Accepted: 6 May 2017

DOI: 10.1111/jzs.12182

ORIGINAL ARTICLE

A new recent genus and of three-toed (Rodentia: ) from China: A living fossil?

Georgy Shenbrot1 | Anna Bannikova2 | Patrick Giraudoux3,4 | Jean-Pierre Quer e5 | Francis Raoul3 | Vladimir Lebedev6

1Mitrani Department of 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 . 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 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 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 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 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 . 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 AL. follows: 30-s denaturation at 94°C, 1-min annealing at 55–64°C, and framework as implemented in *BEAST (Heled & Drummond, 2010). 1-min extension at 72°C. PCR products were purified using the Dia- The units of the analyses correspond to species or well-supported tom DNA Clean-Up kit (Isogen). Approximately 10–40 ng of the intraspecific groups. Following the results of the molecular clock purified PCR product was used for sequencing with each primer by tests (detailed below), we used separate strict clock models for GHR the autosequencing system ABI 3100-Avant using ABI and RAG1 and uncorrelated lognormal relaxed clock models for the PRISMâBigDyeTM Terminator v. 3.1. other three loci. No calibration information was utilized, and the mean rate for GHR was set to one. We used the same partitioning scheme and models as in the ML analysis. A Yule prior for the spe- 2.5 | Phylogenetic analysis: molecular data cies tree shape and the piecewise constant population size model alignment and partitioning were assumed. Default priors were used for all other parameters. In All sequences were aligned by eye using Bioedit version 7.0.9.0 (Hall, total, we conducted three runs of 300 million generations each in 1999). Heterozygous positions (at which two peaks of approximately BEAST version 1.8.3 (Drummond, Suchard, Xie, & Rambaut, 2012). equal intensity are observed) were coded using the IUB ambiguity Parameter convergence was assessed in Tracer. After the first 10% codes. In all analyses, sequences were used as unphased genotypes. of generations were discarded as the burn-in, the maximum clade Phylogenetic reconstructions were performed with the following credibility tree was generated in TreeAnnotator version 1.8.3 (part datasets: (i) each nuclear gene separately; (ii) all nuclear genes com- of the BEAST package). Estimation of the genetic p-distances was bined; (iii) an extended sample of taxa for cytb; and (iv) nuclear and conducted in MEGA6 (Tamura, Stecher, Peterson, Filipski, & Kumar, mitochondrial cytb sequences combined in a species tree estimation. 2013). Based on previous results (Lebedev et al., 2013), the data were parti- tioned by gene and codon position (three subsets per gene). 2.7 | Divergence time estimation

