grandis complex (Rodentia, Gerbillinae) during the Late Quaternary in northwestern Africa: Exploring the role of environmental and anthropogenic changes

Quaternary Science Reviews 164 (2017) 199e216

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Systematics and evolution of the Meriones shawii/grandis complex (Rodentia, Gerbillinae) during the Late Quaternary in northwestern Africa: Exploring the role of environmental and anthropogenic changes €l Cornette b, Aude Lalis b, Violaine Nicolas b, Emmanuelle Stoetzel a, *, Raphae c Thomas Cucchi , Christiane Denys b a HNHP UMR 7194, CNRS, Mus eum national d'Histoire naturelle, Sorbonne Universit es, UPVD, Mus ee de l'Homme, Palais de Chaillot, 17 place du Trocad ero, 75016 Paris, France b ISyEB UMR 7205, CNRS, Mus eum national d'Histoire naturelle, Sorbonne Universit es - UPMC - EPHE, CP 51, 55 rue Buffon, 75005 Paris, France c Arch eozoologie, Arch eobotanique UMR 7209, CNRS, Mus eum national d'Histoire naturelle, Sorbonne Universit es, CP 56, 55 rue Buffon, Paris, France

a r t i c l e i n f o

a b s t r a c t

Article history: Received 2 January 2017 Received in revised form 6 March 2017 Accepted 1 April 2017

Rodents of the Meriones shawii/grandis complex have been attested to in North Africa since the Middle Pleistocene and are abundant in archaeological sites. Today, they are widely spread and represent a major pest to local human populations. This complex, therefore, represents an accurate model for investigating the roles of climate change and human impact in shaping Quaternary faunal diversity and distribution. Many gray areas still exist regarding the systematics, ecology and geographical distribution of this complex, for both present and past populations. The purpose of this study is to compare modern genotyped and fossil Meriones specimens in order to 1) clarify the current systematics and distribution of the Meriones populations of the shawii/grandis complex, 2) document the taxonomic diversity in fossil Meriones from northwestern Africa, and 3) track their phenotypic and biogeographic evolution through time. To answer these questions we used geometric morphometrics on skulls (landmarks) and first upper molars (landmarks and sliding landmarks). We evidenced the existence of two morpho-groups within the M. shawii/grandis complex, with a clear geographic pattern (M. grandis in Morocco vs. M. shawii in Algeria and Tunisia). Currently only one morpho-group, attributed to M. grandis, seems to exist in Morocco, with a small overlap with M. shawii in the most eastern part of the country. However, according to fossil data, M. shawii was also present in Atlantic Morocco during the Late Pleistocene. We have also highlighted the impact of Holocene climate change and habitat anthropization on this arid adapted group. During the Middle Holocene, a major climatic event (last interglacial optimum) seems to have induced a demographic collapse in Moroccan populations and the disappearance of the shawii clade from Morocco (except in the most eastern areas). Both species then re-expanded, benefitting from the increasing aridity and the new ecological niche driven by agriculture dispersal from the Neolithic onwards. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Climate change Anthropic impact Late Pleistocene Holocene Maghreb Gerbillinae Geometric morphometrics

1. Introduction Located between the Mediterranean and sub-Saharan Africa, northwestern Africa encompasses a wide variety of natural environments and represents a crossroads for biodiversity. Small

* Corresponding author. E-mail address: [email protected] (E. Stoetzel). http://dx.doi.org/10.1016/j.quascirev.2017.04.002 0277-3791/© 2017 Elsevier Ltd. All rights reserved.

terrestrial vertebrates make up the majority of this biodiversity, including numerous endemics, particularly in gerbils, shrews, amphibians and squamates (e.g. Bons and Geniez, 1996; Schleich et al., 1996; Thevenot and Aulagnier, 2006; Aulagnier et al., 2008d). In addition, some species displaying a wide distribution across North Africa were found to be composed of several genetic clades, some of which could constitute a separate species, due to Quaternary climatic and environmental variations (e.g. Fromhage et al., 2004; Harris et al., 2004; Carranza and Wade, 2004; Fritz et al., 2006;

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 ski et al., 2012; Zangari et al., 2006; Kapli et al., 2008; Boratyn Husemann et al., 2014; Nicolas et al., 2014a,b; 2015). Moreover, these climatic and vegetation changes, especially in the Saharan area, could also have driven the emergence, evolution and dispersal of anatomically modern humans, present in northwestern Africa from at least 160 ka (e.g. McBrearty and Brooks, 2000; Manica et al., 2007; Smith et al., 2007; Osborne et al., 2008; Compton, 2011; Garcea, 2012; Whiting Blome et al., 2012; Drake et al., 2013). During the Holocene, the dispersal of farming communities during the Neolithic period induced a new era of human niche construction (Boivin et al., 2016). A major challenge today is to evaluate to what extent the increasing impact of human activities, since the Neolithic period interfere, and exacerbate natural phenomena, mainly relating to global climate change and local habitat changes. This study focuses on the rodents of the Meriones shawii/grandis complex (Muridae: Gerbillinae) as a model for investigating the roles of humans and climate change in shaping Quaternary faunal diversity and distribution (Lalis et al., 2016), for two reasons. Firstly, this complex is attested to in North Africa since the Middle Pleistocene (Jaeger, 1975; Tong, 1989; Stoetzel, 2013) and is the most abundant micromammal taxon in most Late Pleistocene assemblages (e.g. Ouahbi et al., 2003; Reed and Barr, 2010; Stoetzel et al., 2010a; Lopez-Garcia et al., 2013; Stoetzel, 2013), prior to any impact of human activities on the environment; and secondly, these anthropophilous rodents represent a major pest for local human populations today (Adamou-Djerbaoui et al., 2010, 2013; Ghawar et al., 2011; Derbali et al., 2012). Currently, three to four Meriones species are found in North Africa. Meriones libycus and M. crassus occupy mainly Saharan and arid areas throughout North Africa to western Asia (Aulagnier et al., 2008a,b,c,d). The Meriones shawii/grandis complex remains poorly understood due to its systematics, ecology and geographical distribution; but it appears to primarily occupy a large coastal fringe covering Morocco, Algeria, Tunisia, Libya, Egypt, and the west side of the Nile (Aulagnier et al., 2008b,d; Hutterer, 2008; Darvish, 2011), where it occasionally overlaps with the M. libycus and M. crassus species (Fig. 1). They are not found in mesic environments, such as forests, grasslands, wetlands, lakes, or rivers, and they avoid rocky basins (Aulagnier et al., 2008d). The systematics of the Meriones shawii/grandis complex still represents a major issue. Several studies consider M. shawii as a valid species within which a recognized number of sub-species could exist, based on the high variability of body size, fur color and skull measurements (Musser and Carleton, 2005; Darvish, 2011). In contrast, several authors consider shawii and grandis as

two subspecies of M. shawii (Petter, 1961; Aulagnier and Thevenot, 1986); whilst others recognize two valid species - M. shawii (Duvernoy, 1842) and M. grandis (Cabrera, 1907) - purely on the basis of external and cranial measurements (Cabrera, 1907; Pavlinov, 2000). However, these ideas are based upon small samples and applied classic morphometric methods (craniometric distances) on specimens from old collections, including specimens trapped in the wild or bred in captivity with doubtful species attribution in the absence of genetic analyses. Consequently, these studies have led to large biometric overlapping and no clear conclusion on the geographical distribution of shawii or grandis (Botton-Divet, 2011). Recent genetic analyses (mtDNA, nDNA, microsatellites; Lalis et al., 2016) have revealed the existence of three mtDNA clades within the M. shawii/grandis complex in northwestern Africa: two clades (A and B) in Morocco (sympatric and genetically closely related, representing a monophyletic group), and one clade (C) mainly in Algeria and Tunisia, with a slight overlap between clades A and C in eastern Morocco. Nuclear DNA has highlighted the existence of only two groups, but with a similar geographic pattern (Morocco vs. Algeria and Tunisia, with a small overlapping region in eastern Morocco). “Modern” jirds of the shawii/grandis complex appear at the end of the Middle Pleistocene, and then dominate the Late Pleistocene micromammal assemblages in North Africa (Stoetzel, 2013). All jirds of “modern” morphology dating to the Late Quaternary were automatically assigned to M. shawii. Two exceptions are remains attributed to M. cf. libycus from Oued Assaka (southern Morocco, Late Pleistocene; Wengler et al., 2002) and to M. cf. crassus from Bir Tarfawi (Egypt, Late Pleistocene, Kowalski et al., 1989, 1993), both arid areas. However, there is no mention of M. grandis in the North African fossil record. Complete skulls are extremely rare in fossil contexts, and most identifiable remains consist of isolated molars or broken mandibles and maxillaries. As Meriones representatives display high similarities in molar morphology, it is possible that several Meriones species were recorded in Late Pleistocene and Holocene North African sequences, but were incorrectly recognized. Consequently, the systematic confusion observed for modern populations may also be true for fossils; few studies have focused on the fossil remains of the shawii/grandis complex, and those that did not attempt to separate the species. For this study, we compared modern genetically typed and fossil Meriones specimens using dental and cranial morphometric markers to: 1) clarify the current systematics and distribution of the Meriones populations of the shawii/grandis complex, through the use of a new protocol adapted to the study of Meriones molars;

Fig. 1. Current distribution of northwestern African Meriones species (data from http://www.iucnredlist.org/).

