Turkish Journal of Zoology Turk J Zool (2016) 40: 900-909 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1505-25

Patterns of skull variation in relation to some geoclimatic conditions in the greater orientalis (Rodentia, ) from

1, 1 2 Abderraouf BEN FALEH *, Hassen ALLAYA , Jean Pierre QUIGNARD , 3 1 Adel Abdel Aleem Basyouny SHAHIN , Monia TRABELSI 1 Marine Biology Unit, Faculty of Sciences of , Tunis El Manar University, Tunis, Tunisia 2 Laboratory of Ichthyology, Montpellier 2 University, Montpellier, France 3 Department of Zoology, Faculty of Science, Minia University, El Minia, Egypt

Received: 15.05.2015 Accepted/Published Online: 24.12.2015 Final Version: 06.12.2016

Abstract: The greater Egyptian jerboaJaculus orientalis is a member of the subfamily Dipodinae and widely distributed in Tunisia. Previous allozymic and karyotypic studies showed high gene flow and absence of genetic structuration. This study aimed to analyze the geographic patterns of cranial morphometric variation among populations of this species in Tunisia. The extent of morphometric patterns was addressed in a survey of 13 craniodental characters among 162 adult specimens collected from 12 localities within its distribution range by using univariate and multivariate statistics. Our results supported the existence of three morphotypes of this species comparable to three climatic zones, the northern, central, and southern regions of Tunisia. The probability of the correct classification of specimens was 99.38%, indicating significant degrees of variation in craniodental characteristics among these three morphotypes. In addition, we tested the effects of age, sex, geography, and some habitat variables (such as precipitation) on the size of the skull. The results showed that latitude and precipitation had significant effects on skull size. Hence, the pattern of morphometric variation is probably correlated with local environmental factors.

Key words: Classical morphometrics, Jaculus orientalis, geographic variation, Tunisia

1. Introduction et al., 2009, 2012b) or on the ecological and morphometric of the genus Jaculus (Erxleben, 1777) are widely parameters of some populations in North and Israel distributed in deserts and semiarid regions across the (Shenbrot, 2013). In Tunisia, detailed genetic analyses by Palearctic (Holden and Musser, 2005). Among them, the means of allozymic markers (23 loci) for six populations greater Egyptian jerboa Jaculus orientalis (Erxleben, 1777) with representative samples per population indicated is found throughout Morocco (Aulagnier and Thévenot, high gene flow and absence of genetic structuration (Ben 1986), (Kowalski and Rzebik-Kowalska, 1991), Faleh et al., 2009). In addition, Ben Faleh et al. (2010a) Tunisia (Vesmanis, 1984), (Ranck, 1968; Hufnagl, karyotyped 12 specimens of J. orientalis and reported that 1972), and Egypt, particularly in the northern and all of the individuals examined had a diploid number (2n southwestern parts of Sinai and the western Mediterranean = 48) and NFa varied from 84 to 88. This variation did not coastal desert (Osborn and Helmy, 1980; Hoath, 2003), seem to be geographically structured, as different NFa with a small extension in Israel (Qumsiyeh, 1996). values were observed among populations of the same According to Amori et al. (2008) and Gharaibeh (1997), locality. Moreover, phylogeography study of J. orientalis its distribution is interrupted in Libya by the arid lowlands in using the cytochrome b (cytb) gene (Ben and mountainous plateau (reaching an altitude of 868 Faleh et al., 2012b) showed strong genetic subdivision m at Al Jabal al Akhdar) and by the Nile Delta in Egypt. into three areas along the west-east axis that corresponded In Tunisia, this species inhabits the northern, central, to: 1) Morocco and western Algeria; 2) eastern Algeria, and southeastern parts of the country (Vesmanis, 1984; Tunisia, and western Libya; and 3) eastern Libya and Gharaibeh, 1997; Ben Faleh et al., 2012b). Egypt. Recently, Shenbrot (2013), based on the analysis Despite the wide distribution of J. orientalis, there are of 14 cranial measurements among 99 specimens of J. few studies that have focused on the genetic variation orientalis collected from Egypt, Libya, Morocco, and within and among populations (Shahin, 2003; Ben Faleh Israel, claimed that there are three morphologically well- * Correspondence: [email protected] 900 BEN FALEH et al. / Turk J Zool differentiated population groups within this geographic The present study was undertaken to investigate the range. size variation of the skull among populations of the greater The documentation of geographic variation of the skull Egyptian jerboa J. orientalis in Tunisia by using classical in relation to climatic and habitat variables is fundamental morphometric analyses of some craniodental parameters for defining boundaries of independent evolutionary units in order to analyze intra- and interpopulation variation in in nature (Renaud and Millien, 2001). Earlier studies of the size of the skull. geographic variation in addressed variation in morphological characters (Monteiro et al., 2003; Bronner 2. Materials and methods et al., 2007; Jansa et al. 2008; Ben Faleh et al., 2012a, 2013). A total of 162 individuals of the greater jerboa J. orientalis Morphometric approaches have been shown to be (86 males, 76 females) were collected from 12 localities powerful to analyze skull variability among rodents in Tunisia between April 2012 and August 2013 (Figure species (Chimimba, 2001; Nicolas et al., 2008; Lalis et 1; Table 1). In the present investigation, we divided our al., 2009; Bezerra and De Oliveira, 2010; Ben Faleh et al., study area into three climatic regions (northern, central, 2012a; Bohoussou et al., 2014). To date, no morphometric and southern) based on the Köppen–Geiger system (Peel studies have reported on the skull variability of J. orientalis et al., 2007). According to Sicilia et al. (2007) and Amor et in Tunisia. al. (2009), the annual precipitation in the northern region