Divergence times in Dipodidae were estimated based on the con- 2.6 | Phylogenetic tree reconstruction catenation of the four nuclear genes. The cytb data were not used Phylogenetic trees were generated by maximum likelihood (ML), for molecular dating because of the high level of saturation observed maximum parsimony (MP), and Bayesian inference (BI). Gene trees in intergeneric comparisons. The molecular clock assumption was for individual loci were reconstructed with ML only. tested separately for each gene using likelihood ratio tests with like- The ML analysis was performed in Treefinder (October 2008 ver- lihood values calculated in PAML 4.7 (Yang, 2007). The analysis was sion) (Jobb, 2008). The appropriate models of sequence evolution performed in BEAST version 1.8.3 (Drummond et al., 2012), assum- were selected for each partition, employing the routine implemented ing separate clock models for each gene, a Yule prior for the tree in Treefinder and using BIC as the criterion. A tree search was con- shape and optimum models (as in the ML analysis) for each partition. ducted with the following options: parameter optimization simultane- Two runs of 100 million generations were conducted. The informa- ous with tree search, optimized partition rates, proportional branch tion on the fossil dipodides that were used for node calibration is lengths for all partitions, and maximum search depth. Bootstrap sup- presented in Table S4. port (1,000 pseudoreplicates) was estimated using model parameters Prior calibration density was modeled using exponential distribu- and rate values optimized for the ML topology. tion. The minimum age of the earliest fossil representative of a clade An unweighted parsimony analysis was performed in PAUP was used as the hard lower bound for the time of its divergence 4.0b10 (Swofford, 2003) with the following options: random addition from the nearest sister group. The parameter of the exponential dis- sequence with 20 replicates, no limit for the number of optimal tribution was chosen so that the soft (95%) upper bound corre- trees, and TBR branch swapping. Clade stability was assessed based sponded to the beginning of the preceding chronological unit (MN on 1000 bootstrap replicates. zone), which contained no fossil from the clade of interest. The A Bayesian tree reconstruction was performed by MrBayes 3.1.2 choice of the type of prior and upper bound is, to a certain extent, (Ronquist & Huelsenbeck, 2003). Models with either two or six rate ambiguous; therefore, we treated the resulting estimates as prelimi- matrix parameters were selected for each partition based on the nary. results of the model selection in Treefinder. Each analysis included two independent runs of four chains (one cold plus three heated fol- 2.8 | Distribution modeling lowing the default settings). The chain length was set at 15 million generations with sampling every 1,000 generations. With these set- All records had original GPS coordinates taken in the field. Environ- tings, the effective sample size exceeded 200 for all estimated mental data for species distribution modeling (SDM) were used as parameters. Tracer 1.6 software (Rambaut & Drummond, 2005) was 30 arc-second grids (approximately 1 km resolution) and were rep- used to check for convergence and determine the necessary burn-in resented by climate, relief, and vegetation variables. The climate fraction, which was set to 1.5 million generations. variables (annual mean temperature, mean monthly temperature To estimate the species tree from data on five independent loci, range, mean temperatures of coldest and warmest quarters, maxi- including mitochondrial cytb, we employed a Bayesian coalescent mal temperature of warmest month, minimal temperature of coldest SHENBROT ET AL. | 359 month, temperature annual range, annual precipitation, and precipi- 3 | RESULTS tation of wettest quarter) were obtained from WORLDCLIM ver- sion 1.4 (Hijmans, Cameron, Parra, Jones, & Jarvis, 2005) available External and skull measurements of the new form in comparison at http://www.worldclim.org. Slope data were derived from altitude with those species occurring in the same region, Dipus sagitta and (extracted from the GOTOPO30 dataset distributed with ArcGIS) Stylodipus andrewsii, are presented in Tables 1 and 2. Photographs of using the Spatial Analyst module of ArcMap. Data on the Normal- the skulls and molars of the above species are provided in Figures 1 ized Difference Vegetation Index (NDVI) were obtained from the and 2. By skull morphology, the new form resembles Stylodipus. VEGETATION Program (http://www.spot-vegetation.com; now However, the results of the principal components analysis demon- http://www.vito-eodata.be); data for 1998–2007, each a 10-day strated that according to the skull measurements, the new form well estimate) and averaged by seasons (winter, spring, summer, and differs from the species of the genus Stylodipus (Figure 3, Table S5), autumn) across all available years. The NDVI is an index of green- as well as from all known contemporary species of Dipodinae (Fig- ness that is directly correlated with productivity and green vegeta- ure 4, Table S6). The comparison of the new form with other con- tion biomass and is widely used in ecological studies (Pettorelli temporary Dipodinae species by body and skull proportions is et al., 2005). presented in Table 3. The SDM was built with MAXENT 3.3.3k software (Phillips, Anderson, & Schapire, 2006). The extent of the study area or “land- 3.1 | Chimaerodipus auritus gen. et sp. nov scape of interest” significantly affects the SDM results (Anderson & Raza, 2010; Elith et al., 2011). To define the study area of a species, 3.1.1 | Holotype we calculated the kernel density of occurrence points of this species with a search radius equal to 4°, reclassified the obtained raster so UMR CNRS XJ0309BH03, ♀, skull, September 2003, China, Ningxia Hui that the original kernel density values equal to or more than 0.05 Autonomous Region, Xiji City, 8 km SW (35.9117°N, 105.6665°E). were converted to 1 and values less than 0.05 to “NoData,” and used this reclassified raster as the mask for clipping environmental 3.1.2 | Paratypes variables to the study area. Models were constructed with default MAXENT settings as these settings were demonstrated to be the UMR CNRS XJ0309BH01, ♀; UMR CNRS XJ0309BH02, ♂; UMR most appropriate for wide-ranging data (Phillips and Dudik 2008; CNRS XJ0309BH06, ♂—all preserved as skulls and obtained in the Warren and Seifert 2011). We used the MAXENT logistic output, same place as holotype. which provides estimates of relative habitat suitability (Elith et al., 2011). To estimate the model’s performance, we used the area under 3.1.3 | Other material the receiver-operating characteristic curve (AUC) test, the exten- sively used measure in species distribution modeling (Elith et al., UMR CNRS XJ0309CB03, ♀—preserved as skull and obtained near 2006). The AUC measures the ability of a model to discriminate the place of holotype (35.9109°N, 105.6646°E); UMR CNRS between sites in which a species is present versus those from which XJ0309AD01, ♀ (skull, 35.9280 °N, 105.6834 °E); UMR CNRS it is absent (Hanley & McNeil, 1982). The AUC values range XJ0309AF02, ♂ (skull, 35.9274°N, 105.6832°E); UMR CNRS between 0 and 1; the value of 1 means an ideally good model per- XJ0309SA14, ♂ (skull, 35.9271°N, 105.6832°E); UMR CNRS formance, the score of 0.5 indicates a predictive discrimination that is not better than random, and values less than 0.5 mean a perfor- TABLE 1 External measurements (upper row: M Æ SE; lower row: mance poorer than random. min–max) of Chimaerodipus auritus in comparison with Dipus sagitta To delineate the areas of real species occurrence, the original and Stylodipus andrewsi from Mongolia model values, ranging continuously from 0 to 1, were transformed to Chimaerodipus Stylodipus a binary 0 or 1 using a threshold value. The threshold value was Species auritus Dipus sagitta andrewsi chosen to be equal to the “maximum training sensitivity plus speci- N 95537 ficity”; it was demonstrated experimentally (Liu, White, & Newell, Body mass (g) 55.00 Æ 9.15 69.21 Æ 9.87 75.32 Æ 8.52 2013) that this threshold provides optimal results. After reclassifica- 36–68 50–95 60–95 tion of the original raster according to the chosen threshold value, Head and body 112.33 Æ 6.26 123.95 Æ 6.14 125.44 Æ 4.26 the reclassified raster was transformed to polygons. Only polygons length (mm) 98–118 112–142 120–135 containing occurrence records were considered as areas of occur- Tail length (mm) 166.56 Æ 14.61 158.39 Æ 7.97 150.01 Æ 6.08 rence. The areas of these polygons were calculated on the map and 137–184 140–177 140–165 converted to the Asia North Albers Equal Area Conic projection Ear length (mm) 30.33 Æ 1.22 19.79 Æ 2.10 17.24 Æ 0.62 using the command “calculate geometry” in sq. km, and the sum of 28–32 17–24 16–19 the areas of these polygons was used as an estimation of geographic Hindfoot 51.89 Æ 1.54 59.63 Æ 2.50 53.12 Æ 1.83 range size. All map operations were performed using ArcMap 10.3 length (mm) 48–53 54–66 50–58 software. 360 | SHENBROT ET AL.