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2) document the taxonomic diversity in fossil Meriones from Morocco during the Late Pleistocene and the Holocene, and 3) track their phenotypic and biogeographic evolution through time and the influence of climatic and anthropogenic changes. We explored the morphometric characteristics of genotyped specimens in order to see whether their phenotypic variability displayed any phylogeographic signal, and to attempt to infer the attribution of museum specimens and fossils by comparing them to the genotyped specimens. Finally, in comparing genetic and morphometric data based on modern and fossil specimens, this study pursued a better understanding of the impact of climate change and anthropogenic pressures on rodent populations at different spatial and temporal scales. 2. Study material 2.1. Modern specimens Modern specimens from across Maghreb were selected from a combination of museum collections and trapping (Fig. 2, Table 1), and both natural (steppes, open forests) and anthropogenic habitats (fallow lands, cultivated fields) were sampled (Stoetzel et al., 2010b, 2012b; Denys et al., 2015). We included specimens of Meriones libycus (n ¼ 37), M. crassus (n ¼ 34), M. shawii/grandis (n ¼ 296), and Psammomys obesus (n ¼ 28)  a sister genus of Meriones (Tong, 1989; Chevret and Dobigny, 2005) that can easily be confused with Meriones in a fossil context due to its close molar morphology (Tong, 1989). The type specimen and the type serie of M. grandis (Cabrera, 1907; type locality: Marrakech, Morocco; stored at the Museo Nacional de Ciencias Naturales in Madrid, Spain) were also included in this study. Unfortunately, the type specimen of M. shawii (Duvernoy, 1842; type locality: Oran, Algeria; supposedly stored at the Mus ee Zoologique in Strasbourg, France) appears to have been lost. Pending the establishment of a neotype for M. shawii, we have included type specimens of three M. shawii subspecies from the Natural History Museum, London; detailed information for each museum specimen used in this study is provided in the supplementary material (Appendix A). In total, 291 specimens came from Morocco, 79 from Algeria, 41 from Tunisia, and 13 from other localities (Afghanistan, Arabia, China, Iran, Israel, Libya, Niger and Syria). We avoided specimens born and bred in captivity, which could have had morphological abnormalities or have been artificially larger than wild specimens due to a richer diet (e.g. Crossley and del lez, 2001; O'Regan and Kitchener, 2005). From the tooth Mar Migue

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analysis we excluded any specimens displaying dental plaque, which could hide part of the molar outline, though most were retained for skull analyses. All recently trapped specimens were genotyped and attributed to one clade (A, B and C for mtDNA data; 1 and 2 for nDNA data) of the M. shawii/grandis complex based on molecular data (Lalis et al., 2016). All museum specimens were identified to species level based on museum labels. 2.2. Fossil material First upper molars were sampled from several Moroccan archaeological caves (Fig. 2, Table 1): El Harhoura 2 (n ¼ 380) and El Mnasra (n ¼ 92) on the North Atlantic coast near Rabat; Tamaris (n ¼ 87), further south near Casablanca; and Guenfouda (n ¼ 11) in eastern Morocco near Oujda. The detailed microvertebrate faunal list of each site is provided in supplementary material (Appendix B). El Harhoura 2 (EH2) and El Mnasra (EM) are two coastal caves mara region which have yielded exceptional located in the Rabat-Te fossil records covering the last 120,000 years (El Hajraoui et al., 2012; Jacobs et al., 2012; Janati Idrissi et al., 2012). The human context in which these settlements occurred is well known: several cultures succeeded each other during the Late Pleistocene (Aterian [Middle Stone Age], Iberomaurusian [Late Stone Age]) and the Holocene (Neolithic) (Nespoulet et al., 2008; El Hajraoui et al., 2012; Stoetzel et al., 2014b). The small vertebrate assemblages from EH2 were extensively studied using taxonomic, taphonomic and palaeoecological analyses (Cornette et al., 2015; Stoetzel et al., 2008, 2010a, 2011a, 2012a, 2013, 2014b). The small vertebrate assemblages from EM are still being studied; however, the preliminary results are interesting and indicate that it could be as rich as EH2 (Amani et al., 2012; Stoetzel et al., 2011b, 2014a, 2014b; Campmas et al., 2015). All the Meriones remains from both sites were identified as belonging to the M. shawii/grandis complex (Stoetzel et al., 2010a, 2011a). The palaeoecological analysis showed a succession of arid and more humid periods during the Late Pleistocene, ending with a humid period during the Middle Holocene, corresponding to the last climatic optimum by 5e6 ka BP (Stoetzel et al., 2011a, 2014b). These environmental changes accompany differences in the relative proportion of small vertebrate species between the EH2 levels; which are not due to the type of predators at the origin of the fossil accumulations, or other taphonomic agents (Stoetzel et al., 2011a). Meriones represent the most abundant small vertebrate taxon in all of the Late Pleistocene levels of EH2, while a significant decrease in the proportion of

Fig. 2. Location of modern and fossil study samples (H ¼ El Harhoura 2, M ¼ El Mnasra, T ¼ Tamaris, G ¼ Guenfouda).

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Table 1 Synthesis of the modern and fossil specimens used in this study (for details of each museum specimens, see supplementary material). Material/Species

Modern/Fossil

a

Meriones gr. shawii/grandis Meriones gr. shawii/grandisa

Numerical dating

Country of origin

El El El El

Harhoura Harhoura Harhoura Harhoura

2 2 2 2

-

level level level level

1 2 3 4a

87

5

1 13

92

1 13

107

87

5

14

92

14

Clade A

Clade B

Clade C

Clade 1

Clade 2

121b 13

112

7

1 13

118

2 13

134

112

7

14

118

15

130 27 15 17 2 22 3 7 6 13 12 6 3 16 9

Morocco Morocco Morocco Morocco

17 23 43 25

Morocco

65

Morocco Morocco Morocco

96 48 63

Morocco Morocco

17 75

Morocco Morocco

87 11

288 F F F F

(Holocene) (Late Pleistocene) (Late Pleistocene) (Late Pleistocene)

F (Late Pleistocene) F (Late Pleistocene) F (Late Pleistocene)

El Mnasra - level 4 El Mnasra - level 6

F (Late Pleistocene) F (Late Pleistocene)

Tamaris Guenfouda

F (Late Pleistocene) F (Holocene)

~5.8e6.9 ka BP (14C) ~12 ka BP (14C) ~51.6e61.9 ka (OSL) ~73.7 ka (OSL) - ~44 ka (ESR/U-Th) ~102.6 ka (OSL) - ~62 ka (ESR/U-Th) ~116.4 ka (OSL) ~108.1 ka (OSL) ~106.7 ka (OSL) - ~92 ka (ESR/U-Th) ~106.7e94.6 ka (OSL) ~111.6e107.4 ka (OSL) - ~89-67 ka (ESR/U-Th) ~23.5e13.5 ka (14C, doubtfull) no dating

Total fossil specimens TOTAL

570 965 Modern/Fossil

Numerical dating

M M

Country of origin

Morocco Algeria

TOTAL b

Clade 2

Morocco Morocco Algeria Tunisia Morocco Algeria Tunisia Other Morocco Algeria Tunisia Other Morocco Algeria Tunisia

El Harhoura 2 - level 6 El Harhoura 2 - level 7 El Harhoura 2 - level 8

a

Clade 1

b

M M M M M M M M M M M M M M M

F (Late Pleistocene)

Meriones gr. shawii/grandisa Meriones gr. shawii/grandisa

Clade C

94 13

El Harhoura 2 - level 5

Material/Species

nDNA Clade B

Morocco Algeria

Total museum specimens

mtDNA Clade A

M M

Total genotyped specimens Meriones grandis Meriones shawii Meriones shawii Meriones shawii Meriones crassus Meriones crassus Meriones crassus Meriones crassus Meriones libycus Meriones libycus Meriones libycus Meriones libycus Psammomys obesus Psammomys obesus Psammomys obesus

n M1

n skulls

mtDNA

nDNA

Genotyped specimens. One skull correspond to an individual (MA142) for which DNA sequence was not available.