Isohyet

Figure 1. A map showing the three climatic regions from which the 162 samples of Jaculus orientalis were collected in Tunisia, with isohyets indicating the average annual rainfall measured in millimeters (mm year–1). Main : B- arid, C- warm temperate. Precipitation: W- desert, S- steppe, s- summer dry. Temperature: a- hot summer, h- hot arid.

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Table 1. The localities and samples sizes (n) from which J. orientalis samples were collected in Tunisia.

Mean of precipitation Altitude Region Locality Latitude Longitude n (mm year–1) (m) North Mjez El Beb 36°39′07″N 9°36′26″E 581 266 11 El Khouat 36°05′25″N 9°22′12″E 423 426 12 Mateur 37°02′23″N 9°39′35″E 600 65 8 Total 31 Central Boumerdes 35°30′11″N 10°44′81″E 282 98 17 Sbeitla 35°13′60″N 9°08′28″E 335 525 13 Amra 34°25′48″N 8°47′56″E 175 297 18 Haidra 35°34′01″N 8°26′31″E 449 737 14 Menzel Chaker 34°56′92″N 10°23′96″E 200 105 13 Total 75 South Gabes 33°53′12″N 10°05′36″E 190 4 13 Medenine 33°21′45″N 10°30′91″E 175 93 15 Matmata 33°32′97″N 9°57′62″E 180 600 15 Ben Gardene 33°08′21″N 11°13′14″E 175 11 13 Total 56