TABLE 2 Skull measurements (mm; upper row: M Æ SE; lower is narrow, with weakly straddling zygomatic arches shifted down rel- row: min–max) of Chimaerodipus auritus in comparison with Dipus ative to the plane of masticatory surface of the upper molars, weakly sagitta and Stylodipus andrewsi from Mongolia inflated auditory bullae, and a long hard palate. The upper incisors Chimaerodipus with non-colored (white) enamel layer. The upper premolar is con- Variables auritus Dipus sagitta Stylodipus andrewsi stantly present. The upper molars have anterior and posterior cin- N 8 173 28 gula. The anteroconulid on the first lower molar is present as an Lcb 28.57 Æ 1.14 30.33 Æ 0.75 30.18 Æ 0.67 independent tubercle; the anteroconulid on the second lower molar 27.3–29.9 28.5–32.1 28.9–31.8 is overdeveloped, comparable in size to the main tubercles. Lr 10.26 Æ 0.57 10.98 Æ 0.36 10.80 Æ 0.31 – – – 9.1 10.8 10.1 11.9 10.1 11.5 3.1.6 | Description and comparison Lz 13.07 Æ 0.56 14.63 Æ 0.46 13.79 Æ 0.45 11.9–13.8 13.6–16.1 12.9–14.6 The body size (mean body mass equals 55 g, mean body and head length is 114 mm; see Tables 1 and 2) is larger than in Eremodipus Bm 17.17 Æ 0.46 20.22 Æ 0.48 21.26 Æ 0.51 but smaller than in other three-toed jerboas. The muzzle is relatively 16.4–17.6 19.2–21.7 20.2–22.1 elongated with a poorly developed snout. The ears are long: Ear Bz 18.74 Æ 0.50 21.65 Æ 0.66 21.62 Æ 0.56 bent forward completely covers the eye and ends in the middle of 17.9–19.2 19.4–23.6 20.3–22.4 the distance between the front edge of the eye and the tip of the Bb 16.03 Æ 0.71 17.87 Æ 0.43 18.10 Æ 0.39 nose. The mean length of the ear equals 27% of the head and body 15.1–16.9 16.8–19.2 17.3–19.0 length, which is considerably greater than in all other three-toed jer- Æ Æ Æ Bi 7.26 0.35 9.99 0.37 9.56 0.36 boas. The fur color on the head and back is dark ocherous-brown, – – – 7.0 7.8 8.8 11.2 9.0 10.4 with a sharp dark longitudinal spray. The underside of the body and Br 4.70 Æ 0.17 5.15 Æ 0.25 6.42 Æ 0.14 the front and lateral surfaces of the feet are pure white. The tail is 4.4–4.9 4.7–5.8 6.2–6.7 relatively long (148% of the head and body length, which is slightly Hr 5.94 Æ 0.23 6.77 Æ 0.28 6.04 Æ 0.26 shorter than in Jaculus jaculus, J. hirtipes, and J. orientalis, but longer 5.6–6.2 6.2–7.8 5.5–6.5 than in all other three-toed jerboas) and not thickened, with a dark Hif 5.48 Æ 0.31 6.54 Æ 0.33 5.75 Æ 0.30 longitudinal strip on the dorsal surface and a terminal tuft forming a 4.8–5.9 5.7–7.6 5.1–6.3 relatively poorly developed, narrow and weakly flattened banner. Lb 9.90 Æ 0.25 11.26 Æ 0.28 13.63 Æ 0.36 The dark longitudinal strip on the dorsal surface of the tail is narrow and does not extend down on the lateral surface. The white terminal 9.5–10.3 10.5–12.1 12.7–14.5 part of the banner is relatively small, two times shorter than its Wb 8.47 Æ 0.41 8.88 Æ 0.28 9.88 Æ 0.23 brownish-black basal band. The brownish-black band on the ventral 7.8–8.9 8.2–9.7 9.5–10.5 side of the tail banner is incomplete, being divided by the wide Lmr 5.92 Æ 0.22 5.74 Æ 0.21 5.44 Æ 0.13 white stripe along the tail rod. By the banner morphology, Chi- 5.6–6.3 5.1–6.2 5.1–5.8 maerodipus is similar to Eremodipus, but differs from Stylodipus (ban- Lcb, condylo-basal length; Lr, rostrum length; Lz, zygomatic length; Bm, ner is absent) and Dipus, Jaculus, and Paradipus (banners are better mastoid breadth; Bz, zygomatic breadth; Bb, braincase breadth; Bi, developed). The hindlimbs are three-toed; the third (middle) toe is interorbital breadth; Br, rostrum breadth; Hr, rostrum height; Hif, height appreciably longer than the lateral ones (second and fourth), the of infraorbital foramen; Lb, tympanic bulla length; Wb, tympanic bulla width; Lmr, upper tooth row length hindfoot brush is black and consists of monotypic, soft, relatively short hairs, deflected forward. Subdigital skin pads are well devel- XJ0309AA02, ♀ (whole body preserved in alcohol, 35.9285°N, oped and distinctly divided into three to four lobes. The conic callus 105.6823°E)—captured approximately 6 km SW of Xiji City. at the base of the toes is well developed; its height and diameter at the base are ~1.5 mm and ~2.2 mm, respectively. Toe claws are straight and acute; the claws of the outer and inner toes are equal in 3.1.4 | Etymology length and distinctly (1.5–2 times) larger than the claw of the middle Genus name Chimaerodipus, from the Greek Chimera (due to an unu- toe. By the relative size of the middle and lateral toes and the pres- sual combination of traits typical of various jerboa lineages) and the ence of the conic callus, Chimaerodipus is similar to Stylodipus, but generic name Dipus; species name auritus, meaning “eared” in Latin. resembles Dipus and Jaculus in toe-claw morphology. The skull is narrow, with a relatively long rostrum; the relative skull width (measured as the ratio of the braincase or zygomatic 3.1.5 | Diagnosis width to the condylo-basal length) is slightly higher than in Paradipus, Small three-toed jerboa with long ears and long tail with a poorly but lower than in other Dipodinae. The nasal bones are relatively expressed black and white terminal banner. The footpads have a short and do not reach forward to the level of the anterior margin short black brush and conic callus at the base of the toes. The skull of the intermaxillary bones (as in most Dipodinae with the exception SHENBROT ET AL. | 361

(a) (b) (c)

FIGURE 1 Skulls of Dipus sagitta (a— ZM MU S-194011 from Mongolia), Chimaerodipus auritus (b—holotype), and Stylodipus andrewsi (c—ZM MU S-194136 from Mongolia). First row: ventral view; second row: dorsal view; third row: lateral view; fourth row: labial view of mandible

of Paradipus). The infraorbital canal is completely closed; however, Dipus); its width twice exceeds its length (as in Stylodipus). The upper its outer wall is only in contact with the body of the maxilla, but is transverse processes of the occipital bone superimposed on the not fused with it (as in most Dipodinae with the exception of Jacu- auditory bullae are short and triangular (as in Dipus, Eremodipus, and lus). The lower zygomatic process of the maxilla is relatively low: Its Paradipus). The fenestrae postglenoideae are extremely small (smaller height-to-width ratio is below 1.5, which is higher than in Paradipus, than in all other Dipodinae), narrowed, and stretched in a longitudi- but lower than in other Dipodinae. The squamosal zygomatic process nal direction; they are not covered from the inside by the outer wall is distinctly bent downwards at 40–45° from the horizontal plane of of the mastoid section of the auditory bullae, thus forming a fissure skull, which is slightly lower than in Paradipus, but higher than in in the cranium (as in Dipus). The auditory bullae are weakly inflated other Dipodinae. The horizontal arm of the zygomatic arch is shifted (less than in other Dipodinae); in the dorsal view, they are not visible ventrally, projecting below the level of the upper molar row (as in (in other Dipodinae, they project from under the braincase laterally Eremodipus). The lacrimal bones are small, triangular, and not shifted and/or caudally). The mastoid cavity is small and simple, without externally (similar to Eremodipus). The lateral surface of the parietal internal ribs or septa (as in Dipus). In volume, the mastoid cavity is bone has no crests (as in Dipus). The interparietal bone is large, close approximately three times smaller than the tympanic one. The bony to triangular in shape with rounded lateral and caudal angles (as in palate is long, with the posterior margin terminating as a long, 362 | SHENBROT ET AL.

