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Geographic Pattern of Cranial Differentiation in the Asian Midday

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Geographic Pattern of Cranial Differentiation in the Asian Midday Accepted on 16 September 2011 Ó 2011 Blackwell Verlag GmbH J Zool Syst Evol Res doi: 10.1111/j.1439-0469.2011.00642.x 1Evolutionary Morphology of Vertebrates, Gent, Belgium; 2Rodentology Research Department, Ferdowsi University of Mashhad, Mashhad, Iran Geographic pattern of cranial differentiation in the Asian Midday Jird Meriones meridianus (Rodentia: Muridae: Gerbillinae) and its taxonomic implications Fatemeh Tabatabaei Yazdi1,2,Dominique Adriaens1 and Jamshid Darvish2 Abstract The existence of cryptic species in the midday jird (Meriones meridianus) has been suggested in literature, although based on little empirical data to support this hypothesis. In this study, a two-dimensional landmark-based geometric morphometric approach was used to investigate whether patterns in intraspecific variation in skull shape and size exist, using 110 skull specimens from more than 20 different localities along the distribution range of M. meridianus. This is the first study of morphological differences on such a big sample size and geographical range, and it tries to find whether skull shape variation in this species is best described as being clinal or rather reflecting cryptic diversity. The latter seems to be the case, as a dimorphic skull phenotype was found, reflecting a geographic disparity between the Middle East and the Far East specimens both in shape and in size. Distinct cranial differences were found in the overall cranial size and, also at the level of the inflation of the bulla, the elongation of the nasal, the length of the teeth row and the incisive foramen, as well as the distance in between the latter two. It thus seems that M. meridianus from Middle East is morphologically distinct from that of the Far East. Furthermore, our results also demonstrate that clinal variation could explain variation within Middle East populations, whereas a more heterogenous pattern is found for those of the Far East. The hypothesis that the observed phenotypic variation may reflect cryptic species is discussed, with the recommendation for a thorough taxonomical revision of the genus in the region. Key words: Central Asia – geometric morphometrics – Iran – Muridae – skull morphology Introduction continuous range of clinal variation requires comprehensive The midday jird (Meriones meridianus Pallas, 1773) is a analyses of characters that allow a quantification of even rodent species distributed from the Northern Caucasus and subtle levels of phenotypic variation. Considering the taxo- eastern Iran [central desert of Kerman (Darvish 2009)] to nomic ambiguities related to this species, emerging patterns Northern Afghanistan, Mongolia and Northern China (Lay in this phenotypic variation may also reflect cryptic species 1967; Hassinger 1973; Sheng et al. 1999; Denys et al. 2001; diversity. Musser and Carleton 2005). Substantial intraspecific varia- To test this hypothesis on clinal variation versus variation tion in morphological (external) characters, such as coat suggesting cryptic species diversity, M. meridianus from the colour, body size and bone structure in populations coming Middle East are compared with those of the Far East (Fig. 1), from different geographical locations has been shown (Cha- by performing a landmark-based geometric morphometric worth-Musters and Ellerman 1947; Wang and Yang 1983; analysis on the skull. Cranial differences, such as a cranial size Zhang 1997; Ito et al. 2010), leading to the description of difference between the specimens from Turkestan (Uzbekistan many subspecies. Seven subspecies have been recognized and Kazakhestan) and those from China (Far East popula- from the Xinjiang of China (Ito et al. 2010), as well as a tions), have already been reported in the past by Chaworth- separate species (Meriones dahlia; Musser and Carleton Musters and Ellerman (1947). Specimens originate from the 2005), whereas other species have been considered synony- localities spanning the species distribution range, including mous [e.g. Meriones chengi by Pavlinov et al. (1990, 1995) specimens collected from the type localities, as for example, and Ito et al. (2010)]. In most keys and revisions on the the topotype of M. chengi (Musser and Carleton 2005). Using genus Meriones, diagnostic features generally are ambiguous the cranium is especially relevant for studying phenotypic (Allen 1940; Chaworth-Musters and Ellerman 1947). Most of variation, as it is both genetically and functionally relevant the studies on M. meridianus mainly provided external and hence subjected to a substantial amount of selective diagnostic features, rather than cranial characters, and are pressure (Caumul and Polly 2005; Cordeiro-Estrela et al. often based