(Mediterranean area: Csa) ranges from 400 and 600 mm Age classes were defined based upon molar wear stages year–1 in the east and 800 to 1500 mm year–1 in the west, as: Stage C0, no upper M3 is erupted; Stage C1, upper M3 and the average annual temperature is between 17 and 19 is erupted but not worn; Stage C2, cusps are still visible °C. In the central region (steppe plain [Sahel] and plateau on all molars and link between first and second lobe of [Tell]: BSh), the annual precipitation value ranges from 200 the upper M3 is very narrow; Stage C3, the longitudinal to about 600 mm year–1 and the average annual temperature link between first and second lobe of upper M3 is larger varies between 15 and 19 °C. However, in the southern and, in general, wider on the upper M12; Stage C4, the region (desert zone: BWh), the annual precipitation longitudinal link is very wide but cusps remain visible on ranges from 75 to 200 mm year–1 and the average annual the other molars (Ben Faleh et al., 2013). temperature fluctuates between 19 and 22 °C (see Figure 1 Thirteen craniodental measurements were taken for details). following Ben Faleh et al. (2010b, 2012a) using digital It is noteworthy that the northern part of the eas­ternmost calipers (RUPAC, Italy). Values were approximated to Atlas Mountains (Medjerda Mountains), the Medjerda the nearest 0.01 mm and include: greatest length of Rivers, and the Chott el Jerid region constitute obvious skull (GRLS), length of palatal foramen (PAFL), smallest geographical barriers for many taxa in Tunisia (Millington interorbital width (INTE), zygomatic breadth on the et al., 1989; Ben Othmen et al., 2009; Abdallah et al., 2012; zygomatic process of the squamosal (ZYGO), length of Farjallah et al., 2012). The northern region comprised the maxillary tooth row (UPTE), greatest breadth of nasals populations of Mateur, Medjez el-Beb, and El Khouat. In (BNAS), greatest length of nasals (LNAS), length of this region, most of the habitats of J. orientalis are mountains mandibular tooth row (LOTE), length of auditory bulla with low altitude. The central zone included the populations (BULL), greatest breadth of braincase (BRCA), mandible of Haidra, Sbeitla, Menzel Chaker, Amra, and Boumerdes height at angular process (PCPA), postpalatal width and the habitat is characterized by plains and shrub steppe. (PPW), and lower jaw length (LJL). The southern region incorporated the populations of Gabes, First we performed analyses of variance (ANOVA) Medenine, Matmata, and Ben Gardene and most of the and multiple analyses of variance (MANOVA) to test the habitats are desert steppe, rocky desert, sand-dune desert, influence of sexual dimorphism, age, and geographical and salt-lakes (see Figure 1 and Table 1 for details). variables (precipitation) on the size of the skull. The

902 BEN FALEH et al. / Turk J Zool significance of differences among the three climatic 3. Results regions was tested by means of one-way ANOVA. The 162 skulls measured, corresponding to individuals When statistically significant differences were detected, of age classes ranging from C2 to C4, were used in the Scheffé (1959) post hoc tests were used to determine the statistical analyses. MANOVA showed that the craniodental statistically nonsignificant subsets. measurements were not significantly correlated with either We also conducted principal component analysis age (Wilks’ lambda = 0.83; P = 0.39) or sex (Wilks’ lambda (PCA) for the log-transformed data of morphometric = 0.93; P = 0.63); therefore, we continued to treat the whole variables. The first component was highly loaded to data set as a pooled sample. show the size effect. Therefore, the remaining principal Additionally, there was a size gradient for the 13 components (PCs) were used as variables in discriminant craniodental measurements between populations; the function analysis (DFA). Stepwise selection (F for entry: lowest values were shown in the northern specimens, 13.92; for removal: 12.81) was used to obtain the subset of while the largest values were those of the southern region those variables that provided the best discrimination. (Table 2). Statistically significant differences between ANOVA, including geographic location as a factor for geographically variable regions were evaluated by means all the analyzed variables, showed that all the morphometric of Mahalanobis distances and Wilks’ lambda statistics variables differed significantly between populations of the (Klecka, 1980). Correlations between measurements of three climatic regions (Wilks’ lambda = 0.015; P < 0.001). the DFA were computed to establish the contribution of the given variable for the total among-group variation. In These results were confirmed by using Scheffé post hoc addition, regressions were used to explore the correlations tests (Table 3). between log data and latitude, longitude, altitude, and In PCA, the first PC accounted for 89.13% of the total variation and was positively correlated with all linear precipitation. All multivariate analyses were based on log10- transformed cranial morphometric data. All statistical dimensions of skull size, indicating that there is a skull analyses of morphometric parameters were performed size effect on the morphometric characters of the analyzed using PAST 1.81 (Hammer et al., 2001) and Statistica v.10 climatic regions (Table 4). The second and third PCs (StatSoft, Inc., www.statsoft.com). explained only 5.27% of the total variation. In addition, the

Table 2. The 13 craniodental measurements (in mm) of the 162 samples of J. orientalis collected from the northern, central, and southern regions in Tunisia.