(a) (b) (c)

FIGURE 2 Molars of Dipus sagitta (a— ZM MU S-192277 from Mongolia), Chimaerodipus auritus (b—XJ0309AF02), and Stylodipus andrewsi (c—ZM MU S- 171250 from Mongolia). First row: upper molars; second row: lower molars backwardly directed median spine; the distance between the poste- rior margin of the hard palate and the posterior margin of the last 3 molar is nearly equal to the length of the tooth row (as in Jaculus jaculus and J. hirtipes). The palatine foramina are medium-sized, oval, 2 and stretched in a longitudinal direction (as in Dipus). The ascending 1 ramus of the mandible is broad and low (as in Stylodipus), entirely lacking foramina (all other Dipodinae, with the exception of a few 0 specimens of Stylodipus, have a foramen at the base of the condylar process). The angular process of the mandible has one large foramen FACTOR2 –1 (as in most Dipodinae with the exception of Jaculus); the inflection of the ventral and caudal angles (medially and laterally, respectively) –2 is expressed less than in other Dipodinae. The upper incisors are moderately thick with a well-developed –3 longitudinal groove; enamel on their front surface is white (as in most –4 –3 –2 –1 0 1 2 Dipodinae with the exception of Dipus; in the last one, the enamel of FACTOR1 the upper incisors is yellow). The upper premolar is constantly present FIGURE 3 Distribution of the studied specimens of the species (as in Dipus and Stylodipus andrewsii) but small. The molar crowns are of Chimaerodipus and Stylodipus genera in the morphospace of the of medium height, with terraced masticatory surfaces at the early first two principal components; black circles: Chimaerodipus auritus; stages of wear. On unworn molars, the height of the crown (measured black squares: Stylodipus andrewsi; black diamonds: Stylodipus for M2) is 105-110% of its length, which is higher than in Dipus, sungorus; and black triangles: Stylodipus telum SHENBROT ET AL. | 363

Scirtodipus, and fossil species of Stylodipus, but lower than in other well expressed; they are shifted backward relative to the hypocone Dipodinae. Molar row is relatively long (Lmr composes approximately and metacone, forming a cingulum posterior. The cingula posterior in 21% of Lcb), which is similar to Paradipus, slightly more than in Dipus Chimaerodipus are developed to a similar extent as in Eremodipus,less (with some marginal overlap), and significantly greater (without over- than in Plioscirtopoda, but more than in Scirtodipus;inDipus, Stylodipus, lap) than in other Dipodinae, including all species of Stylodipus. Jaculus, Eremodipus, and Paradipus, cingula anterior are absent. The The paired outer and inner main tubercles of the upper molars longitudinal crest connects the hypocone with the paracone; it is ori- (protocone–paracone and hypocone–metacone) are strongly opposite ented at an angle of 30° to the longitudinal axis of the tooth (as in (as in most Dipodidae with the exception of Dipus, Scirtodipus,and most Dipodinae with the exception of Eremodipus and Paradipus). In some specimens of Plioscirtopoda). Anteroconules are present on all most specimens of Chimaerodipus, there is a small spur at the labial three upper molars; they are shifted forward relative to the protocone side of the longitudinal crest in M1, representing the rudimental and paracone and are connected to the protocone by the antero- mesostyle. Such a rudimental mesostyle is also present only in Scir- lophe, forming a cingulum anterior. The cingula anterior in Chimaerodi- todipus and some specimens of fossil Dipus, but is absent in all other pus are developed to a similar extent as in Dipus and fossil species of Dipodinae. The upper molars of Chimaerodipus have three entrant Stylodipus, less than in Plioscirtopoda and Scirtodipus, but more than in folds (paraflexus, metaflexus, and posteroflexus) on the labial side and recent species of Stylodipus;inJaculus, Eremodipus and Paradipus,cin- one (hypoflexus) on the lingual side. The anterior labial entrant folds gula anterior are absent. Posterostyles on all three upper molars are (paraflexuses) are relatively large and straight on the first and second upper molars and small on the third. The central labial (metaflexuses) 2.0 and the lingual (hypoflexuses) entrant folds are straight, large, and

1.5 wide; on the first and second molars, they are wider than the main tubercles. The posterior labial entrant fold (posteroflexus) is small and 1.0 shallow; it is well expressed only on the first upper molars. In the 0.5 number and relative size of the entrant folds of the upper molars, Chi- 0.0 maerodipus is similar to Plioscirtopoda, but differs from other Dipodi- nae. The relative size of the entrant folds on the upper molars in –0.5 Chimerodipus auritus Dipus sagitta

FACTOR2 Chimaerodipus is appreciably larger than in other Dipodinae. Moreover, –1.0 Stylodipus andrewsii Stylodipus sungorus the total number of folds in Chimaerodipus is different from those in Stylodipus telum –1.5 Jaculus blanfordi other three-toed jerboas (except Plioscirtopoda). Jaculus hirtipes Jaculus jaculus –2.0 Jaculus orientalis On the first two lower molars, the internal main tubercles are dis- Eremodipus lichtensteini tinctly shifted forward relative to the external ones (the metaconid rela- –2.5 Paradipus ctenodactylus –3.0 –2.5 –2.0 –1.5 –1.0 –0.5 0.0 0.5 1.0 1.5 2.0 2.5 tive to the protoconid and the entoconid relative to the hypoconid), as FACTOR1 in most Dipodinae with the exception of Eremodipus. The anteroconulid is present on the first lower molar as a small tubercle, independent of or FIGURE 4 Distribution of specimens of all known contemporary species of three-toed jerboa (subfamily Dipodinae) in the partially fused with the metaconid but clearly visible as a small antero- morphospace of the first two principal components labial protuberance of the metaconid, as in some fossil species of

TABLE 3 Comparison of Chimaerodipus auritus with other contemporary Dipodinae species by body and skull proportions