Meriones is observed in Holocene level 1, attributed to the Neolithic (Stoetzel et al., 2011a). Meriones are currently poorly represented mara on the Septentrional Atlantic plains, including the Rabat-Te region (Aulagnier and Thevenot, 1986; Aulagnier, 1992), probably due to the increasing urbanization of the coast in this region. Tamaris, also named the Grotte des Gazelles (Casablanca region), yielded relatively little material during rescue excavations, prior to destruction of the site. The levels studied, attributed to the Late Pleistocene, yielded Middle Stone Age industries and faunal remains (Bougariane et al., 2010; Daujeard et al., 2011). The small mammals have only been subjected to preliminary studies (Bougariane et al., 2010; Geraads et al., 2010; Stoetzel, unpublished) and the Meriones remains have all been identified as M. shawii (Geraads et al., 2010). Radiocarbon dating on gastropod shells provided ages of between 23,500 and 13,500 years BP, but these ages are probably underestimated as the gastropod shells may be intrusive (Bougariane et al., 2010) or a reservoir effect could have

occurred. Due to the evidence of both large and small faunas, the environment was probably open and relatively arid (Bougariane et al., 2010; Geraads et al., 2010), in keeping with the presence of gerboa, Jaculus sp. (Stoetzel, unpublished). A taphonomic study was performed on the large mammals, primarily with a zooarchaeological purpose (human vs. carnivore accumulations; Daujeard et al., 2011), but not on the small mammal assemblages. The samples from Guenfouda cave (Oujda region) came from Holocene levels where Neolithic artifacts (lithic tools, Cardial ceramics) and domestic faunas were also found (Aouraghe et al., 2008, 2010; Bougariane, 2013); however, as yet, no numerical dating is available. The small mammal assemblages were previously studied by Lopez-Garcia et al. (2013), who attributed the Meriones remains from Guenfouda to M. shawii. The palaeoecological study concluded a mosaic landscape dominated by a Mediterranean climate that was slightly drier than today (LopezGarcia et al., 2013), but no thorough taphonomic study was

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performed. This site is particularly interesting, as it is located in a zone where clades A and C of the M. shawii/grandis complex, highlighted by Lalis et al. (2016), co-occur. However, only a few Meriones fossil teeth were able to be considered from this site. Most of the fossil small vertebrate assemblages, especially from caves, consisting of predator pellet/scat accumulations (Andrews, 1990), were prey bones that may have been subjected to ingestion and digestion by predators. Enamel dissolution on teeth is common in such assemblages (Andrews, 1990; Stoetzel et al., 2011a; Fernandez-Jalvo et al., 2016), and may change the outline of the molars. We therefore excluded from our analyses all specimens presenting such alterations, as well as all broken or cracked molars. 3. Methods 3.1. Preliminary remarks To compare modern and fossil specimens we relied on the first upper molars as phenotypic markers, since teeth represent the most diagnostic and abundant element in fossil assemblages. Skulls were only considered for systematic purposes based on genotyped specimens. Moreover, specimens were pooled independently of their sex  since sex is impossible to assess on fossil remains  and no sexual dimorphism was observed on the skull morphology and size within Meriones (Pavlinov, 2000; Darvish, 2009; Botton-Divet, 2011; Tabatabaei Yazdi et al., 2014; Nanova, 2014). 3.2. Age classes One of the difficulties in studying Meriones molars is their semihypsodont characteristic. In very young individuals, molars are unrooted and show a high crown; while in adults molars are fully rooted and the crown-height progressively decreases with toothwear, while its occlusal surface increases. In addition, contrary to hypsodont arvicoline rodents for which tooth-wear does not impact the tooth morphology in the occlusal view, in Meriones, the drawing of the occlusal surface changes notably between young and old individuals. The semi-hypsodont Meriones molars, therefore, are intermediate between murine molars (rooted, bunodont) and arvicoline molars (unrooted, hypsodont). Consequently, the study method had to be adapted, and we established the age classes based on tooth eruption, root development, and aspect of the occlusal surface of Meriones molars (Fig. 3), following previous works (Petter, 1956; Barreau et al., 1991; Momenzadeh et al., 2008) and personal observations. In juveniles (classes 1 and 2), molars do not totally emerge, lophs are still individualized, and the molar outline is partly hidden by the maxillary/mandible bone. In adults (classes 3 and 4), tooth eruption is complete and tooth-wear is progressively more pronounced giving a “prismatic” aspect to the occlusal surface. In very old individuals (class 5), the crown is markedly worn and the lateral parts of the enamel are prone to disappear. In order to avoid any bias linked to the age of the specimens, and after having tested several situations (data not shown), we chose to only consider the middle classes 3 and 4 (adults), and eventually late stage 2 and early stage 5. 3.3. Geometric morphometrics 3.3.1. Skulls Skull analyses on genotyped specimens of the M. shawii/grandis complex (analyzed by Lalis et al., 2016) explore the genetic vs. morphometric systematics and geographic pattern of this complex in northwestern Africa.

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Several studies have been conducted on Meriones skulls and tympanic bullae using traditional morphometrics (Momenzadeh et al., 2008; Darvish, 2009, 2011; Nanova, 2014) or geometric morphometric approaches (Momtazi et al., 2008; Tabatabaei Yazdi and Adriaens, 2011, 2013; Tabatabaei Yazdi et al., 2012, 2014, 2015; Dianat et al., 2016). However, these studies mostly focused on Asian populations, and rarely included Northern African specimens (Darvish, 2009, 2011). Due to the morphological differences between the M. shawii/grandis complex and Asian Meriones, notably in the posterior part of the skull (tympanic bullae), we combined methodologies from previous studies (Tabatabaei Yazdi et al., 2012; Tabatabaei Yazdi and Adriaens, 2013) and adapted them to the North African Meriones. Twenty-two landmarks (LM) were positioned on the dorsal side of the skull and 24 on the ventral side (Fig. 4a, Appendix C). 3.3.2. Molars All Meriones species have very similar molar morphology (Tong, 1989; Stoetzel et al., 2010a) and are close to the Psammomys genus; therefore it is almost impossible to distinguish them solely on the basis of isolated molar observations, except when considering size parameters, which is difficult due to the existence of high variability inducing overlapping (Stoetzel et al., 2010a). Here, we attempted to test the efficiency of geometric morphometric approaches to maximize the identification of Meriones molars within the fossil context, and to perform modern vs. fossil comparisons. To quantify the complex molar form of Meriones, we combined landmarks (LM) with sliding landmarks (SLM) on the first upper molars (M1) following Cucchi et al. (2014). Nineteen LM and 76 SLM were used, representing a total of 95 points (Fig. 4b). Twelve LM were positioned at the maximum curvature of the salient and reentrant angles of the lophs. An additional 7 LM were placed on the maximum curvature of the molar outline, between which the 76 SLM were positioned on the outline (Fig. 4b). The referential data-set includes well-identified museum collections of P. obesus, M. libycus, M. crassus, and genotyped specimens of the M. shawii/grandis complex (Table 1). Other M. shawii/ grandis specimens from museum collections, as well as fossils, did not participate in the construction of the reference data set and were re-assigned a posteriori. 3.4. Data acquisition and analyses Skulls and molars were photographed using a digital camera coupled with a binocular microscope. Specimens were carefully placed in the same standardized position throughout the data acquisition. The right side was systematically considered, and when the left side was used (fossil molars, modern skulls with broken/ unusable right side) the pictures were mirrored before landmark positioning. Landmarks were then placed on the digital pictures and the coordinates of the LM and SLM were captured using TPS Dig 2 (Rohlf, 2016a). To remove information on position, scale, and orientation from the Cartesian coordinate configurations, we performed a generalized Procruste analysis using TPS relw (Rohlf, 2016b) to produce a new set of shapes coordinates. The semi-landmarks were forced to slide on a tangent according to the Bending Energy algorithm (Bookstein, 1997). The resulting Procrustes shape coordinates from this superimposition were used as shape variables for subsequent statistical analyses. The centroid size of the M1 and the skulls was measured using the square root of the sum of the squared distances between each point and the centroid of the configuration. A standard preliminary procedure of repetition tests of orienting-digitizing and landmark positioning was performed on molars, revealing no significant bias (intra-specimen measurement

