 BINs with no intraspecific morphological and Discovery in European Gracillariid Moths. Front. Ecol. Evol. 9:626752. differences found, and no known ecological differentiation. Double-digest restriction-site doi: 10.3389/fevo.2021.626752 associated DNA sequencing (ddRAD) analysis showed strong mitonuclear discrepancy Frontiers in Ecology and Evolution| www.frontiersin.org 1 February 2021| Volume 9| Article 626752 fevo-09-626752 February 14, 2021 Time: 16:51 # 2 Lopez-Vaamonde et al. Hidden Diversity in Leaf-Mining Moths in four out of five species studied. This discordance is not explained by Wolbachia- mediated genetic sweeps. Finally, 26 species were classified as “unassessed species splits” containing 71 BINs and some involving geographical isolation or ecological specialization that will require further study to test whether they represent new cryptic species. Keywords: barcode index number, cryptic diversity, Gracillariidae, Lepidoptera, mitonuclear discordance, new candidate species, RAD sequencing, Wolbachia INTRODUCTION the discrepancy is mitochondrial drive causing the replacement of one mitotype by another due to the introduction of the Alarming projections of biodiversity loss indicate that we have intracellular bacterium Wolbachia which spreads by causing entered the world’s sixth mass extinction (Raven and Miller, cytoplasmic incompatibility, or by another agent with the same or 2020). Meanwhile, only a small fraction of species on Earth have similar genetic strategy. Divergent COI clusters have been found been formally described and assigned a scientific name (Scheffers to have different Wolbachia strains in some (Kodandaramaiah et al., 2012), so many taxa are likely to go extinct before we know et al., 2013) but not all cases (Bereczki et al., 2015). of their existence (Eggleton, 2020). The incompleteness of our Here, we explore the diversity of European Gracillariidae, current census of life, referred as the “Linnean shortfall” (Raven the largest family of leaf-mining micro-moths, by analyzing and Wilson, 1992), is especially acute for the most diverse yet least DNA barcode data in the context of the current taxonomy studied groups such as small insects, and for the high diversity of the family on a continental scale. The Gracillariidae are tropics (Delabye et al., 2019; Lopez-Vaamonde et al., 2019). one of the most species-rich families of Lepidoptera with The increasing use of genetic tools in species discovery has 1996 described species worldwide, data on September 23, shown the shortfall to be greater than previously recognized 2020 (De Prins and De Prins, 2020), though many more because of the frequent discovery of sets of two or more cryptic species await description, particularly in the neotropics (Lees species that have been incorrectly classified as a single taxon due et al., 2014). In contrast, the faunistics, alpha taxonomy and to their morphological similarity. In particular, DNA barcoding, ecology of this family in Europe are relatively well known a tool for species identification based on the use of a single (Doorenweerd et al., 2014), with 24 genera and 263 species standard DNA marker (a fragment of the COI mtDNA gene; recorded (Supplementary Table S1). The majority of gracillariids Hebert et al., 2003), has contributed to the discovery of many are leaf miners (their larvae feed and live within a single new species, including among them the most closely studied leaf) and feed on a huge diversity of different host plants and best documented groups of organisms (Hrbek et al., 2014). (De Prins and De Prins, 2020). However, most species are Some of those new species are cryptic, rare and of conservation monophagous or oligophagous (Lopez-Vaamonde et al., 2003). value; assessing the level of cryptic diversity and identifying Several species are serious pests of agricultural and ornamental their biodiversity
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