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Rodentia: Dipodinae) from China: a Living Fossil?

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Rodentia: Dipodinae) from China: a Living Fossil? Accepted: 6 May 2017 DOI: 10.1111/jzs.12182 ORIGINAL ARTICLE A new recent genus and species of three-toed jerboas (Rodentia: Dipodinae) from China: A living fossil? Georgy Shenbrot1 | Anna Bannikova2 | Patrick Giraudoux3,4 | Jean-Pierre Quer e5 | Francis Raoul3 | Vladimir Lebedev6 1Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Abstract Research, Ben-Gurion University of the The new recent genus and species of three-toed jerboas (Rodentia: Dipodinae), from Negev, Midreshet Ben-Gurion, Israel southern Ningxia, China, is described. This form demonstrated a unique mixture of 2Lomonosov Moscow State University, Moscow, Russia external, cranial, and dental characters that individually are typical for one or 3Chrono-Environment Department, another of all known genera of Dipodinae. Based on morphological characters, it is Universite Bourgogne Franche-Comte/ CNRS, Besancßon, France recovered as the part of Dipodinae tree, distinct from all other members due to its 4Institut Universitaire de France, Paris, unique combination of morphological characters, and appears to be a nearly ideal France living ancestor of all other dipodines. In contrast to morphology, the molecular data 5INRA, UMR CBGP, Campus international de Baillarguet, Montferrier-sur-Lez Cedex, indicate a relatively young age for this lineage and consistently place it as the sister France group to Stylodipus. The results of the molecular clock analysis suggest that the sep- 6 Zoological Museum, Moscow State aration of the two lineages dates back to the Early Pliocene or the Pliocene/Mio- University, Moscow, Russia cene boundary. The estimated geographic range of the new form seems extremely Correspondence small. The conservational status of the new species remains to be determined; how- Georgy Shenbrot, Mitrani Department of Desert Ecology, Jacob Blaustein Institutes ever, the available information suggests that it requires protection. for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel. KEYWORDS Email: [email protected] China, comparative morphology, distribution modeling, molecular clock analysis, molecular Funding information phylogeny, three-toed jerboas Russian state programs, Grant/Award Number: AAAA-A16116021660077-3; Russian Science Foundation, Grant/Award Number: 14-50-00029; Russian Foundation for Basic Research, Grant/Award Number: 17-04-00065a Contributing authors: Georgy Shenbrot ([email protected]); Anna Bannikova ([email protected]); Patrick Giraudoux ([email protected]); Jean-Pierre Quer e ([email protected]); Francis Raoul ([email protected]); Vladimir Lebedev ([email protected]). 1 | INTRODUCTION Feldstein, & Meiri, 2016; Shenbrot, Sokolov, Heptner, & Koval’skaya, 1995; Zazhigin & Lopatin, 2001). Three-toed jerboas (subfamily Dipodinae) are represented by 10–11 In 2003, an international team of ecologists led by P. Giraudoux recent and 15 fossil species arranged in five contemporary and three obtained, in southern Ningxia, several specimens of three-toed jer- extinct genera distributed across the Saharo-Gobian Desert belt from boas (Dipodinae) preliminarily identified as Dipus sagitta (Pallas, the Late Miocene to present days (Lebedev et al., 2013; Shenbrot, 1773) (Giraudoux & Raoul, 2015; Raoul et al., 2008). However, 356 | © 2017 Blackwell Verlag GmbH wileyonlinelibrary.com/journal/jzs J Zool Syst Evol Res. 2017;55:356–368. SHENBROT ET AL. | 357 detailed morphological and molecular study of these specimens 2.2 | The parsimony analysis of morphological data revealed that they represent a new, previously unknown form. This form demonstrated a unique mixture of external, cranial, and dental The analysis was based on a matrix containing information on denti- characters that individually are typical for one or another of all tion, as well as external and cranial morphology. The matrix includes known genera of Dipodinae. We describe this form below. 12 OTUs representing all recent and two fossil genera of Dipodinae and three outgroup taxa belonging to the jerboa subfamilies Euchoreutinae and Allactaginae. The detailed description of character 2 | MATERIAL AND METHODS states is given in Table S1. As in Shenbrot (1992), the analysis was based on a priori assumptions about polarity, character state order- 2.1 | Morphological and morphometric analyses ing, and the irreversibility of certain transformations. A method of External measurements of Chimaerodipus were taken in the field by character weighting was employed that estimated the weight of each F. Raoul and colleagues. External measurements used for comparison individual character as inversely proportional to its minimum possible with other Dipodinae species were