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Fig. 3. Age classes used in this study (Meriones upper tooth-raw in occlusal view).

variability ≪ inter-specimen variability; data not shown). Size differences were investigated using ANOVA with pairwise t-tests comparisons using Bonferroni correction. Patterns of shape variation were investigated using a Principal Component Analysis (PCA) and differences between groups were tested using a MANOVA and pairwise comparisons using t-tests with Bonferroni correction. To compare shape differences between modern and fossil specimens or between modern taxa, we performed Discriminant Function Analysis (DFA) on the n axes of the PCA, representing 99% of the total variance (reduction of dimensionality). For the skulls, we used the first 31 axes for the dorsal view and the first 34 axes for the ventral view; for molars, we used the first 34 axes of the PCA. In order to increase the efficiency of the discriminations, the log of the centroid size was also considered for DFA if there was a significant difference between the considered groups. In these cases, we used the term “form” (shape þ size) instead of “shape”. Cross validations were performed to obtain classification matrices. Statistical analyses were performed using SYSTAT (v.12) and PAST (v. 2.17b and 3.14). 4. Results 4.1. Skull size and shape The analysis of skulls only considered genotyped specimens of the M. shawii/grandis complex. The typed specimens of each clade (A, B and C) did not show significant differences in dorsal (ANOVA: p ¼ 0.3913) or ventral (ANOVA: p ¼ 0.7163) skull centroid size (Fig. 5). Therefore, no size correction of the shape variables was required to investigate the shape difference among clades. MANOVA (dorsal: p < 0.001; ventral: p < 0.001) indicated significant differences in skull shape. The DFA graphs show a clear discrimination between the three clades, especially on the first discriminant axis between clades A þ B, and clade C (Fig. 6). Clades A and B are discriminated on the second axis, but less efficiently. The percentage of correct classification after cross validation was between 83% and 93% for the dorsal view, and between 84% and 96% for the ventral view (Table 2). Interestingly, clade C specimen MA234  which was systematically wrongly re-classified as clade A  corresponds to a specimen trapped at Guenfouda, eastern Morocco, and shows discrepancy between mtDNA and nDNA clade assignation (Lalis et al., 2016). Moreover, most of the incorrect classifications are between clades A and B, which are also the closest genetically (Lalis et al., 2016). The main morphological differences between the three clades are as follows (Fig. 7): for the dorsal view, compared to clades A and

B, clade C presents a longer nasal, point 17 (intersection of the upper and lower supramastoid apophyses of the squamosal) is located more anteriorly, and the parietal is relatively short. Clade B is close to clade A, but with a shorter nasal. For the ventral view, compared to clades A and B, clade C shows a larger tympanic bullae, a shorter toothrow, and a larger zygomatic arch at the level of point 16. Here again, clades A and B are close to each other, but in clade A, points 10 and 11 are located more anteriorly, and the tympanic bullae is smaller. 4.2. Molar size Significant overall differences of centroid size were observed among the taxa (ANOVA: p < 0.001). In Fig. 8a and Table 3a we can see that within the genotyped specimens, clade C has a significantly smaller M1 than clades A and B. Within specimens from museum collections, P. obesus, which is classically considered as larger than most Meriones species (Aulagnier et al., 2008d), presents a molar size similar to that of M. shawii/grandis. Molar size is therefore not a valid criterion in distinguishing Psammomys and Meriones, especially when considering isolated molars in a fossil context. M. crassus and M. libycus display a significantly smaller size than representatives of the M. shawii/grandis complex (museum collections and genotyped specimens). Fossil specimens exhibit wide size variability, especially at EH2, but fit within the range of museum specimens of M. grandis, M. shawii and molecular clades A and B. When looking at the detailed size data of fossil sequences (Fig. 8b), we can observe a slight tendency toward an increase in size over time. There is a significant difference between EM level 6 (OSL: ~107-111 ka BP) on the one hand, and EM level 4 (OSL: ~94106 ka BP) and EH2 levels l, 2, 4, 5 and 6 (14C level 1: ~5.8 ka BP; OSL level 6: ~116 ka BP) on the other (Table 3b). However, this observation is not really supported by statistics within the EH2 sequence (pairwised comparisons were not significant); moreover, the Holocene level from Guenfouda is the same as the Late Pleistocene levels from the other sites. In addition, within the M. shawii specimens from the MNHN (Paris), the range of size variability is large, and it seems that the two groups were most likely classified together. Moreover, these two groups are structured geographically, with larger specimens coming mainly from Morocco and smaller specimens coming mainly from Tunisia or Algeria (Fig. 8c). Finally, we found different groups based on molar size: a “smallsized group” composed of M. crassus and M. libycus, a “large-sized group” composed of Moroccan specimens of the shawii/grandis complex (genotyped specimens from clades A and B; M. grandis and

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part of the M. shawii specimens from museum collections), and a “medium-sized group” composed of Algerian and Tunisian populations of the shawii/grandis complex (genotyped specimens from clade C, including one Moroccan specimen, and part of the M. shawii specimens from museum collections). 4.3. Molar form The modern Meriones specimens present significant differences in M1 shape (MANOVA: p < 0.001; Table 4). Since the size was significantly different between some of the considered groups, we choose to include the log of the centroid size in the DFA analysis in order to increase the efficiency of the discriminations, and have therefore used the term “form” (shape þ size) rather than “shape”. The DFA was performed on the different reference groups (M. crassus, M. libycus, Moroccan clades A and B, and Algerian clade C of the M. shawii/grandis complex) and evidenced a good discrimination level: 79%e92% of correct classification (Table 5). Most of the incorrect reclassifications concerned clades A and B, which are also the closest genetically (Lalis et al., 2016). Compared to size analysis, the most striking difference observed in Fig. 9 is between P. obesus and all the representatives of the Meriones genus on axis 2. It appears that while P. obesus and M. shawii/grandis were not distinguishable on size alone, molar form allowed good discrimination at the genus level. Meriones

205

crassus and M. libycus are well distinguished from their molar form on axis 3 of the DFA. Both species are distinct from clades A and B on axis 1. Within the M. shawii/grandis complex, clade C is distinguishable from clades A and B on axis 1. Within the A and B clades, molar form is not discriminant and therefore they belong to the same morpho-group. We re-assigned the fossil specimens and the M. shawii/grandis specimens from the museum collections in order to see in which morpho-group they should be placed (Table 5, Appendix A, Fig. 9b). The Moroccan specimens labelled M. grandis in the museum collections corresponded mainly to clades A and B, and the holotype of M. grandis was attributed to clade A. A large part of the M. shawii specimens from collections (based upon external measurements) were assigned to clade C and came from either Algeria or Tunisia. Surprisingly, however, the type specimens of the M. shawii subspecies (M. s. trouessarti, M. s. auziensis, M. s. crassibula) from the NHM (London) were assigned to clade A or even to M. crassus. The Meriones shawii specimens from the MNHN (Paris) seemed to be composed of two morpho-groups structured geographically, with more than 62% attributed to clades A and B and more than 32% to clade C. These results confirm the observations made on size (Fig. 8) and argue for the mixing of several species in the M. shawii collection from the MNHN (Paris). Regarding the fossil material from the studied archaeological caves (Table 5, Fig. 10), we found a clear dominance of clades A and

Fig. 4. Position of the landmarks (LM) and sliding landmarks (SLM) used in this study: a) Meriones skull in dorsal and ventral view; b) Meriones first upper molar in occlusal view (green points ¼ internal LM, red points ¼ external LM, dotted lines and numbers in brackets ¼ SLM). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

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Fig. 5. Distribution of the centroid size of the studied skulls of the M. shawii/grandis genotyped specimens belonging to clades A, B and C: a) in dorsal view; b) in ventral view.

