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Serpentes: Viperinae) Amphibia-Reptilia 41 (2020): 285-311 brill.com/amre Review Evaluating taxonomic inflation: towards evidence-based species delimitation in Eurasian vipers (Serpentes: Viperinae) Inês Freitas1,∗, Sylvain Ursenbacher2,3, Konrad Mebert4,5, Oleksandr Zinenko6, Silke Schweiger7, Wolfgang Wüster8,JoséC.Brito1, Jelka Crnobrnja-Isailovic´9,10, Bálint Halpern11, Soumia Fahd12, Xavier Santos1, Juan M. Pleguezuelos13, Ulrich Joger14, Nikolay Orlov15, Edvárd Mizsei16,17, Olivier Lourdais18, Marco A.L. Zuffi19, Alexandru Strugariu20,¸Stefan Remus Zamfirescu21, Íñigo Martínez-Solano22, Guillermo Velo-Antón1, Antigoni Kaliontzopoulou1, Fernando Martínez-Freiría1,* Abstract. The designation of taxonomic units has important implications for the understanding and conservation of biodiversity. Eurasian vipers are a monophyletic group of viperid snakes (Serpentes, Viperinae), currently comprising four genera (Daboia, Macrovipera, Montivipera and Vipera) and up to 40 species. Taxonomic units have been described using a wide variety of methods and criteria, and consequently, considerable controversy still surrounds the validity of some currently listed species. In order to promote a consensus- and evidence-based taxonomy of Eurasian vipers, we analysed published mitochondrial and nuclear DNA sequences for this group to reconstruct phylogenetic relationships among currently recognized viper species. We also compiled information on external morphology to assess their morphological distinctiveness. Phylogenetic inference based on mtDNA sequences shows contrasting levels of divergence across genera and species and identifies several instances of non-monophyly in described species. Nuclear DNA sequences show extremely low levels of genetic variation, with a widespread pattern of allele sharing among distant species, and even among genera. Revision of morphological data shows that most species designations rely on scalation traits that overlap extensively among species of the same genus. Based on our combined assessment, we recognize 15 taxa as valid species, three taxa which likely represent species complexes, 17 taxa of doubtful validity as species, and five taxa for which species status is maintained but further research is highly recommended to assess taxonomic arrangements. We stress the need to implement integrative taxonomic approaches for the recognition of evidence-based taxonomic units in Eurasian vipers. Keywords: integrative taxonomy, morphology, mt-DNA, nuclear DNA, phylogeny, Viperidae. 1 - CIBIO/InBIO – Research Center in Biodiversity and Vienna, Burgring 7, 1010 Vienna, Austria Genetic Resources of the University of Porto, Vairão, 8 - Molecular Ecology and Fisheries Genetics Laboratory, Portugal School of Natural Sciences, Bangor University, Bangor 2 - Department of Environmental Science, Section of Con- LL57 2UW, Wales, UK servation Biology, University of Basel, Basel, Switzer- 9 - Faculty of Sciences and Mathematics, University of land Niš, Niš, Serbia 3 - info fauna-karch, Centre de coordination pour la pro- 10 - Institute for Biological Research “S. Stankovic”,´ Uni- tection des amphibiens et des reptiles de Suisse, versity of Belgrade, Belgrade, Serbia Neuchâtel, Switzerland 11 - MME BirdLife Hungary, Budapest, Hungary 4 - Global Biology, Waldmattstr, Birr, Switzerland 12 - Faculté des Sciences de Tétouan, Université Abdel- 5 - IDECC, Institute of Development, Ecology, Conserva- malek Essaâdi, Tétouan, Morocco tion and Cooperation, Rome, Italy 13 - Departamento de Zoología, Facultad de Ciencias, Uni- 6 - Museum of Nature, V. N. Karazin Kharkiv national versidad de Granada, Granada, Spain University, Kharkiv, Ukraine 14 - State Natural History Museum, Braunschweig, Ger- 7 - Herpetological Collection, Natural History Museum many Downloaded from PubFactory at 08/07/2020 12:07:29PM © Freitas et al., 2020. DOI:10.1163/15685381-bja10007via free access This is an open access article distributed under the terms of the CC-BY 4.0 License. 286 I. Freitas et al. Introduction species are therefore intended to identify bio- logically cohesive populations with recent com- The designation of taxonomic units has impor- mon ancestry rather than to recognize unusual tant implications for the way we study, describe patterns of distribution or morphology (Kaiser and understand biodiversity, as well as for how et al., 2013). we mobilize efforts and allocate resources to de- Eurasian vipers are a monophyletic group velop conservation strategies. Over the years, within the subfamily Viperinae (Serpentes, different criteria and tools have been used to de- Viperidae), whose members are distributed pri- fine species, leading to a succession of species marily in the Palaearctic region, i.e., non- concepts that resulted in extended