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Molecular Phylogeny of the Notostraca ⇑ Michael Korn A,B, , Nicolas Rabet C, Hemant V

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Molecular Phylogeny of the Notostraca ⇑ Michael Korn A,B, , Nicolas Rabet C, Hemant V Molecular Phylogenetics and Evolution 69 (2013) 1159–1171 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogeny of the Notostraca ⇑ Michael Korn a,b, , Nicolas Rabet c, Hemant V. Ghate d, Federico Marrone e, Anna K. Hundsdoerfer a a DNA-Laboratory, Museum of Zoology, Senckenberg Natural History Collections Dresden, Königsbrücker Landstrasse 159, D-01109 Dresden, Germany b Limnological Institute, University of Konstanz, Mainaustr. 252, D-78464 Konstanz, Germany c MNHN, UPMC, CNRS, IRD, UMR, 7208 BOREA 43, rue Cuvier, 75 005 Paris, France d Department of Zoology, Modern College, Shivajinagar, Pune 411 005, India e Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Università di Palermo, via Archirafi 18, I-90123 Palermo, Italy article info abstract Article history: We used a combined analysis of one nuclear (28S rDNA) and three mitochondrial markers (COI, 12S Received 3 November 2012 rDNA, 16S rDNA) to infer the molecular phylogeny of the Notostraca, represented by samples from the Revised 11 July 2013 six continents that are inhabited by this group of branchiopod crustaceans. Our results confirm the Accepted 7 August 2013 monophyly of both extant notostracan genera Triops and Lepidurus with good support in model based Available online 20 August 2013 and maximum parsimony analyses. We used branchiopod fossils as a calibration to infer divergence times among notostracan lineages and accounted for rate heterogeneity among lineages by applying Keywords: relaxed-clock models. Our divergence date estimates indicate an initial diversification into the genera Tri- Triops ops and Lepidurus in the Mesozoic, most likely at a minimum age of 152.3–233.5 Ma, i.e., in the Triassic or Lepidurus Divergence dates Jurassic. Implications for the interpretation of fossils and the evolution of notostracan morphology are Fossil calibration discussed. We further use the divergence date estimates to formulate a biogeographic hypothesis that Relaxed molecular clock explains distributions of extant lineages predominantly by overland dispersal routes. We identified an additional hitherto unrecognised highly diverged lineage within Lepidurus apus lubbocki and three addi- tional previously unknown major lineages within Triops. Within T. granarius we found deep differentia- tion, with representatives distributed among three major phylogenetic lineages. One of these major lineages comprises T. cancriformis, the T. mauritanicus species group and two hitherto unrecognised T. gra- narius lineages. Samples that were morphologically identified as T. granarius diverged from the most basal nodes within this major lineage, and divergence dates suggested an approximate age of 23.7– 49.6 Ma for T. cancriformis, indicating the need for a taxonomic revision of Triassic and Permian fossils that are currently attributed to the extant T. cancriformis. We thus elevate T. cancriformis minor to full spe- cies status as Triops minor Trusheim, 1938 and include in this species the additional Upper Triassic sam- ples that were attributed to T. cancriformis. We further elevate T. cancriformis permiensis to full species status as Triops permiensis Gand et al., 1997. Ó 2013 Elsevier Inc. All rights reserved. 1. Introduction unequal treatment of fossil finds: often, Notostraca with a Triops- like telson (without a terminal supra-anal plate) were ascribed to The Notostraca (tadpole shrimp) represent a group of branchio- T. cancriformis (Gore, 1986; Gand et al., 1997; Kelber, 1999), pod crustaceans that has existed since at least the late Devonian whereas fossils bearing a posterior elongation of their telson into (Garrouste et al., 2012). At least one of its genera, namely Triops a supra-anal plate were always described as new species, either Schrank, 1803, appears to have attained a morphology indistin- within the extant genus Lepidurus Leach, 1819 (see Barnard, guishable from that of modern forms by the Upper Triassic (Trus- 1929), or more often even within a new genus (Yang and Hong, heim, 1938). Due to this similarity to modern forms, these 1980; Tchernyshev, 1940; Hegna and Ren, 2010). The closest Triassic fossils were classified as a subspecies of the extant Triops known relatives of the Notostraca are the Kazacharthra Nozohilov, cancriformis (Trusheim, 1938). This appears to have initiated an 1957, an extinct group of phyllopods known only from the upper Triassic to the lower Jurassic of Asia (Briggs et al., 1993; Olesen, 2009). Together, they form the Calmanostraca Tasch, 1969. The ⇑ Corresponding author. Address: DNA-Labor, Museum für Tierkunde, early Devonian