B. However, in the oldest levels of EH2, EM and Tamaris, there was a significant representation of clade C, which decreased slightly over time. In contrast, in the Holocene levels of EH2 and Guenfouda, only clades A and B were represented. Some fossil specimens were also assigned to M. crassus and/or M. libycus, but in low proportions. No fossil specimen was assigned to Psammomys.

5. Discussion 5.1. New inputs on the systematics of the modern Meriones shawii/ grandis complex

(A, B and C) and two nuclear clades (1 and 2) within the M. shawii/ grandis complex in northwestern Africa, and showed a clear distinction between the occidental (Morocco) and oriental (Algeria, Tunisia, eastern Morocco) populations. They concluded that these two main groups should be considered as two sister species that diverged in the Early Pleistocene, but who retained possibilities of hybridization (we are probably in the presence of an ongoing speciation); however, they could not determine to which species (shawii or grandis) each clade belonged. Our morphometric study shows the existence of two morpho-groups within the M. shawii/ grandis complex, with a similar geographic pattern in both skull shape and molar size and shape (Morocco vs. Algeria, Tunisia and eastern Morocco). By comparing these genotyped specimens to

Lalis et al. (2016) evidenced the existence of three mtDNA clades

Fig. 6. Shape differences (conformation) of the studied skulls of the M. shawii/grandis genotyped specimens belonging to clades A, B and C, expressed by the two axes of the DFA performed on the first 31 axes of the PCA for the dorsal view (a) and on the first 34 axes of the PCA for the ventral view (b).

E. Stoetzel et al. / Quaternary Science Reviews 164 (2017) 199e216 Table 2 Classifications provided by Discriminant Function Analyses on the skull shape variables (dorsal and ventral view) of the M. shawii/grandis genotyped specimens belonging to clades A, B and C. A Skull dorsal: Classification Matrix A 103 B 0 C 1 Total 104 Jackknifed Classification Matrix A 96 B 5 C 1 Total 102 Skull ventral: Classification Matrix A 106 B 1 C 1 Total 108 Jackknifed Classification Matrix A 96 B 4 C 2 Total 102

B

C

% correct

8 6 0 14

0 0 13 13

93 100 93 93

15 1 1 17

0 0 12 12

86 17 86 83

3 5 0 8

0 0 13 13

97 83 93 96

12 2 2 16

1 0 10 11

88 33 71 84

collection specimens (including type specimens) we evidenced that the two occidental clades (mtDNA clades A and B, nDNA clade 1) corresponded to M. grandis; while the oriental clade (mt DNA clade C, nDNA clade 2) corresponded to M. shawii, with a contact zone in eastern Morocco. These results contradict the statement of Pavlinov (2000), who said that the geographic distribution of M. shawii and

207

M. grandis widely overlap in Tunisia, Algeria and eastern Morocco. However, the fact that some M. shawii ancient sub-species belong to the M. grandis (clade A) morpho-group indicates that M. grandis may also occur in western Algeria, a region whose small fauna is still poorly understood. This result may also be biased by the low number of specimens belonging to these M. shawii sub-species (only three specimens, all coming from Algeria). The collection specimens from the MNHN (Paris), which were previously assigned to M. shawii, seem to be composed of two groups, both in size and shape, and a geographical structure: a Moroccan group composed of larger specimens, which can be reassigned to M. grandis, and a group composed of smaller specimens from Algeria and Tunisia, which could correspond to “true” M. shawii, and perhaps also to other species (M. crassus, M. libycus). This result raises the question of the validity of some museum collections (including specimens trapped a long time ago and/or misidentified in the field) as reference data-sets, and highlights the necessity to revise these collections. We have detailed in Appendix A the re-attribution of specimens according to our results on molar form. Such misidentifications were not highlighted for the other collections, notably because of a lesser number of specimens (London) and/or because the specimens all came from the same location (Marrakech region for the Bonn and Madrid specimens). Some morphological features revealed by the geometric morphometric analysis of skulls and molars are in agreement with previous studies: clades A and B (i.e. M. grandis) display notably smaller tympanic bullae than clade C (i.e. M. shawii), as previously evidenced by Cabrera (1907). Following the statement that the development of tympanic bullae is linked to arid habitats, especially in Gerbilline rodents (e.g. Petter et al., 1984; Momenzadeh et al., 2008; Momtazi et al., 2008), M. shawii is more likely to occur in more arid habitats than M. grandis, as previously suggested

Fig. 7. Consensus skull shapes of the M. shawii/grandis genotyped specimens belonging to clades A, B and C.

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Fig. 8. Distribution of the centroid size of the studied modern and fossil molars of Meriones and Psammomys: a) main modern and fossil groups, b) detailed data by fossil level and collection origin, c) detail of the geographic origin of the M. shawii specimens from the Mammiferes et Oiseaux laboratory (MNHN, Paris). A, B and C ¼ genotyped M. shawii/grandis specimens belonging to clades A, B and C; Foss ¼ fossil; EH2 ¼ El Harhoura 2; EM ¼ El Mnasra; Guenf ¼ Guenfouda; London ¼ specimens from the NHM (London); M&O ¼ specimens from the Mammiferes et Oiseaux laboratory (MNHN, Paris); Madrid ¼ specimens from the MNCN (Madrid).

by several authors (Petter and Saint Girons, 1965; Aulagnier et al., 2008b; Hutterer, 2008). Concerning size, it is generally agreed that the grandis group is larger than the shawii group, if considering

both external and skull measurements (Petter, 1961; Petter and Saint Girons, 1965; Pavlinov, 2000). Our analysis confirmed such trends on molars (upper M1 and toothrow) but not on skulls.

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209

Table 3 Size differences between the studied modern and fossil molars of Meriones and Psammomys (ANOVA): P-values of the post hoc pairwise comparisons (with Bonferroni correction) are provided. a) main modern and fossil groups, b) detailed data by fossil level. A, B and C ¼ genotyped M. shawii/grandis specimens belonging to clades A, B and C; Foss ¼ fossil; EH2 ¼ El Harhoura 2; EM ¼ El Mnasra; Guenf ¼ Guenfouda.

A

B

C

Foss_EH2 Foss_EM Foss_Guenf Foss_Tamaris M.crassus M.grandis M.libycus M.shawii P.obesus

A B

1.000

C

0.004

1.000

Foss_EH2

1.000

1.000 0.009

Foss_EM

0.052

1.000 0.851

0.043

Foss_Guenf

1.000

1.000 1.000

1.000

Foss_Tamaris 0.222

1.000 <0.001 0.003

1.000 <0.001

1.000

<0.001

<0.001

<0.001

<0.001

1.000

1.000

<0.001

<0.001

<0.001

<0.001

<0.001

1.000

<0.001

1.000 0.617

1.000

1.000

1.000

1.000

<0.001

1.000

<0.001

1.000 1.000

1.000

1.000

1.000

0.123

<0.001

0.1206

0.004

M.crassus

<0.001 0.048 0.336

M.grandis

0.418

M.libycus

<0.001 0.048 1.000

M.shawii

1.000

P.obesus

1.000

<0.001

1.000 <0.001 0.002

Foss_EH2_c1

1.000

Foss_EH2_c2 Foss_EH2_c3 Foss_EH2_c4a Foss_EH2_c5 Foss_EH2_c6 Foss_EH2_c7 Foss_EH2_c8 Foss_EM_c4 Foss_EM_c6 Foss_Guenf Foss_Tamaris