Geographic region Northern (n = 31) Central (n = 75) Southern (n = 56) Variables Mean ± SD Range Mean ± SD Range Mean ± SD Range PAFL 5.61 ± 0.09 5.45–5.81 6.21 ± 0.15 5.71–6.45 6.71 ± 0.16 6.18–6.99 BNAS 7.18 ± 0.01 7.09–7.43 7.41 ± 0.04 7.31–7.50 7.76 ± 0.16 7.16–7.99 LNAS 12.81 ± 0.09 12.64–12.99 13.24 ± 0.12 12.86–13.47 13.65 ± 0.20 13.15–13.98 INTE 9.67 ± 0.12 9.47–9.88 10.24 ± 0.11 9.78–10.5 10.71 ± 0.14 10.38–10.99 PPW 17.84 ± 0.10 17.61–17.99 18.21 ± 0.15 17.78–18.50 18.69 ± 0.15 18.12–18.98 LJL 24.61 ± 0.15 24.32–24.91 25.17 ± 0.14 24.71–25.45 25.72 ± 0.18 25.11–25.99 LOTE 6.56 ± 0.12 6.17–6.81 7.00 ± 0.13 6.38–7.32 7.70 ± 0.18 7.11–7.99 PCPA 8.42 ± 0.21 8.12–8.77 9.15 ± 0.16 8.71–9.53 9.65 ± 0.16 9.16–9.93 BULL 12.12 ± 0.07 12.00–12.35 12.60 ± 0.15 12.11–12.88 12.83 ± 0.12 12.47–12.99 ZYGO 26.74 ± 0.07 26.61–26.88 27.24 ± 0.13 26.71–27.5 27.71 ± 0.15 27.13–27.96 BRCA 17.72 ± 0.13 17.45–17.99 18.23 ± 0.12 17.82–18.49 18.65 ± 0.21 18.12–18.93 UPTE 6.21 ± 0.06 6.09–6.36 6.63 ± 0.13 6.27–6.91 7.06 ± 0.11 6.82–7.27 GRLS 36.94 ± 0.02 36.90–36.99 37.1 ± 0.13 36.45–37.43 37.71 ± 0.18 37.17–37.92

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Table 3. Results of ANOVA. The a posteriori Scheffé test was used to evaluate the significant differences between the northern, central, and southern regions of Tunisia.

Results of Scheffé test Region Northern and central Northern and southern Central and southern Variables P (significance) P (significance) P (significance) PAFL 0.00 (**) 0.00 (**) 0.03 (*) BNAS 0.01 (**) 0.01 (**) 0.00 (**) LNAS 0.00 (**) 0.00 (**) 0.0003 (***) INTE 0.00 (**) 0.03 (*) 0.00 (**) PPW 0.005 (**) 0.00 (**) 0.00 (**) LJL 0.00 (**) 0.00 (**) 0.00 (**) LOTE 0.0001 (***) 0.00 (***) 0.00 (**) PCPA 0.00 (**) 0.00 (**) 0.00 (**) BULL 0.002 (***) 0.04 (**) 0.0002 (***) ZYGO 0.03 (*) 0.00 (**) 0.01 (*) BRCA 0.00 (**) 0.00 (**) 0.000000 (***) UPTE 0.000000 (***) 0.00 (**) 0.00 (**) GRLS 0.004 (**) 0.02 (**) 0.01 (*)

*P < 0.05; **P < 0.01; ***P < 0.001.

Table 4. Principal component (PC) loadings of the 13 morphometric characters.