controversy tropical Eurasia and North Africa (Phelps, within the research community (Mayden, 1997; 2010). This group is phylogenetically sister to de Queiroz, 2007). Nowadays, a species is of- a clade of Middle Eastern vipers, constituted ten defined as a separately evolving metapop- by the genera Eristicophis and Pseudocerastes ulation lineage that possesses relevant charac- (see Phelps, 2010; Zheng and Wiens, 2016), teristics that allow assessing its distinctiveness which are not considered in this work. At the from others (i.e., the unified species concept; time of writing, the most recent and comprehen- de Queiroz, 2007, and its precursor, the evolu- sive list of reptiles (i.e., The Reptile Database; tionary species concept; Simpson, 1961; Wiley, Uetz, Freed and Hošek, 2019) lists four gene- 1978; Frost and Hillis, 1990). This definition is ra and 40 species within Eurasian vipers (ta- linked to the integrative taxonomy framework, ble 1): Daboia, with 4 species; Macrovipera, which is based on the combination of different with 3 species; Montivipera, with 8 species; lines of evidence (e.g., genetic, morphological, and Vipera, with 25 species. However, Eurasian ecological) and methodologies (e.g., phyloge- vipers have a long taxonomic history, and dif- netic inference, ordination methods, ecological ferent authors have used a wide variety of meth- modelling) to objectively identify taxa (Dayrat, ods and criteria to define taxonomic units, as re- 2005) that – in an ideal case – would repre- flected in previous species lists (e.g., Mallow, sent independently evolving species. Names of Ludwig and Nilson, 2003; Phelps, 2010). At the genus level, the history of Eurasian 15 - Zoological Institute, Russian Academy of Sciences, St. vipers is relatively simple. Through most of the Petersburg, Russia 20th century, all species considered here were 16 - Department of Tisza River Research, Centre for Eco- included in the single genus Vipera (Boulenger, logical Research, Hungarian Academy of Sciences, De- 1896, 1913; Schwarz, 1936; Klemmer, 1963; brecen, Hungary Minton, Dowling and Russel, 1968). The mav- 17 - Department of Ecology, University of Debrecen, De- brecen, Hungary erick German herpetologist Albert Franz 18 - Centre d’Etudes Biologiques de Chizé, CNRS, UMR Theodor Reuss described numerous genera 7372, Villiers en Bois, France within the Eurasian vipers (reviewed by Krec- 19 - University of Pisa – Museum Natural History, Calci sák, 2007), but these gained little traction with (Pisa), Italy subsequent authors, except where the names 20 - Research Department – Faculty of Biology, “Alexandru Ioan Cuza” University of Ia¸si, Ia¸si, Romania had priority for subsequently validated clades. 21 - Department of Biology – Faculty of Biology, “Alexan- Obst (1983) was the first author to challenge the dru Ioan Cuza” University of Ia¸si, Ia¸si, Romania monogeneric classification of Eurasian vipers, 22 - Museo Nacional de Ciencias Naturales – CSIC, by separating the larger species into the genus Madrid, Spain ∗ Daboia, together with Pseudocerastes.This Corresponding author; e-mail: ifi[email protected]; split however, was not adopted by most subse- [email protected] quent researchers. Herrmann, Joger and Nilson Downloaded from PubFactory at 08/07/2020 12:07:29PM via free access Species delimitation in Eurasian vipers Table 1. Currently listed species of Eurasian vipers according to Uetz, Freed and Hošek (2019), depicting the criteria used for species designation, our recommended status, in some cases provisional, including justification, suggestions for further work and IUCN red list category (also for included taxa). Percentages of divergence from the closest sister species or clade are given for a small fragment of cyt b (196 bp; supplementary table S3). “DVAS” means Doubtful Validity As Species, may represent geographic variation, a subspecies or diverged population, hence, currently we recommend to decline its species status; “LSC” means Likely Species Complex (i.e., group of closely related taxa, possibly more than one species, but delimitations are not clear yet), hence, currently maintain species status; and “pending” indicates that, despite some incongruences with the divergence threshold delimitation, single-species recognition is currently maintained, but further research is required to assess taxonomic status. Cyt b divergence categories: Low = 2% or less; Moderate = 3or4%;High= 5% or more. LC = Least Concern; NT = Near Threatened; VU = Vulnerable; EN = Endangered; CR = Critically Endangered. Species Criteria Status Reason Further work IUCN Daboia mauritanica morphological species high genetic divergence (15%) NT (D. Gray, 1849 deserti NT) Daboia palaestinae morphological species high genetic divergence (15%) LC (Werner, 1938) Daboia
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