on local samples without covering the speciesÕ 2008). distribution range (e.g. Allen 1940). Especially in the arid As such, the aims of this study are to (1) reveal the patterns habitat of the Iranian regions (especially the Iranian plateau), of intraspecific skull shape and size variation in M. meridi- this species has remained poorly studied (Misonne 1975). As anus along its distribution range; (2) test the hypothesis the midday jirds from the Iranian plateau are geographically whether continuous clinal variation rather than cryptic most distinct from the Far East specimens, morphological phenotypic differentiation explains the observed patterns; differences resulting from clinal variation can be expected. To and (3) find potential diagnostic cranial characters allowing what degree M. meridianus intraspecific variation reflects a further taxonomical clarification of this species. For the second aim, the congruence of shape variation in specimens from Iran with that of the Middle East is evaluated, where in Corresponding author: Fatemeh Tabatabaei Yazdi (fatemeh.tabatabaei @ugent.be, [email protected]) the case of clinal variation, a more similar phenotype is Contributing authors: Dominique Adriaens (dominique.adriaens expected with Middle East specimens that are geographically @ugent.be), Jamshid Darvish ([email protected]) closest. J Zool Syst Evol Res (2012) 50(2), 157–164 158 Tabatabaei Yazdi, Adriaens and Darvish Fig. 1. Map showing sampling localities of the Meriones meridianus (closed circles) and groups of sampling locality (ovals) used in this study. The dashed line separates the Middle East from the Far East groups Material and Methods Shape models based on the three sides of the skulls were digitized using the software TpsDig 2.12 (Rohlf 2004). Only one side (left side) Specimens analysed of the skulls was used so that specimens that were broken on one side In total, 110 skull specimens of M. meridianus (Pallas, 1773) from 21 could still be included (Elewa 2004). In case, the right side was used localities, originating from Iran to Mongolia and China, were used. (left side was broken), the landmark set was mirrored (following the Juvenile specimens, identified based on the eruption and amount of assumption that left–right asymmetry was smaller than the level of wear on the molars (M2; Petter 1959; Tong 1989; Pavlinov 2008), were intra- and interspecific variation that was the subject of this study). On excluded from the analyses. The only available type specimens the ventral, dorsal and lateral sides of cranium, respectively 20, 19 and [Meriones auceps (BMNH 8.8.4.30 male) and paratype of Gerbillus 21 two-dimensional (2D) landmarks, were chosen on the basis that psammophilus (1867N°138 MNHN)] were broken and thus not be they include all relevant features of the cranium (Fig. 2). The included in the analyses. landmarks were defined for each view of the cranium based upon the The specimens were obtained from the collections of the Smithso- terminology used by Popesko et al. (2002) and Tong (1989; Table S2). nian Natural Museum of Natural History, Washington, DC, USA (USNM), the Field Museum of Natural History, Chicago, CA, USA (FMNH), the British Museum of Natural History, London, UK Data analysis (BMNH), and the Muse´ e national dÕHistoire naturelle, Paris, France Shape analysis (MNHN). The list of studied specimens with catalogue numbers is A generalized procrustes analysis was performed using past (PAlaeon- available in the appendix. tologica STatistics) ver. 1.74 (Hammer et al. 2001), to standardize the Specimens were plotted according to the geographical coordinates of non-shape related variation in landmark coordinates. As such, land- the sample location, using ArcGIS, ArcMap 9.2 (Fig. 1). Latitude mark configurations were aligned by Procrustes superimposition, with and longitude were assigned based on the field notes of the collectors, removing differences in rotation and translation and by scaling to unit the collections catalogue of the museums or the climate-database of the centroid size (Gower 1975; Bookstein et al. 1985; Rohlf and Slice 1990; Food and Agriculture Organization of the United Nations (FAO, Rohlf and Marcus 1993). Both uniform and non-uniform partial warps 2007; Table S1). were calculated in past. Principal component analyses (PCA), using To perform robust canonical variate analyses, localities repre- past, and Canonical variate analysis (CVA), using statistica (StatSoft, sented by only a few specimens were pooled according to their version 7.0, www.statsoft.com, StatSoft, Inc., Tulsa, USA) were geographic proximity into eight analytical groups. Considering their performed on partial warp scores of each data set separately for the use in statistical analyses, samples far from other localities and dorsal, ventral and lateral data, to investigate the intraspecific variation having
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