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Phylogeny, Species Delimitation and Biogeography of the Endemic

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Phylogeny, Species Delimitation and Biogeography of the Endemic applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Zoological Journal of the Linnean Society, 2021, XX, 1–17. With 4 figures. Phylogeny, species delimitation and biogeography of the endemic Palaearctic tribe Tomarini (Lepidoptera: Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab055/6358824 by guest on 01 October 2021 Lycaenidae) ANATOLY V. KRUPITSKY1,2,*, , NAZAR A. SHAPOVAL3, DMITRY M. SCHEPETOV4, IRINA A. EKIMOVA4, and VLADIMIR A. LUKHTANOV3, 1Department of Entomology, Biological Faculty, Lomonosov Moscow State University, Leninskie gory, GSP-1, korp. 12, Moscow 119991, Russia 2Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky prospect 33, Moscow 119071, Russia 3Department of Karyosystematics, Zoological Institute of the Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg 199034, Russia 4Department of Invertebrate Zoology, Biological Faculty, Lomonosov Moscow State University, Leninskie gory, GSP-1, korp. 12, Moscow 119991, Russia Received 31 March 2021; revised 20 May 2021; accepted for publication 6 July 2021 The tribe Tomarini is represented by the sole genus Tomares, comprising about eight species distributed from the western Mediterranean to Central Asia. We carried out a multilocus phylogenetic and a biogeographical analysis to test the taxonomy of the genus by several molecular species delimitation methods and reveal patterns shaping the current distribution of Tomares. The phylogenetic analysis based on four molecular markers recovered the monophyly of the genus and recovered two deep-branching lineages: an African clade and an Asian clade. Species delimitation analyses suggested six or ten putative species depending on the method applied. The haplotype network analysis of the Tomares nogelii clade revealed no phylogeographical and taxonomic structure. We consider the taxon Tomares nesimachus (syn. nov.) a synonym of T. nogelii and reinstate Tomares callimachus dentata stat. rev. for populations from south-eastern Turkey. Tomares originated between the early Oligocene and the early Miocene, most probably in south-west Asia. The split of the most recent common ancestor of Tomares occurred between the middle-late Miocene and middle-late Pliocene, probably as a response to increasing aridification and habitat fragmentation. Differentiation of the Asian clade took place in south-west Asia during the Pliocene and Pleistocene and coincided temporally with the evolution of Tomares host plants of the genus Astragalus (Fabaceae). ADDITIONAL KEYWORDS: evolution – molecular phylogeny – phylogeography – taxonomy. INTRODUCTION territory of the modern south-western Palaearctic underwent numerous interconnected geological and A large biogeographical area covering the climatic changes (Steininger & Rögl, 1996; Zachos Mediterranean, south-west Asia, the Pontic- et al., 2001). From an evolutionary viewpoint, the Caspian region and Central Asia, also known as most crucial events were uplifts and formations of the south-western Palaearctic, or Tethyan (Ancient mountain systems and islands, the closure of the Mediterranean) Subkingdom of the Boreal Kingdom Tethys Ocean, the Messinian salinity crisis and sensu Takhtajan (1986), is united by geological history Quaternary geological changes, including series of (de Lattin, 1967; Takhtajan, 1986). The distribution glaciations and interglacial periods (Hewitt, 2004; of organisms in the Tethyan region has been strongly Schmitt, 2007; Hamon et al., 2013; Pirouz et al., 2017). influenced by historical factors. In particular, the These events created conditions for the dispersal of organisms and speciation and shaped the region in *Corresponding author. E-mail: [email protected] question as a biodiversity hotspot (Myers et al., 2000). © 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–17 1 2 KRUPITSKY ET AL. The south-western Palaearctic is an area containing Nekrutenko & Effendi, 1980, Tomares fedtschenkoi many endemic groups of butterflies, including (Erschoff, 1874) and Tomares mauritanicus (Lucas, remarkable genera of Papilionidae, such as Zerynthia 1849) are characterized by distinct morphological Ochsenheimer, 1816, Allancastria Bryk, 1932, Archon diagnostic traits and are easily recognizable, whereas Hübner, 1822 and Hypermnestra Ménétriés, 1848, the status of the taxa Tomares dobrogensis Caradja, Pieridae genus Zegris Boisduval, 1836, and numerous 1895, Tomares nesimachus Oberthür, 1894, Tomares Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab055/6358824 by guest on 01 October 2021 genera and subgenera of Nymphalidae and Lycaenidae, nogelii Herrich-Schäfer, 1851, Tomares romanovi