Variables PC1 PC2 PC3 PAFL 0.503 0.519 –0.06 BNAS 0.229 –0.166 0.01 LNAS 0.176 0.07 –0.231 INTE 0.284 0.07 –0.087 PPW 0.133 –0.04 –0.005 LJL 0.123 0.033 0.652 LOTE 0.463 –0.722 –0.275 PCPA 0.380 0.335 –0.028 BULL 0.15 0.129 –0.083 ZYGO 0.099 0.02 0.025 BRCA 0.140 0.01 –0.609 UPTE 0.368 –0.181 0.004 GRLS 0.06 –0.06 0.231

904 BEN FALEH et al. / Turk J Zool length of the palatal foramen (PAFL) had a high loading skull size parameters varied significantly with latitude and on the second axis, while the lower jaw length (LJL), on the precipitation (Table 5). contrary, had a high loading on the third axis, indicating the presence of different measurements among the three 4. Discussion geographic regions (Table 4). Our approach allowed, for the first time, to describe the In DFA, two discriminant functions (DFs) were skull variability of J. orientalis populations in Tunisia. All produced and both functions made significant morphometric analyses (ANOVA, MANOVA, and DFA) contributions to distinguishing morphological variation clearly showed that the 12 populations of J. orientalis among the three climatic regions (P < 0.001) (Figure examined in this study were distributed among three 2). The first DF accounted for 96% of the total variation morphotypes, which showed high levels of morphometric between populations of the three climatic regions. The factor structure matrix indicated that LOTE was the most Table 5. Regressions of the different skull size parameters in positively correlated variable on the first DF, while GRLS relation to the environmental factors in the three geographic was the most positively correlated variable on the second regions (the northern, central, and southern) in Tunisia. axis. Stepwise forward DFA resulted in 99.38% correct classification for the samples in the three climatic regions. Factors Log data (significance) Squared Mahalanobis distances between populations of the three geographic regions were 63.45 between Latitude 6.311e-5 (***) populations from the northern and central regions, 241.47 Longitude 0.5614 (NS) between those from the northern and southern regions, and 65.89 between those from the central and southern Altitude 0.07845 (NS) regions. Precipitations 7.312e-03 (***) Regressions were performed based on log data versus latitude, longitude, altitude, and precipitation. All of the ***P < 0.001; NS: not significant.

Figure 2. Plot of individuals in discriminant space obtained from a three-climatic regions stepwise discriminant function analysis (DFA) using cranial variables. Only the first two discriminant functions are plotted (Wilk’s λ = 0.150, F (26.294) = 80.740, P < 0.001).