Chimaerodipus Paradipus Dipus Stylodipus Jaculus J. J. J. Eremodipus auritus ctenodactylus sagitta andrewsi S. sungorus S. telum blanfordi hirtipes jaculus orientalis lichtensteini N 9 30 232 37 7 114 28 9 26 47 66 Tail length/ 1.48 1.31 1.25 1.20 1.25 1.26 1.40 1.54 1.57 1.52 1.38 HBL Ear length/ 0.27 0.23 0.15 0.14 0.15 0.15 0.18 0.20 0.16 0.23 0.15 HBL Planta length/ 0.46 0.52 0.49 0.42 0.44 0.44 0.48 0.52 0.52 0.52 0.49 HBL N 8 42 882 3,728 22 316 100 32 24 82 108 Bm/Lcb 0.60 0.65 0.67 0.70 0.68 0.67 0.73 0.78 0.77 0.71 0.80 Bz/Lcb 0.66 0.63 0.72 0.72 0.72 0.72 0.74 0.72 0.74 0.75 0.68 Bb/Lcb 0.56 0.54 0.59 0.60 0.58 0.59 0.64 0.66 0.65 0.65 0.62 Lb/Lcb 0.35 0.40 0.38 0.45 0.43 0.41 0.47 0.51 0.50 0.45 0.53 Lmr/Lcb 0.21 0.20 0.19 0.16 0.17 0.16 0.17 0.17 0.17 0.19 0.18

HBL, head and body length; Lcb, condylo-basal length; Bz, zygomatic breadth; Bb, braincase breadth; Lb, tympanic bulla length; Lmr, molar row length 364 | SHENBROT ET AL.

FIGURE 5 Recorded distribution points of Chimaerodipus auritus (a) and its predicted distribution by MAXENT modeling with a logistic threshold value equal to 0.585

Stylodipus. The size of the anteroconulid on M1 in Chimaerodipus is simi- lar to that in Plioscirtopoda (but in the latter, the anteroconulid is always fused with the metaconid) and smaller than in Scirtodipus and Paradipus; in other Dipodinae, this cusp is either completely absent or very small and present in only a few (less than 10%) individuals. The posterostylid is well developed on all three lower molars; it is connected to the hypo- conid and displaced backward from the entoconid, forming a distinct cingulum posterior as in most Dipodinae (with the exception of Paradi- pus and the M2-M3 of Plioscirtopoda, in which the posterostylid is com- pletely fused with the hypoconid and does not form a cingulum posterior). On the second lower molar, the anteroconulid is overdevel- oped, being comparable in size to the main tubercles (as in Jaculus and

Paradipus; in other Dipodinae, the anteroconulid on M2 is significantly smaller). Among the additional elements on lower molars, ectoconulids are usually present; the longitudinal labial crests (ectolophids) are mod- erately developed. On the first lower molar, there are two lingual (ento- flexid and posteroflexid), one anterior (protoflexid) and one labial FIGURE 6 The most parsimonious tree inferred from the

(hypoflexid) entrant folds. On the M2, there are two lingual (entoflexid morphological data. The numbers above the branches correspond to and posteroflexid) and two labial (protoflexid and hypoflexid) entrant bootstrap support values folds. On the third lower molar, there are one lingual (entoflexid) and one labial (hypoflexid) entrant fold. The presence of the former sepa- at 1 km south of PingFeng (35.7°N, 105.6°E, 30 km SW of Xiji City), rates Chimaerodipus (and Dipus)fromStylodipus.Alltheentrantfoldsare Xiji County, Ningxia, at an altitude of about 2000 m.a.s.l. Three indi- straight; the posteroflexid on M2 and the entoflexid on M3 are short viduals were trapped in ploughed potato fields in the valley bottom and narrow; the other folds are relatively long and wide. The number near the village, five in recently afforested set-aside fields with rela- – and relative size of the entrant folds of M1 in Chimaerodipus are the tively dense but low (50 60 cm) herbaceous cover composed of same as in most Dipodinae except Paradipus.OnM2, the number and Saussurea fastuosa, Saussurea cf. uniflora, Indigofera heterautha, and relative size of the lingual entrant folds in Chimaerodipus are as in Dipus, Setaria cf. violacea (Figure S4), and one was brought in by people, and Plioscirtopoda, Scirtodipus,andStylodipus, whereas those of the labial thus could not be attributed to a specific habitat. During the time of folds are as in Scirtodipus and Jaculus. trapping (September 2003), all individuals were in non-breeding condi- tions. Other species of small trapped with Chimaerodipus 3.1.7 | Ecological and geographic distribution were Tscherkia triton, Cricetulus longicaudatus, Mus musculus, Rattus tanezumi, Spermophilus sp. (alashanicus or dauricus), and Ochotona dau- Eight of the available individuals, including the holotype, were urica. The obtained SDM (Figure 5, Table S7) demonstrated that suit- trapped on the loess plateau between the GaoTong (35.9°N, able habitats for Chimaerodipus (defined by a minimum training 105.7°E) and ZhaoNao (35.9°N, 105.6°E) villages at 0-150 m from presence, an equal training sensitivity and specificity, and a maximum the main road (6–8 km SW of Xiji City) and one (no. XJ0309SA14) training sensitivity plus specificity criteria with a logistic threshold SHENBROT ET AL. | 365

(a) 1.0/100 /100 (?)Paralactaga elater 0.8 0.1 major 56 92 61 89 Orientallactaga sibirica 1.0/100 /100 Euchoreutes naso AA02 0.5 77 BH03 60 BH06 Chimaerodipus auritus 1.0/100 /100 AF02 } BH02 1.0/100 /100 1.0/55/- SA14 1.0/100 /100 Stylodipus andrewsi Stylodipus sungorus 1.0/99/97 1.0/97/100 Stylodipus telum Eremodipus lichtensteini 1.0/100 /100 0.9/72/54 Jaculua blanfordi Jaculua hirtipes 1.0/84/78 1.0/100 /100 Jaculua jaculus 1.0/100 /100 Jaculua orientalis 1.0/100 /100 Ds1 Ds2}Dipus sagitta 1.0/100 /100 0.9/71/100 Ds3 Paradipus ctenodactylus Cardiocranius paradoxus 1.0/100 /100 Salpingotus crassicauda 0.01 Salpingotus kozlovi