including the diverse subgenus Agrodiaetus Hübner, Christoph, 1882 and Tomares telemachus Zhdanko, 1822. This region is also a diversity centre for many 2000, constituting the T. nogelii complex sensu Nazari Holarctic butterfly genera. & Ten Hagen (2020), remains disputable in different Historical biogeography and evolution of the taxonomic works (Van Oorschot & Wagener, 2000; Palaearctic butterflies has been a focus of numerous Weidenhoffer & Bozano, 2007; Nazari & Ten Hagen, studies. Several main geological events have been 2020). The morphological investigations (Van Oorschot hypothesized to play a key role in the diversity and & Wagener, 2000) and integrative studies combining evolution of the south-western Palaearctic butterfly morphological and molecular phylogenetic analyses genera. Quaternary glaciations shaped distribution based on fragments of COI and EF1α genes recently in the case of Pyrgus Hübner, 1819 (Hernández- performed by Nazari & Ten Hagen (2020) have Roldán et al., 2011), Proterebia Roos & Arnscheid, revealed no clear differentiation between the species 1980 (Bartoňová et al., 2018), Maniola Schrank, 1801 of this group. Research by Nazari & Ten Hagen (2020) (Kreuzinger et al., 2015) and Melanargia Meigen, reduced the number of Tomares species to eight by 1828 (Habel et al., 2005). Orogenies and isolations of formally synonymizing T. telemachus with T. romanovi landmasses acted as drivers of diversification in the and reconsidering the status of T. dobrogensis as a case of Allancastria (Nazari & Sperling, 2007; Nazari subspecies of T. nogelii. et al., 2007) and Hypermnestra (Nazari & Sperling, The species of the genus Tomares inhabit warm, 2007). Formation of the Mediterranean Basin, the grassy biotopes, from a coastal zone to a subalpine Messinian salinity crisis and Quaternary glaciations mountain belt ≤ 3000 m a.s.l. (Larsen, 1974; induced radiation and dispersal in Zerynthia (Nazari Hesselbarth et al., 1995; Tuzov et al., 2000). Larval host & Sperling, 2007; Dapporto, 2010), Pararge Hübner, plants of the genus are different species of Fabaceae 1819 (Weingartner et al., 2006; Livraghi et al., 2018) (Higgins & Riley, 1970; Weidenhoffer & Vanek, 1977; and Pseudophilotes Beuret, 1958 (Todisco et al., 2018; Jordano et al., 1990; Hesselbarth et al., 1995; Tennent, Bartoňová et al., 2020). 1996; Tuzov et al., 2000; Muñoz Sariot, 2011). Some One of the butterfly genera endemic to the south- species are monophagous or oligophagous, using only western Palaearctic is Tomares Rambur, 1840, from one or several species of the legume genera Astragalus the family Lycaenidae, subfamily Theclinae, the sole and Astracantha (Zhdanko, 1997; Van Oorschot & member of the tribe Tomarini Eliot, 1973. This tribe Wagener, 2000; Tuzov et al., 2000). Most Tomares was erected on the basis of external morphological species are locally distributed and strongly connected characters (Eliot, 1973). Later, Kuznetsov & Stekolnikov with their host plants. As a consequence, they suffer (2001) confirmed this treatment based on study of the from overgrazing and destruction of habitats owing functional morphology of the male genitalia. In recent to human activities. Some of them are of conservation phylogenetic studies, Tomarini is recovered as a sister concern in several regions; for instance, T. nogelii was group to a clade comprising Eumaeini, Loxurini and listed as a vulnerable species in Europe (regionally Deudorigini (Espeland et al., 2018). extinct in the European Union) in the International According to the taxonomic reviews of the genus, Union for Conservation of Nature European Red Tomares comprises between eight and ten species List of Butterflies (Van Swaay et al., 2010) and the (Hesselbarth & Schurian, 1984; Hesselbarth et al., Red Book of Ukraine (Budashkin & Plyushch, 2009), 1995; Van Oorschot & Wagener, 2000; Tuzov et al., and critically endangered and locally extinct in the 2000; Weidenhoffer & Bozano, 2007; Nazari & Ten Romanian Red List of Butterflies (Rákosy, 2003). Hagen, 2020) distributed throughout the south- The distribution range of the genus Tomares is western Palaearctic. The centre of diversity for the broadly divided into two disjoint parts. The first genus lies in Anatolia (Turkey), where up to six one comprises the territory uniting North Africa species have been recorded, some of them living and the western Mediterranean of Europe from sympatrically in certain localities (Hesselbarth Portugal to France, hosting two species (T. ballus and et al., 1995; Van Oorschot & Wagener, 2000). Species T. mauritanicus). The second part of the range is a wide such as Tomares ballus (Fabricius, 1787), Tomares area uniting the Pontic-Caspian and Irano-Turanian callimachus (Eversmann, 1848), Tomares desinens regions, which
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