Foss_EH2_c1 Foss_EH2_c2

1.000

Foss_EH2_c3

0.086

0.645

Foss_EH2_c4a 1.000

1.000

0.156

Foss_EH2_c5

1.000

1.000

0.012

1.000

Foss_EH2_c6

1.000

1.000

1.000

1.000

0.939

Foss_EH2_c7

0.294

1.000

1.000

1.000

0.144

1.000

Foss_EH2_c8

0.377

1.000

1.000

0.938

0.137

1.000

1.000

Foss_EM_c4

1.000

1.000

0.208

1.000

1.000

1.000

0.854

0.863

Foss_EM_c6

0.005

0.030

1.000

0.002

<0.001

0.014

1.000

1.000

0.014

Foss_Guenf

1.000

1.000

1.000

1.000

1.000

1.000

1.000

1.000

1.000

1.000

Foss_Tamaris

1.000

1.000

<0.001

1.000

1.000

0.016

0.002

0.001

1.000

<0.001

Our results, combined with those obtained by Lalis et al. (2016) clearly show that M. grandis and M. shawii can be considered as two distinct species. The two Moroccan clades A and B within M. grandis could be the result of an ancient divergent event dating from the Middle Pleistocene. 5.2. Which species occurred in the Late Quaternary sequences of Morocco? While it was almost impossible to accurately attribute isolated molars to Psammomys or Meriones on the basis of molar size or “classic” morphological features on molars, our geometric morphometric study has shown that they can be efficiently discriminated on the basis of the M1 form. In addition, we have shown that all the fossil material was composed of Meriones, and that Psammomys never occurred in the studied sequences. In the Moroccan studied fossil sites, the M. shawii/grandis group was largely dominant. But, whereas all jird remains were usually automatically attributed to M. shawii in studies of North African fossil assemblages, we found a clear dominance of the Moroccan clades A and B that corresponded to M. grandis. This is confirmed by ancient DNA analysis showing that clades A and B were represented in the EH2 levels 1 and 4a (i.e. during the Holocene and the Late Pleistocene; Guimaraes et al., 2016). These authors did not identify the genetic sequence belonging to clade C in the EH2 sequence, but our study has clearly recorded significant numbers of the oriental clade (C, M. shawii) in the Late Pleistocene levels of EH2, EM and Tamaris. These contrasting results can be explained by the fact that few DNA sequences were obtained for level 4a, and during this

1.000

period, according to our morphometric results, M. grandis was dominant in the community (70% of Meriones specimens investigated). From the Holocene levels of EH2 and Guenfouda, our morphometric study did not evidence any M. shawii, only M. grandis. Consequently, if the two species are currently wellstructured geographically (occidental, M. grandis vs. oriental, M. shawii), it may not have always been the case in the past; there is evidence of M. shawii in Atlantic Morocco during the Late Pleistocene, before it was outcompeted by M. grandis during the Holocene. At EH2 and EM, the decrease of the M. shawii proportion though time (smaller size), versus the parallel increase of the M. grandis proportion (larger size), may also explain the slight tendency in size increase previously observed in the fossil populations of EH2 and EM over time (Fig. 8b). Some fossil specimens were also assigned to M. crassus and/or M. libycus in the Late Pleistocene levels of EH2 and EM, but always in low proportions (less than 6%)  which may represent the actual presence of these species, a “background noise” or a “statistical artifact”. Based upon palaeoecological studies (Stoetzel et al., 2011a), in the Late Pleistocene levels of EH2 and EM the environment was less humid and more open than in the EH2 Holocene level, where only M. grandis is represented. At Guenfouda, the proportion of M. crassus is significant (18.2%), as is M. libycus (9.14%), though to a lesser extent, and may be linked to the geographic location of this site in the semi-arid to arid eastern plateau of Morocco. M. libycus can still be found today in this area venot, 1986; Aulagnier et al., 2008c), (Fig. 1; Aulagnier and The which is not the case on the North Atlantic coast of Morocco, where the three other study sites are located. However, we must keep in

210

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Table 4 Form (shape þ size) differences between the studied modern and fossil molars of Meriones and Psammomys (MANOVA). P-values of the post hoc pairwise comparisons (with Bonferroni correction) are provided: a) main modern and fossil groups, b) detailed data by fossil level. A, B and C ¼ genotyped M. shawii/grandis specimens belonging to clades A, B and C; Foss ¼ fossil; EH2 ¼ El Harhoura 2; EM ¼ El Mnasra; Guenf ¼ Guenfouda.

A

B

C

Foss_EH2 Foss_EM Foss_Guenf Foss_Tamaris M.crassus M.grandis M.libycus M.shawii P.obesus

A B

61.632

C

<0.001 fail

Foss_EH2

<0.001 1.962

<0.001

Foss_EM

<0.001 7.632

0.020

<0.001

Foss_Guenf

2.594

fail

0.001

fail

Foss_Tamaris <0.001 5.531

2.377

<0.001 <0.001

<0.001

5.559

M.crassus

<0.001 11.406 <0.001 <0.001

<0.001

<0.001

<0.001

M.grandis

<0.001 64.443 17.443 <0.001

<0.001

26.311

<0.001

<0.001

M.libycus

<0.001 53.754 13.353 <0.001

<0.001

7.763

<0.001

<0.001

0.009

M.shawii

<0.001 50.208 8.270

<0.001

<0.001

6.719

<0.001

<0.001

<0.001

<0.001

P.obesus

<0.001 fail

19.392 <0.001

<0.001

41.148

<0.001

<0.001

<0.001

<0.001

Foss_EH2_c1

<0.001

Foss_EH2_c2 Foss_EH2_c3 Foss_EH2_c4a Foss_EH2_c5 Foss_EH2_c6 Foss_EH2_c7 Foss_EH2_c8 Foss_EM_c4 Foss_EM_c6 Foss_Guenf Foss_Tamaris

Foss_EH2_c1 Foss_EH2_c2

65.026

Foss_EH2_c3

10.523

24.456

Foss_EH2_c4a 61.233

65.588

33.462

Foss_EH2_c5

0.423

31.711

0.515

62.092

Foss_EH2_c6

0.005

0.275

0.007

4.624

0.433

Foss_EH2_c7

3.111

12.777

0.146

10.095

0.079

0.773

Foss_EH2_c8

0.134

5.889

0.030

15.914

0.113

0.904

63.579

Foss_EM_c4

fail

65.856

31.472

65.934

49.174

17.527

59.747

44.399

Foss_EM_c6

0.001

0.05

0.008

0.785

<0.001

0.002

18.139

5.354

37.218

Foss_Guenf

fail

fail

18.203

fail

0.416

0.069

27.143

3.383

fail

1.254

Foss_Tamaris

<0.001

<0.001

<0.001

<0.001

<0.001

<0.001

<0.001

<0.001

5.5652

<0.001

mind the low quantity of studied material for Guenfouda.

5.3. Meriones community evolution over time: climatic vs. anthropic impact We looked at the general microvertebrate composition of the different levels of EH2, which is the best documented site and the one with the longest chronological sequence (Stoetzel et al., 2010a, 2011a, 2012a). Meriones were dominant in all the Late Pleistocene levels (representing between 35% and 60% of the total small mammal communities), though they encountered a significant reduction during the Holocene (~24%), together with faunal changes (Stoetzel et al., 2011a). Since potential taphonomic biases have been ruled out, the observed modifications in small vertebrate composition may accurately reflect changes in the environment (Stoetzel et al., 2011a). In this study, we have shown that the Middle Holocene was also a key period concerning a shift in Meriones species distribution. Indeed, during the Late Pleistocene, both M. grandis and M. shawii occurred in Morocco; however, during the Holocene, M. shawii became extinct in Moroccan fossil records. The decrease in the relative proportion of Meriones and the disappearance of M. shawii from the Moroccan Holocene fossil assemblage are in agreement with palaeodemographic data obtained thanks to the genetic analyses of modern populations (Lalis et al., 2016), which highlighted a bottleneck in Moroccan populations of M. grandis during the Holocene, and possibly slightly earlier. The global palaeoclimatic data (e.g. Brun, 1989, 1991; Dupont and Hooghiemstra, 1989; Hooghiemstra et al., 1992; Petit-Maire, rou, 1997; DeMenocal, 2008; Whiting Blome et al., 1992; Le Houe