(b) Cardiocranius paradoxus 1 1 Salpingotus kozlovi Salpingotus crassicauda Euchoreutes naso FIGURE 7 (a) The maximum-likelihood 1 Orientallactaga sibirica tree depicting the relationships between 1 Allactaga major (?)Paralactaga elater the examined representatives of 1 Dipodidae. The numbers above and below Chimaerodipus auritus 1 the branches correspond to bootstrap 0.99 Stylodipus telum 1 Stylodipus sungorus support and posterior clade probabilities 0.99 Stylodipus andrewsi (MrBayes), respectively. Both ML and BI 0.63 Eremodipus lichtensteini analyses were performed based on the 0.99 Jaculus blanfordi concatenation of four nuclear genes. (b) 0.88 1 Jaculus hirtipes 0.96 The species tree determined by *BEAST 1 Jaculus jaculus based on alignments of four nuclear genes Jaculus orientalis_A 1 A and one mitochondrial gene. The numbers 1 Dipus sagitta_ Dipus sagitta_B above the branches correspond to 0.003 posterior clade probabilities Paradipus ctenodactylus

TABLE 4 Times of most common ancestors (TMRCA) for value equal to 0.585 in all three cases) are distributed mainly in south- Dipodidae as determined by BEAST using an uncorrelated relaxed ern Ningxia and adjacent parts of Gansu. The total estimated area of clock model based on the concatenation of four nuclear genes suitable habitats was 1509 sq. km; if isolated patches with areas less TMRCA Mean (Mya) 95% HPD Interval than 5 sq. km were removed, the estimation of the area of suitable Dipodidae 20.42 18.06–23.05 habitats decreased to 1060 sq. km; the area of the polygon with real – observation records was 408 sq. km. Allactaginae including stem 16.46 16 17.32 Cardiocraniinae 12.59 10.14–15.15 Chimaerodipus + Stylodipus 4.85 3.84–5.9 3.1.8 | The results of the parsimony analysis of Dipus including stem 8.44 8.2–8.89 morphological data Eremodipus + Jaculus 4.73 3.75–5.74 In the parsimony tree based on the morphological characters (Figure 6), Euchoreutinae including stem 16.47 16–17.34 the Chimaerodipus lineage is placed as the sister group to all other Dipo- Stylodipus 2.23 1.39–3.09 dinae; however, this arrangement is not supported by bootstrap values Stylodipus + Chimaerodipus 6.83 5.98–7.74 (<50%). Other dipodines are grouped into two clades: Paradipus + Ere- clade including stem modipus + Jaculus and Dipus + Stylodipus + Scirtodipus + Plioscirtopoda. Jaculus 1.73 1.18–2.31 Dipodinae 10.52 9.46–11.74 3.1.9 | Molecular results (Figure S5a-e). Three nuclear genes (BRCA1, RAG1, and IRBP) place The phylogenetic position of Chimaerodipus based on the molecular Chimaerodipus as a sister group of the monophyletic Stylodipus with data showed little variation between individual gene trees support for this association ranging from high to low. In the GHR 366 | SHENBROT ET AL. tree, Chimaerodipus is part of the unresolved polytomy along with 4 | DISCUSSION the species of Stylodipus and the Jaculus + Eremodipus clade. In the cytb tree (Figure S5e), Chimaerodipus and Stylodipus form a well-sup- There are numerous cases of newly revealed mammalian species that ported monophyletic group; yet, the relationships between other were detected primarily based on genetic data (e.g., Ben Faleh et al. genera of Dipodinae are poorly resolved. Estimates of genetic diver- 2012; Pages et al. 2010). In contrast to these, Chimaerodipus repre- gence (cytb gene, p-distance) over sequence pairs between groups sents a rare event of discovery of a new non-tropical taxon, which is are provided in Table S8. highly divergent from its sister taxa in external and cranial morphol- The ML, MP, and Bayesian analyses of nuclear concatenation ogy and genetic (divergence time is about 5 Mya). By skull morphol- recovered nearly identical topologies; thus, only the ML tree is ogy, Chimaerodipus resembles Stylodipus with less inflated auditory shown (Figure 7a). The tree pattern is fully concordant with previ- bullae, but deeply differ from it by external characters. The level of ously published phylogenetic results (Lebedev et al., 2013; Pisano genetic divergence between Chimaerodipus and Stylodipus is similar et al., 2015). The Chimaerodipus + Stylodipus clade receives maximum to that among other genera of Dipodinae. Thus, we can definitely support in all analyses. The species tree determined by BEAST sup- consider Chimaerodipus as the separate genus. ports the same relationships between dipodines (Figure 7b). Paradoxically, Chimaerodipus appears to be a nearly ideal living The obtained estimates of divergence time are presented in ancestor of all other dipodines from the morphological standpoint. If Table 4 (see also the chronogram in Figure 8). According to the this is true, it can be considered as the Lazarus taxon, which, by def- results, the split between Chimaerodipus and Stylodipus dates back to inition, is the taxon that temporarily disappeared from the fossil the Early Pliocene–Late Miocene (mean = 4.8 Mya, 95% HPD inter- records before reappearing unchanged (Wingall & Benton, 1999). val = 3.8–5.9 Mya), whereas the separation of the Chimaerodi- Based on morphological characters, Chimaerodipus is recovered as pus + Stylodipus clade occurred 6.0–7.7 Mya. the part of Dipodinae tree, distinct from all other members due to its

Paradipus ctenodactylus Jaculus orientalis Jaculus jaculus Jaculus hirtipes Jaculus blanfordi Eremodipus lichtensteini Stylodipus telum Stylodipus sungorus Stylodipus andrewsi A02A A02F B02H Chimaerodipus auritus B06H B03H S14A

Ds2 Ds3 Dipus sagitta Ds1 Orientallactaga sibirica Allactaga major Paralactaga elater Euchoreutes naso Cardiocranius paradoxus Salpingotus kozlovi 3.0 Salpingotus crassicauda

Mya 232 22 21 20 19 18 17 16 15 14 13 12 11 10 9 8 7 6 5 4 3 2 1 0 Miocene Pliocene Early Middle Late Early Late Q