taken, in most cases, in the field number of steps (equal to the number of states in a character minus by G. Shenbrot. For Jaculus orientalis, these measurements were one). All reconstructions were conducted in Paup 4b10* (Swofford, taken from the original collector’s labels of the specimens deposited 2003). Starting topology was obtained via a stepwise addition with in the mammalian collections of the Smithsonian Institution, Wash- random order (10 replicates). The search for optimal trees was con- ington, DC, USA (USNM); for J. jaculus, the data published by Ben ducted using TBR branch swapping with the MULPARS option on. Faleh et al. (2010) were used. To test clade stability, a bootstrap analysis was performed with Skulls were measured with dial calipers to the nearest 0.1 mm 1000 pseudoreplicates using the same tree search options as above. according to Shenbrot (1990). Thirteen cranial measurements were For continuous traits (such as the overall size or relative size of mor- analyzed (Figure S1): condylo-basal length (Lcb), rostrum length (Lr), phological structures), character states were generated by ranking zygomatic length (Lz), mastoid breadth (Bm), zygomatic breadth (Bz), taxa according to their mean values. The index of hypsodonty was braincase breadth (Bb), interorbital breadth (Bi), rostrum breadth (Br), coded using four states: low (<0.7), intermediate (0.85–1.10), high rostrum height (Hr), height of infraorbital foramen (Hif), tympanic (1.4–1.7), and extra-high (>2.0). bulla length (Lb), tympanic bulla width (Wb), and upper tooth row length (Lmr). Only adult (reproductively mature individuals after at 2.3 | Specimens examined for genetic analysis least one winter, more than 9 months old) and subadult (adult size but reproductively not mature individuals, 4–7 months old) speci- In the molecular analysis, nine specimens of the new form were mens were included in the analyses. Age was assessed based on used, including the holotype and paratypes. Most of sequences rep- molar wear patterns, and the criteria were the same as provided by resenting other taxa of Dipodidae were retrieved from GenBank Shenbrot et al. (1995). External measurements of Chimaerodipus (Data S1). The total dataset used in the phylogenetic reconstructions were taken from specimens depositing in collection of Unite Mixte contained all currently recognized genera and species (five genera de Recherche Chrono-environnement, Universite de Bourgogne and ten species) of Dipodinae; several species belonging to Allactagi- Franche-Comte, Centre national de la recherche scientifique (UMR nae, Euchoreutinae, and Cardiocraniinae were used as outgroups. CNRS). The skulls of specimens of Jaculus jaculus, J. hirtipes and The list of specimens sequenced de novo, the collection sites, the J. orientalis used in comparison were studied in the Steinhardt museum catalogue, and the GenBank accession numbers are given in Museum of Natural History, Tel-Aviv University (TAU), the National Table S2. Natural History Collections at the Hebrew University, Jerusalem (HUJ), and USNM; those of all other species were studied in the 2.4 | DNA isolation, PCR amplification, and Zoological Museum of Moscow State University (ZM MU). The num- sequencing ber of specimens used for morphometric analysis is listed in Tables 2 and 3. Data were analyzed using a principal components analysis. A sample for genetic analysis was obtained by small ear tissue biop- The analysis was performed on non-transformed data with a correla- sies of live-trapped animals. Genomic DNA from ethanol-preserved tion matrix. tissues was extracted using a standard protocol of proteinase K In the molar description, we followed nomenclature by Shenbrot digestion, phenol–chloroform deproteinization, and isopropanol pre- (1984) adapted for Dipodinae (Figure S3). For molar comparisons of cipitation (Sambrook, Fritsch, & Maniatis, 1989). recent species, only subadults and juvenile specimens with unworn Fragments of four nuclear genes (GHR, IRBP, RAG1, and BRCA1) masticatory surfaces were selected in the ZM MU and TAU collec- were amplified and sequenced in animals using external forward/re- tions. Descriptions of the molars of fossil forms were taken from the verse primer combinations, as well as internal primers (Table S3), literature (Liu, Zhang, Cui, & Fortelius, 2008; Savinov, 1970; Topa- according to our previous studies (Lebedev et al., 2013). Cytochrome chevskiy, 1973; Zazhigin & Lopatin, 2001); the genus Jaculodipus b sequences (1140 bp) were obtained using the combination of pri- Zazhigin & Lopatin, 2001 was not included in the comparison as it is mers L_glu_jak/H_thr_jak (Table S3). The double-stranded poly- known only by the two lower molars. merase chain reaction (PCR) usually entailed 30–35 thermal cycles as 358 | SHENBROT ET
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