3.267

2012; Drake et al., 2013) and the palaeoecological studies performed at EH2 (Stoetzel et al., 2011a) have shown that the Late Pleistocene was characterized by an alternation of relatively arid and humid periods which accompanied changes in the landscape, but always in relatively open contexts (steppes or semi-wooded steppes, savanna-like environments). The Holocene was characterized by a particularly green landscape, with numerous wooded areas and fresh water ponds, which corresponds to the last climatic optimum, also known in Africa as the “green Sahara”. Our results strengthened the hypothesis previously exposed by Lalis et al. (2016), which showed the drastic impact of the last climatic optimum on Meriones populations. Today, the M. shawii/grandis complex is restricted to semi-arid and arid open areas, avoiding humid and forested regions (Aulagnier et al., 2008d). We can therefore suggest that during the humid period of the Middle Holocene, when Mediterranean forests expanded and the climate was more humid (e.g. Brun, 1989, 1991; Hooghiemstra et al., 1992; Le rou, 1997; Petit-Maire, 1999; DeMenocal et al., 2000; Houe Stambouli-Essassi et al., 2007; DeMenocal, 2008; Jalut et al., 2009; Nour el Bait et al., 2014), the steppic habitats, more suitable for Meriones, decreased drastically in the northern half of Morocco, leading to population collapses and changes in their geographic distribution. However, the M. shawii/grandis were not able to extend their range further south, where other Meriones species occurred (M. crassus, M. libycus), probably because they were less competitive in such arid environments. This may have led to a west-east re-organization of the M. shawii/grandis distribution, and it is probably during this period that M. shawii became restricted to Algeria, Tunisia and the arid eastern margins of Morocco. This is in

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211

Table 5 Classifications provided by Discriminant Function Analyses on molar size and shape variables. Groups used to compute the discriminant axes are species from the reference data set. Museum and fossil specimens were considered as supplementary specimens and attributed a posteriori in the reference groups. A

B

C

Reference data set (Classification Matrix) A 79 8 1 B 0 5 0 C 1 0 13 M.crassus 0 0 1 M.libycus 2 0 0 P.obesus 0 0 0 Total 82 13 15 Reference data set (Jackknifed Classification Matrix) A 65 17 3 B 5 0 0 C 1 0 12 M.crassus 0 0 1 M.libycus 4 0 1 P.obesus 0 0 1 Total 75 17 18 M. shawii/grandis museum specimens (n and % of predicted attribution) M.grandis_M&O 6 (60.0%) 3 (30.0%) 1 (10.0%) M.grandis_Bonn 100 (88.5%) 6 (5.3%) 5 (4.4%) M.grandis_Madrid 7 (100.0%) 0 (0.0%) 0 (0.0%) M.shawii_London 2 (66.7%) 0 (0.0%) 0 (0.0%) M.shawii_M&O 30 (53.6%) 5 (8.9%) 18 (32.1%) Fossil specimens (n and % of predicted attribution) Foss_EH2_c1 14 (82.4%) 3 (17.6%) 0 (0.0%) Foss_EH2_c2 18 (78.3%) 3 (13.0%) 1 (4.3%) Foss_EH2_c3 34 (79.1%) 2 (4.7%) 5 (11.6%) Foss_EH2_c4a 16 (64.0%) 4 (16.0%) 4 (16.0%) Foss_EH2_c5 47 (72.3%) 7 (10.8%) 11 (16.9%) Foss_EH2_c6 60 (62.5%) 16 (16.7%) 15 (15.6%) Foss_EH2_c7 29 (60.4%) 1 (2.1%) 18 (37.5%) Foss_EH2_c8 35 (55.6%) 5 (7.9%) 21 (33.3%) Foss_EM_c4 12 (70.6%) 2 (11.8%) 2 (11.8%) Foss_EM_c6 33 (44.0%) 7 (9.3%) 33 (44.0%) Foss_Guenf 7 (63.6%) 1 (9.1%) 0 (0.0%) Foss_Tamaris 69 (79.3%) 14 (16.1%) 4 (4.6%)

keeping with the M. shawii preference for more “arid” habits compared to M. grandis. Today, Meriones is one of the most abundant rodents in northwestern Africa, causing significant damages to cultivated fields and seed supplies (Adamou-Djerbaoui et al., 2010, 2013). In addition, M. shawii/grandis are mostly found in cultivated areas, and more rarely in natural environments (Zaime and Gautier, 1988; Stoetzel et al., 2010b, 2012b; Sekour et al., 2014; Denys et al., 2015). The oldest evidences of domestic plants and animals in North Africa date from approximately 6.5e7.5 ka BP in northern Morocco (KafTaht-El-Ghar: Ouchaou and Amani, 1997; Ballouche and Marinval, 2003; Ifri Oudadane: Morales et al., 2013) and Tunisia (Doukanet el Khoutifa: Mulazzani et al., 2016). But the productive economy (pastoralism, agriculture) seems to have been belated in other regions, following different patterns, pathways and timings (Mulazzani et al., 2016). In agreement with this assessment, neither domestic plants and animals, nor commensal rodents were evidenced in Neolithic level 1 of EH2 (~5.8 ka BP), located on the Atlantic coast near Rabat (Stoetzel et al., 2011a, 2014b). This level, therefore, precludes any anthropogenic impact on the environment. We can hypothesize that after a drastic decrease and species shift in the Middle Holocene, recorded in level 1 of EH2, Meriones adapted well to the new ecological niche offered by humans with the dispersal of agriculture during the Neolithic period. This means that, contrary to what is generally expected, recent environmental changes in synergy with anthropogenic pressure could have benefitted the development of some indigenous rodents, like M. grandis in Morocco and M. shawii in Algeria and Tunisia, although it created disequilibrium in the ecosystem. Consequently,

M.crassus

M.libycus

P.obesus

% correct

0 0 0 30 0 0 30

0 0 0 2 35 0 37

0 0 0 1 0 28 29

90 100 93 88 95 100 92

1 0 1 30 2 1 35

2 0 0 2 30 0 34

0 0 0 1 0 26 27

74 0 86 88 81 93 79

0 1 0 1 1

(0.0%) (0.9%) (0.0%) (33.3%) (1.8%)

0 1 0 0 2

(0.0%) (0.9%) (0.0%) (0.0%) (3.6%)

0 0 0 0 0

(0.0%) (0.0%) (0.0%) (0.0%) (0.0%)

0 0 2 0 0 4 0 2 0 1 2 0

(0.0%) (0.0%) (4.7%) (0.0%) (0.0%) (4.2%) (0.0%) (3.2%) (0.0%) (1.3%) (18.2%) (0.0%)

0 1 0 1 0 1 0 0 1 1 1 0

(0.0%) (4.3%) (0.0%) (4.0%) (0.0%) (1.0%) (0.0%) (0.0%) (5.9%) (1.3%) (9.1%) (0.0%)

0 0 0 0 0 0 0 0 0 0 0 0

(0.0%) (0.0%) (0.0%) (0.0%) (0.0%) (0.0%) (0.0%) (0.0%) (0.0%) (0.0%) (0.0%) (0.0%)

the impact of the human niche construction on the ecosystem, has not only been detrimental to the biodiversity (Boivin et al., 2016).

6. Conclusion and perspectives Our study has shown that cranial and dental markers obtained thanks to geometric morphometric analyses are more efficient than “classical” craniometric distances in distinguishing M. shawii and M. grandis specimens. By using a large number of genotyped and museum specimens, we can now assess that clades A and B correspond to M. grandis, occurring in Morocco, while clade C corresponds to M. shawii, occurring mainly in Algeria, Tunisia, and eastern Morocco. We have also evidenced confusion in the specific attribution of some museum specimens that can be now correctly re-attributed. According to genetic data (Lalis et al., 2016), M. shawii and M. grandis are very close species. This closeness may be related to an ongoing divergence, and/or reinstatement after isolation. However, the last hypothesis is not supported by our data, which indicates a co-occurrence of M. shawii and M. grandis in Morocco throughout the Late Pleistocene. Indeed, while currently only M. grandis seems to exist in Morocco, M. shawii did occur there in the past, though its numbers gradually reduced during the Late Pleistocene. A major event then seems to have occurred during the Middle Holocene which led to a demographic collapse (bottleneck) in the Moroccan populations of the shawii/grandis group, along with the disappearance of M. shawii from Morocco, most probably under climate pressure (last interglacial optimum). Since Meriones of the shawii/grandis complex are currently highly abundant in North Africa, especially in cultivated

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Fig. 9. Form differences (size þ shape) of the studied molars of Meriones and Psammomys, expressed by the three first axes of the DFA (performed on the 34 first axes of the PCA and the centroid size): a) Results of the DFA showing the distribution of the specimens from the reference data-set; b) Reattribution of the fossil and museum specimens; each symbol corresponds to a group mean, bracketed by the standard deviation; numbers refer to the archaeological levels for each site.