Castracollis wilsonae Fayers and Trewin, 2003 is Königsbrücker Landstrasse 159, D-01109 Dresden, Germany. Fax: +49 0351 either placed in the Calmanostraca (Fayers and Trewin, 2003)or 795841 4327. is treated as sister group to Calmanostraca (Olesen, 2009). E-mail addresses: [email protected] (M. Korn), [email protected] (N. Rabet), [email protected] (H.V. Ghate), [email protected] (F. Marrone), The taxonomy of the Notostraca has been hampered by the [email protected] (A.K. Hundsdoerfer). exceptionally high morphological variability typical of the group, 1055-7903/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2013.08.006 1160 M. Korn et al. / Molecular Phylogenetics and Evolution 69 (2013) 1159–1171 and by the low number of known morphological characters of tax- (Dumont and Negrea, 2002) where it may remain for decades until onomic significance (Longhurst, 1955). This situation led to numer- re-flooding of the habitat occurs (e.g. Straka, 2004). This necessar- ous species descriptions that referred to the morphology of ily results in highly reduced long-term gross metabolic rates and individual specimens rather than to that of diagnosible morpho- longer effective generation times in these taxa, and hence it is species (Longhurst, 1955). This rendered many descriptions useless probable that their rates of molecular evolution differ from those for practical application and made correct species identification of other arthropods that lack such prolonged dormant stages (for nearly impossible. Thus, the revision of Longhurst (1955) was an a review of factors affecting rates of molecular evolution, see important step in the taxonomy of the Notostraca, since he re- Bromham and Penny, 2003). tained only taxonomic entities that clearly could be distinguished. In the present study, we use a combined analysis of one nuclear He reduced the number of species to only nine worldwide: Triops and three mitochondrial markers to infer the molecular phylogeny cancriformis (Bosc, 1801–1802), Triops granarius (Lucas, 1864), Tri- of representative notostracan samples from all six continents that ops longicaudatus (LeConte, 1846), Triops australiensis (Spencer and are inhabited by this group of branchiopod crustaceans. We then Hall, 1896), Lepidurus apus (Linn., 1758), Lepidurus arcticus (Pallas, use non-notostracan branchiopod fossils to calibrate divergence 1793), Lepidurus lynchi Linder, 1952, Lepidurus bilobatus Packard, times among notostracan lineages based on molecular data. 1877 and Lepidurus batesoni Longhurst, 1955. Lynch (1966) rede- scribed Lepidurus lemmoni Holmes, 1894, treating L. lynchi as a syn- 2. Materials and methods onym, and redescribed Lepidurus couesii Packard, 1875 (see Lynch, 1972) which had been treated as a synonym of L. apus apus by 2.1. Taxon sampling Longhurst (1955). Based on a preceding molecular study by King and Hanner (1998) and a morphological reinvestigation, Rogers For the present study, we aimed to acquire representative sam- (2001) reinstated Lepidurus packardi Simon, 1886 (treated as a sub- ples of as many major phylogenetic lineages of Notostraca as pos- species of L. apus by Longhurst, 1955) and described a new species, sible. For the genus Lepidurus, it was unfortunately not possible to Lepidurus cryptus Rogers, 2001. In addition, a new Central Asian obtain fresh samples of L. batesoni and L. mongolicus. Both have species, Lepidurus mongolicus Vekhov, 1992 was discovered, lead- been collected only once, the former in 1911 from an unknown site ing to nine currently valid species in the genus Lepidurus. Molecu- possibly located in Kazakhstan (the species is known from only lar studies have also resulted in the reinstatement of Triops three male specimens, see Longhurst, 1955), the latter in 1975 newberryi (Packard, 1871) among American Triops and in a revision from a remote locality (Lake Ulan-Nur) in the Gobi desert (Vekhov, of T. cancriformis that led to the reinstatement of Triops mauritani- 1992). cus Ghigi, 1921 and Triops simplex Ghigi, 1921 and to the descrip- Tissue vouchers were deposited in the tissue collection of the tion of four new species, Triops baeticus Korn, 2010, Triops Museum of Zoology (Museum für Tierkunde), Senckenberg Dres- gadensis Korn and García-de-Lomas, 2010, Triops vicentinus Korn, den (Germany) under the MTD-TW numbers listed in Table 1. Se- Machado, Cristo and Cancela da Fonseca, 2010 and Triops emeriten- quences of an Australian sample (Triops australiensis) and of a sis Korn and Pérez-Bote, 2010 thus raising the number of valid spe- specimen from the Austrian commercial kit (T. cancriformis cancri- cies in the genus Triops to 11 (see Korn et al., 2006, 2010). Several formis) already available in GenBank were also included in the phy- molecular phylogenetic studies have shown the need for
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