905 BEN FALEH et al. / Turk J Zool differences in Tunisia. The patterns of variability were of anatomic forms could partition their food resources by consistent with the variation in size of the skull among the developing local adaptations to different habitats (Lalis three climatic regions (northern, central, and southern). et al., 2009). As a result, several morphometric studies However, the observed variability among populations of demonstrated significant geographical differences in the these climatic regions was not related to age, although cranial shape of rodents occupying distinct ecological the current samples did not present skulls with initial biomes (Taylor et al., 2005). Numerous studies have shown stages C0 and C1 of age classes. This variability was also the presence of local differentiation in the size and shape of not dependent upon sex where the sex ratio was quite the skull at the population level in (Polly, 2007; equilibrated (86 males versus 76 females). The absence of Lalis et al., 2009). The differences of skull shape between significant variability between populations based upon age the three morphotypes assigned here could perhaps reflect and sexual dimorphism was also reported in numerous the local adaptation without genetic structuring, i.e. rodents such as Jaculus jaculus (Ben Faleh et al., 2010b, morphological differentiation in the presence of gene flow 2010c, 2013), Mastomys natalensis (Lalis et al., 2009), (Lieberman et al., 2004; Lalis et al., 2009). Rattus rattus (Ben Faleh et al., 2012a) and Malacomys Our results demonstrate that the effects of edwardsi (Bohoussou et al., 2014). change as well as the morphological plasticity and natural The 12 J. orientalis specimens that were previously selection on morphological traits have occurred over short karyotyped by Faleh et al. (2010a; 2n = 48 and NFa varies periods in natural populations of J. orientalis. Indeed, the from 84 to 88) have different skull morphometrics in the fact that phenotypic characters (e.g., body size) may evolve three climatic regions (or morphotypes). This variation in an undirected, Brownian motion pattern is consistent did not seem to be geographically structured, as different with the randomly varying selection in areas with different NFa values are observed among populations of the same environmental pressures including different ecological locality. Similar variations of NFa are reported in numerous parameters such as those present in the different habitats African rodents (Volobouev et al., 2002; Dobigny et al., of J. orientalis (Wolf et al., 2009). In this way, our findings 2010). Such polymorphism, which does not affect the are congruent with the high morphometric variability that diploid number, is often associated with rearrangements appeared among populations of the lesser jerboa Jaculus such as pericentric inversions or heterochromatin jaculus from Tunisia (Ben Faleh et al., 2013) using the addition (Ben Faleh et al., 2010a). This divergence same morphometric characters. between chromosomal and morphometric data analysis of Body size as well may play an important role in the J. orientalis populations examined herein is probably due adaptive profile of the species and is sometimes subjected to different ecological circumstances between the three to rapid evolutionary change (Kuncová and Frynta, 2009). climatic regions. As speculated by Lalis et al. (2009), the Thus, many hypotheses are cited to explain this variation variability in the cranial characters could preferentially by means of a combination of climatic factors (James 1970), reveal a rapid and local adaptation. metabolism rate, mating success, cost of transport, and Detailed genetic analyses of 23 loci in six populations competition (Ben Faleh et al., 2012a). The present results of J. orientalis from Tunisia indicated that the genetic indicate that the variation of skull size among J. orientalis diversity expressed by observed heterozygosity (Hobs), populations was clearly associated with an environmental percentage of polymorphic loci (P), and number of alleles gradient. Other authors assumed that the shape and skull per locus (A) seems to be correlated with the populations’ differences among populations might not be attributed to density. The mean value of FST between populations is static allometric differences (Duarte et al., 2000; Reis et al., apparently low (0.0019) and accounts for high gene flow 2002; Klingenberg, 2013). and an absence of genetic structuration. This is congruent Additionally, regressions for latitude and precipitation with the present morphometric data as well as the data were significant in the whole data set. The major trend of reported on numerous other species (Ben Faleh size variation observed was associated with a latitudinal et al., 2010b; Nicolas et al., 2010; Kovaleva et al., 2012; gradient, as previously reported for other rodents (Reis Ledevin and Millien, 2013). However, we concluded that et al., 2002; Macholán et al., 2008; Martínez and Di Cola, allozymic variability may reflect phenotypic plasticity at 2011). In this context, significant effect of precipitations the cellular level (Storz et al., 2013), perhaps as a response and latitude on the skull of the black rat Rattus rattus from to nutritional stress (Denver and Crespi, 2006). Tunisia were also reported (Ben Faleh et al., 2012a). The In summary, with of the analyses of 13 craniodental three morphotypes recognized herein seem to correspond traits, it was found that there are three distinct morphotypes to the Tunisian specimens of J. orientalis that belong to the living in different environments. Therefore, we could raise second clade (eastern Algeria, Tunisia, and western Libya) the hypothesis of local and morphological adaptation obtained in a phylogeographical study of J. orientalis in without genetic structuring. It is known that differences North Africa (Ben Faleh et al., 2012b).

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The high morphometric divergence between In conclusion, the ANOVA, MANOVA, and DFA populations of J. orientalis collected from the northern, results of this study clearly demonstrate that the three central, and southern regions in Tunisia is in agreement climatic regions characterizing the with the published data on this species from North Africa correspond to three morphotypes of J. orientalis. The and Israel (Shenbrot et al., 2013). In this investigation, three analysis also revealed an extensive variation in skull size among populations of the three morphotypes, which was morphologically well-differentiated groups of populations attributed to environmental variation. are demonstrated between the highly geographically isolated and deeply ecologically divergent populations in Acknowledgments the western and eastern parts of the range and between The authors are grateful to all people who participated the geographically weakly isolated and ecologically similar in the collection of samples. We also thank the two Egypt/Libya and Israel/Sinai populations (Shenbrot et al., anonymous reviewers who reviewed our paper for their 2013) . very useful and informative comments.

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