fields, this group would have then benefited from the new ecological niche driven by agriculture dispersal from the Neolithic onwards. It would be interesting to proceed with geometric morphometric analyses at the population level, in order to better understand whether or not there is any influence from climate, altitude, vegetation or other environmental factors on the cranial and dental morphology of modern Meriones shawii/grandis populations throughout North Africa, as was highlighted for other jird species (Tabatabaei Yazdi and Adriaens, 2011; Tabatabaei Yazdi et al., 2014); with a final objective to transpose this ecological information onto the past and track palaeoenvironmental changes, thanks to morphometric changes in Meriones, over time. It would also be interesting to perform 2D or 3D geometric morphometrics on tympanic bullae (well preserved on some fossil sites, such as EH2 and EM), whose size and shape are related to environmental conditions (arid/humid) and/or social purposes in rodents (Petter et al.,

1984; Momenzadeh et al., 2008; Momtazi et al., 2008). Furthermore, few sites other than EH2 and EM have recorded such a high abundance of microfaunal remains for the last climatic cycle in North Africa. The Holocene site of Guenfouda and the Late Pleistocene site of Tamaris tend to confirm the results obtained at EH2 and EM. But the study of other fossil sequences, which yielded large amounts of rodent remains dating to the Late Quaternary, remains necessary to validate (or not) our preliminary hypotheses and assumptions. Another dimension would be to include Algerian and Tunisian archaeological sites, in order to see if the Moroccan clades A and B were more largely distributed in the past, or if they represent true Moroccan endemics since the beginning of the Late Pleistocene. Our study confirms growing interest in comparing genetic and morphometric data for taxonomic and archaeological purposes to predict interesting perspectives. This also includes palaeogenetic data, as fossil DNA was recently found in the Meriones bones of the

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Fig. 10. Percentages of reattribution of fossil specimens to the reference groups based on Table 5.

EH2 sequence (Guimaraes et al., 2016). Aknowledgements This work was conducted as part of a post-doctoral fellowship (E.S.) funded by the LabEx BCDiv of the Mus eum national d'Histoire naturelle (MNHN, Paris, France). Modern trapped specimens were obtained within the framework of the ANR-09-PEXT-004 ‘MOHMIE’ Project (coord. C. Denys) in Morocco, and the Tassili 09mdu755 Project (coord. C. Denys), with help from Karim Souttou (Institut National Agronomique, Algiers) in Algeria. Specimens from museum collections came from the Mammals section of the Zoology and Comparative Anatomy unit of the Mus eum national d'Histoire naturelle (MNHN, Paris, France), the Natural History Museum (London, UK) and the Alexander Koenig Museum (Bonn, Germany). E.S. received support from the SYNTHESYS Project (http://www. synthesys.info/) which is financed by European Community Research Infrastructure Action under the FP7 “Capacities” Program. We especially thank Paula Jenkins and Roberto Portela Miguez from the Natural History Museum (London), Rainer Hutterer from the Zoologisches Forschungsmuseum Alexander Koenig (Bonn), and pez Errasquín from the Museo Josefina Barreiro and Elena Lo Nacional de Ciencias Naturales (Madrid) for their assistance in consultation and/or loan of specimens. We also thank MarieDominique Wandhammer (director of the Mus ee Zoologique of Strasbourg, France) for her help with research on the type specimen of M. shawii. E.S. also benefited from financing from the Merimee ) to take pictures of fossil Programme (coord. D. Grimaud-Herve specimens from Guenfouda at the IPHES, Tarragona (Spain). A huge thank you to Jordi Agusti and Juan-Manuel Lopez-Garcia for their welcome at the IPHES, and to Hassan Aouraghe (Science Faculty of Oujda, University Mohammed 1, Morocco) for allowing us to include the Guenfouda specimens in our study; and to Aicha Oujaa (INSAP, Rabat, Morocco) and Samir Zouhri (Science Faculty of Casablanca, University Aïn Chock, Morocco) for allowing us to include the Tamaris specimens. The fossil specimens from El Harhoura 2 and El Mnasra caves were recovered and studied within the mara Archaeological Mission (dir. framework of the El Harhoura-Te R. Nespoulet and M.A. El Hajraoui), under the administrative supervision of the Institut National des Sciences de l’Arch eologie et du Patrimoine (Rabat, Morocco) and financial support from the Minist ere des Affaires Etrang eres et du D eveloppement International (France) and the Minist ere de la Culture (Maroc). We thank Maxime

Cammas for his help with the maps, and Jill Cucchi (Editing and Translation Services) for copy-editing the English (financed by the LabEx BCDiv). Finally, a great thank to P. David Polly and a second anonymous reviewer for their constructive remarks that allowed to improve this manuscript. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.quascirev.2017.04.002. References  fe rences Adamou-Djerbaoui, M., Djelaila, Y., Denys, C., Baziz, B., 2010. Pre daphiques et infestation chez Meriones shawii (Mammalia, Rodentia) dans la e gion de Tiaret (Alge rie). Revue d’Ecologie (la Terre la Vie) 65, 63e72. re Adamou-Djerbaoui, M., Denys, C., Chaba, M.M., Djelaila, Y., Labdelli, F.,  gime alimentaire d’un rongeur nuisible (MerAdamou, M.S., 2013. Etude du re rie. Leban. Sci. J. 14 iones Shawii Duvernoy, 1842, Mammalia, Rodentia) en Alge (1), 15e32. oenvironnements (ChaAmani, F., Bougariane, B., Stoetzel, E., 2012. Faunes et Pale nath, A., Dibble, H. (Eds.), pitre XVI). In: El Hajraoui, M.A., Nespoulet, R., Debe histoire de la Re gion de Rabat-Te mara. Villes et Sites Arche ologiques du Pre Maroc. Partie 3: Grotte d’El Mnasra, vol. III, pp. 110e117. Andrews, P., 1990. Owls, Caves and Fossils. Natural History Museum Publications, London, p. 231. Aouraghe, H., Gagnepain, J., Haddoumi, H., El Hammouti, K., Ouchaou, B., Bailon, S., historique de Mestour, B., Oujaa, A., Bouzouggar, J., Billy, A., 2008. La grotte pre sultats (fouilles 2004-2007). Actes Guenfouda, Maroc oriental : les premiers re me Rencontre des Quaternaristes Marocains (RQM4), Oujda, 15-17 de la 4e novembre 2007, pp. 299e319. Aouraghe, H., Agusti, J., Ouchaou, B., Bailon, S., Lopez-Garcia, J.M., Haddoumi, H., El Hammouti, K., Oujaa, A., Bougariane, B., 2010. The Holocene vertebrate fauna from Guenfouda site, Eastern Morocco. Hist. Biol. 22 (1), 320e326. se d’Etat. Zooge ographie des Mammife res du Maroc : de Aulagnier, S., 1992. The cifique   l’e chelle re gionale, vol. 2. l’analyse spe a la typologie de peuplement a  Montpellier, p. 236. Universite venot, M., 1986. Catalogue des mammife res sauvages du Maroc. Aulagnier, S., The rie Zoologie, n 41, Rabat, p. 163. Travaux de l’Institut Scientifique, Se Aulagnier, S., Granjon, L., Amori, G., Hutterer, R., Krystufek, B., Yigit, N., 2008a. Meriones crassus. The IUCN Red List of Threatened Species 2008: e.T13161A3414954. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS. T13161A3414954.en. Downloaded on 28 April 2016. Aulagnier, S., Granjon, L., Amori, G., Hutterer, R., Krystufek, B., Yigit, N., Mitsain, G., 2008b. Meriones shawi. The IUCN Red List of Threatened Species 2008: e.T42666A10742674. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS. T42666A10742674.en. Downloaded on 28 April 2016. Aulagnier, S., Granjon, L., Shenbrot, G., Bukhnikashvili, A., 2008c. Meriones libycus. The IUCN Red List of Threatened Species 2008: e.T13164A3416049. http://dx. doi.org/10.2305/IUCN.UK.2008.RLTS.T13164A3416049.en. Downloaded on 28 April 2016. Aulagnier, S., Haffner, A.J., Mitchell-Jones, A.J., Moutou, F., Zima, J., 2008d. Guide des

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