FIGURE 8 The chronogram for Dipodidae as determined in BEAST based on a nuclear concatenation. The node bars show 95% HPD intervals for node ages SHENBROT ET AL. | 367 unique combination of morphological characters. This result highlights distribution. Nevertheless, the absence of specimens of this species the fact that most of the character states that Chimaerodipus shares in the main world collections indicates its very narrow and with other Dipodinae genera can be considered as plesiomorphic. probably relict patterns of geographic distribution. We found that Moreover, in its general body appearance and in the dorsal skull view, the species was locally abundant. It is probably well known to local Chimaerodipus resembles a small five-toed jerboa (such as Paralactaga people. Anecdotally, a picture of this species was published in a elater, subfamily Allactaginae) rather than a three-toed jerboa. book reviewing the vertebrates of Ningxia (Wang, 1990) under the In contrast to morphology, molecular data indicate a relatively name “Stylodipus telum” (together with a drawing of the skull of the young age for its lineage and consistently place Chimaerodipus as the true S. telum with a description clearly related to S. andrewsi). The sister group to Stylodipus. The inclusion of Chimaerodipus does not conservational status of the new species remains to be determined; change the backbone of the well-supported Dipodinae tree produced however, the available information suggests that it requires in a previous analysis (Lebedev et al., 2013), which placed Paradipus protection. as sister to other dipodines and identified Dipus as the sister group to the clade including Stylodipus and Eremodipus + Jaculus. It should ACKNOWLEDGEMENTS be mentioned that two specimens from our sample of Chimaerodipus, incorrectly identified as Dipus sagitta, were examined in another We thank Wang Junli, Kenichi Takahashi, Dominique Rieffel, and Nadine Bernard for their help in the field and Samara Bel for her molecular study (Pisano et al., 2015), which yielded a phylogeny con- cordant with the one presented here. help in English editing. Molecular phylogenetic studies were sup- ported by the Russian Foundation for Basic Research, Project 17-04- The observed discrepancy between our molecular and morphologi- cal results can be explained by the retention of primitive morphological 00065a (experimental work), the Russian Science Foundation, Project 14-50-00029 (phylogenetic analysis), and state programs AAAA- traits in Chimaerodipus, on the one hand, and numerous parallelisms in A16116021660077-3. This is publication no. 937 of the Mitrani more advanced dipodines, on the other. Thus, the status of Chimaerodi- Department of Desert Ecology. pus as a dipodine ancestor (i.e., assuming no reversals in its branch) would imply the parallel acquisition of most apomorphies (such as enlarged multichambered bulla, simplified molar crown pattern) by all ORCID other recent genera of three-toed jerboas. The importance of paral- lelisms in jerboa evolution is also illustrated by other results of our mor- Georgy Shenbrot http://orcid.org/0000-0002-5075-7349 phological reconstructions, which, in agreement with some of the Patrick Giraudoux http://orcid.org/0000-0003-2376-0136 previous analyses (Lebedev et al., 2013), placed Paradipus in a clade with Jaculus and Eremodipus. This grouping is most likely an artifact of REFERENCES the high specialization of these three taxa to arid environments and, in particular, to sand dwelling and herbivory, which are characteristic of Anderson, R. P., & Raza, A. (2010). The effect of the extent of the study Paradipus and Eremodipus. Conflicts between phylogenetic trees region on GIS models of species geographic distributions and estimates derived from morphological and molecular characters are common and of niche evolution: preliminary tests with montane (genus Nephelomys) in Venezuela. Journal of Biogeography, 37, 1378–1393. are typically associated with the discordant position of taxa with high Ben Faleh, A., Cosson, J. F., Tatard, C., Ben Othmen, A., Said, K., & Gran- adaptive specializations (Potapova, 2014, 2015; Potapova & Rossolimo, jon, L. (2010). Are there two cryptic species of the lesser jerboa Jacu- 2008). Thus, given the apparent difficulties in morphology-based phylo- lus jaculus (Rodentia: Dipodidae) in Tunisia? Evidence from molecular, genetic reconstructions, we can conclude that although Chimaerodipus morphometric, and cytogenetic data. Biological Journal of the Linnean Society, 99, 673–686. is very similar to the common ancestor of Dipodinae, it can hardly be Ben Faleh, A., Granjon, L., Tatard, C., Ski, Z. B., Cosson, J. F., & Said, K. treated as such, and its status as a Lazarus taxon has no unequivocal (2012). Phylogeography of two cryptic species of African desert jer- support. boas (Dipodidae: Jaculus). Biological Journal of the Linnean Society, The level of genetic divergence between Chimaerodipus and Sty- 107,27–38. Cerling, T. E., Harris, J. M., MacFadden, B. J., Leakey, M. G., Quade, J., lodipus roughly corresponds to that between the genera Jaculus and Eisenmann, V., & Ehleringer, J. R. (1997). Global vegetation change Eremodipus. The results of the molecular clock analysis suggest that through the Miocene/Pliocene boundary. Nature, 389, 153–158. separation of the Chimaerodipus lineage, as well as the Jaculus/Ere- Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian modipus split, dates back to the Early Pliocene or the Pliocene/Mio- phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973. cene boundary. This time is characterized by rapid landscape Elith, J., Graham, C. H., Anderson, R. P., Dudık, M., Ferrier, S., Guisan, A., changes across Eurasia, in particular by increasing of aridization at ... Zimmermann, N. E. (2006). Novel methods improve prediction of the end of Miocene (Cerling et al., 1997; Velichko & Nechaev, species’ distributions from occurrence data. Ecography, 29, 129–151. 2005). The exact nature of the palaeo-events that led to the split of Elith, J., Phillips, S. J., Hastie, T., Dudık, M., Chee, Y. E., & Yates, C. J. the Chimaerodipus and Stylodipus branches remains unclear. (2011). A statistical explanation of MaxEnt for ecologists. Diversity and Distributions, 17,43–57. The estimated geographic range of Chimaerodipus auritus seems Giraudoux, P., & Raoul, F. (2015). MicromAsia: small mammal surveys in extremely small. Certainly, the SDM based on a few occurrence Western China and Kyrgyztan. Chrono-environment. http://dataosu. points from a small area can underestimate the extent of obs-besancon.fr/FR-18008901306731-2015-08-06-20 368 | SHENBROT ET AL.

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment Shenbrot, G. I. (1984). Dental morphology and phylogeny of five-toed editor and analysis program for Windows 95/98/NT. Nucleic Acids jerboas of the subfamily Allactaginae. Archives of Zoological Museum Symposium Series, 41,95–98. of Moscow State University, 22,61–92 [in Russian]. Hanley, J. A., & McNeil, B. J. (1982). The meaning and use of the area Shenbrot, G. I. (1990). Geographical variation of the Turkmenian jerboa, under a Receiver Operating Characteristic (ROC) curve. Radiology, Jaculus turcmenicus (Rodentia, Dipodidae), and problems of its protec- 143,29–36. tion. Zoologicheskyi Zhournal (USSR), 69, 114–121 [in Russian, English Heled, J., & Drummond, A. J. (2010). Bayesian inference of species trees summary]. from multilocus data. Molecular Biology and Evolution, 27, 570–580. Shenbrot, G. I. (1992). Cladistic approach to the analysis of phylogenetic Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. relationships among dipodoid rodents (Rodentia, Dipodoidea). (2005). Very high resolution interpolated climate surfaces for global Archives of Zoological Museum of Moscow State University, 29, 176– land areas. International Journal of Climatology, 25, 1965–1978. 201. [in Russian]. Jobb, G.. (2008). TREEFINDER version of October 2008. [Computer soft- Shenbrot, G., Feldstein, T., & Meiri, S. (2016). Are cryptic species of the ware and manual]. Munich, Germany. , Jaculus jaculus (Rodentia, Dipodidae), really Lebedev, V., Bannikova, A., Pages, M., Pisano, J., Michaux, J., & Shenbrot, cryptic? Re-evaluation of their taxonomic status with new data from G. (2013). A molecular phylogeny of Dipodoidea based on four nuclear Israel and Sinai. Journal of Zoological Systematics and Evolutionary genes versus morphological . Zoologica Scrripta, 42, 231–249. Research, 54, 148–159. Liu, C., White, M., & Newell, G. (2013). Selecting thresholds for the pre- Shenbrot, G. I., Sokolov, V. E., Heptner, V. G., & Koval’skaya, Y. U. M. diction of species occurrence with presence-only data. Journal of Bio- (1995). Mammals of the Fauna of Russia and contiguous countries. geography, 40, 778–789. Dipodoid Rodents. Moscow: Nauka Press [in Russian]; English transla- Liu, L.-P., Zhang, Z.-C., Cui, N., & Fortelius, M. (2008). The Dipodidae (jer- tion (2008). Jerboas. Mammals of Russia and Adjacent Regions. Sci- boas) from loc. 30 of Baode and their environmental significance. entific editors: RS Hoffmann, DE Wilson. Enfield, New Hampshire: Vertebrata Palasiatica, 46, 124–132. Science Publishers. Pages, M., Chaval, Y., Herbreteau, V., Waengsothorn, S., Cosson, J.-F., Swofford, D. L. (2003). PAUP – phylogenetic analysis using parsimony. Ver. Hugot, J.-P., ... Michaux, J. (2010). Revisiting the taxonomy of the 4b. 10. [Computer software and manual]. Champaign, Illinois: Illinois Rattini tribe: A phylogeny-based delimitation of species boundaries. Natural History Survey. BMC Evolutionary Biology, 10,1–27. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). Pettorelli, N., Vik, J. O., Mysterud, A., Gaillard, J. M., Tucker, C. J., & MEGA6: molecular evolutionary genetics analysis version 6.0. Molecu- Stenseth, N. C. (2005). Using the satellite-derived NDVI to assess lar Biology and Evolution, 30, 2725–2729. ecological responses to environmental change. Trends in Ecology & Topachevskiy, V. A. (1973). Rodents of the Tamanian faunistic complex of Evolution, 20, 503–510. Krym. Kiev: Naukova Dumka Press. Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy Velichko, A. A., & Nechaev, V. P. (Eds.) (2005). Cenozoic climatic and modeling of species geographic distributions. Ecological Modelling, environmental changes in Russia. The Geological Society of America. 190, 231–259. Special Paper, 382,1–229. Phillips, S. J., & Dudık, M. (2008). Modeling of species distributions with Wang, X. (Ed.) (1990). Vertebrate fauna of Ningxia. Yinchuan: Ningxia Peo- Maxent: New extensions and a comprehensive evaluation. Ecography, ple’s Publishing House. 31, 161–175. Warren, D. L., & Seifert, S. N. (2011). Ecological niche modeling in Max- Pisano, J., Condamine, F. L., Lebedev, V., Bannikova, A., Quer e, J.-P., ent: The importance of model complexity and the performance of Shenbrot, G. I., ... Michaux, J. R. (2015). Out of Himalaya: the impact model selection criteria. Ecological Applications, 21, 335–342. of past Asian environmental changes on the evolutionary and biogeo- Wingall, P. B., & Benton, M. J. (1999). Lazarus taxa and fossil abundance graphical history of Dipodoidea (Rodentia). Journal of Biogeography, at times of biotic crisis. Journal of the Geological Society, London, 156, 42, 856–870. 453–456. Potapova, E. G. (2014). Zygomasseteric construction in rodents (typologi- Yang, Z. (2007). PAML 4: Phylogenetic analysis by maximum likelihood. cal, adaptive and taxonomic aspects). Zoologicheskyi Zhournal (Russia), Molecular Biology and Evolution, 24, 1586–1591. 93, 841–856 [in Russian, English summary]. Zazhigin, V. S., & Lopatin, A. V. (2001). The history of the Dipodoidea Potapova, E. G. (2015). Specificity and evolutionary transformation of (Rodentia, Mammalia) in the Miocene of Asia: 4. Dipodinae at the jaw musculature in Laonastes aenigmamus and Ctenodactylus gundi Miocene-Pliocene transition. Paleontological Journal, 35,61–75. (Ctenodactyloidea, Rodentia). Archives of Zoological Institute RAN, 319, 401–417 [in Russian, English summary]. Potapova, E. G., & Rossolimo, O. L. (2008). Morphological diversity of mandible in the dormice family (Gliridae, Rodentia). Archives of Zoo- SUPPORTING INFORMATION logical Museum of Moscow State University, 49, 389–412 [in Russian, Additional Supporting Information may be found online in the English summary]. Rambaut, A., & Drummond, A. (2005). Tracer version 1.5. [Computer pro- supporting information tab for this article. gram distributed by the authors]. UK: Department of Zoology, Univer- sity of Oxford. Raoul, F., Pleydell, D., Quer e, J.-P., Vaniscotte, A., Rieffel, D., Takahashi, K., ...Giraudoux, P. (2008). Small-mammal assemblage response to defor- How to cite this article: Shenbrot G, Bannikova A, estation and afforestation in central China. Mammalia, 72, 320–332. Giraudoux P, Quer e J-P, Raoul F, Lebedev V. A new recent Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phyloge- genus and species of three-toed jerboas (Rodentia: netic inference under mixed models. Bioinformatics, 19, 1572–1574. Dipodinae) from China: A living fossil? J Zool Syst Evol Res. Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: a lab- – oratory manual. New York: Cold Spring Harbor Lab. Press. 2017;55:356 368. https://doi.org/10.1111/jzs.12182 Savinov, P. F. (1970). Dipodidae (Rodentia) of the Kazakhstanian Neo- gene. In K. K. Flerov (Ed.), Data on the evolution of terrestrial verte- brates (pp. 91–134). Moscow: Nauka Press. [in Russian].