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Morphological and Genetic Differentiation of Eremina Desertorum (Gastropoda, Pulmonata, Helicidae) in Egypt

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Morphological and Genetic Differentiation of Eremina Desertorum (Gastropoda, Pulmonata, Helicidae) in Egypt Zoologica Scripta Morphological and genetic differentiation of Eremina desertorum (Gastropoda, Pulmonata, Helicidae) in Egypt REHAM F. ALI,MARCO T. NEIBER,FRANK WALTHER &BERNHARD HAUSDORF Submitted: 7 May 2015 Ali, R.F., Neiber, M.T., Walther, F. & Hausdorf, B. (2016). Morphological and genetic dif- Accepted: 29 June 2015 ferentiation of Eremina desertorum (Gastropoda, Pulmonata, Helicidae) in Egypt. —Zoologica doi:10.1111/zsc.12134 Scripta, 45,48–61. To understand the processes that result in morphological and genetic diversity, we studied the differentiation of the land snails Eremina d. desertorum and Eremina desertorum irregularis in the deserts of northern Egypt. These two taxa are differentiated with regard to shell size and shape and are separated by a narrow hybrid zone west of Alexandria. The lack of differ- ences in the genitalia and the lack of reciprocal monophyly of the mitochondrial haplotypes of E. d. desertorum and E. desertorum irregularis support their classification as subspecies rather than distinct species. Low genetic distances indicate that the differentiation is proba- bly less than half a million years old. The genetic data indicate a population expansion in agreement with other evidence that the Nile region in northern Egypt was more humid well into historical times than today. Shell size and shape are correlated with a climatic gra- dient from cooler and more humid conditions along the Mediterranean coast to arid and hot conditions in the interior. The decrease of body size with decreasing precipitation and increasing temperature might be explained by limited time for food intake in the more arid regions. The shape differences between the taxa are partly an indirect consequence of selec- tion for body size, but are also directly affected by selection for reduction of aperture size. Corresponding author: Bernhard Hausdorf, Zoological Museum, Centre of Natural History, University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany. E-mail: [email protected] Reham F. Ali, Department of Zoology and Agricultural Nematology, Faculty of Agriculture, Cairo University, Post Box 12613, Gammaa Street, Giza, Egypt. E-mails: [email protected] Marco T. Neiber, Frank Walther, and Bernhard Hausdorf, Zoological Museum, Centre of Natu- ral History, University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany. E-mails: [email protected], [email protected] Introduction mental gradient of decreasing precipitation and increasing A central goal of evolutionary biology is the understanding temperature from the Mediterranean coast inland. of the processes that result in morphological and genetic Eremina Pfeiffer, 1855 includes large desert snails that are diversity. Land snails were often used as model organisms distributed through northern Africa from the Cape Verde for evaluating the roles of selection and history in the Islands, Mauretania and Morocco eastwards to the Sinai origins of biodiversity (Davison 2002). In particular notable Peninsula, the Gaza strip and southern Israel, and south- are the classical studies of Cepaea that nicely illustrated the wards to Somalia (Hesse 1915; Kaltenbach 1934, 1942; Lla- action and effects of natural selection on shell phenotypes bador 1960; Verdcourt 1960; Groh 2005; Heller 2009). The in the wild (Cain & Sheppard 1954). However, patterns of genus is represented by E. advena (Webb & Berthelot, 1833) diversity are often difficult to detect and to understand if and E. myristica (Shuttleworth, 1852) (Groh 2005) on the they are influenced by a host of historical and environmen- Cape Verde Islands and by E. dillwyniana (Pfeiffer, 1851) tal factors in complex ecosystems (e.g. Fiorentino et al. (=Helix duroi Hidalgo, 1886 = E. linanprietoae Cossignani & 2008). Therefore, we have studied the morphological and Galindo, 2012) and E. vermiculosa (Morelet, 1874), of which genetic differentiation of the land snail Eremina desertorum E. inexpectata Llabador, 1960 is considered a subspecies (Forsskal, 1775) in a manageable ecosystem, the deserts of (Kittel 2012), in Northwest Africa (Llabador 1960). In northern Egypt, which is dominated by a steep environ- Northeast Africa, E. desertella (Jickeli, 1872) is found along 48 ª 2015 Royal Swedish Academy of Sciences, 45, 1, January 2016, pp 48–61 R. F. Ali et al. Differentiation in Eremina desertorum in Egypt the coast of the Red Sea from Sudan to Cape Guardafui in In this study, we examined the morphological and Somalia (Verdcourt 1960; records from northern Egypt genetic differentiation of the two main taxa of this (Pallary 1909) refer to small forms of E. desertorum) and is complex, E. d. desertorum (Fig. 1A–C) and E. desertorum perhaps introduced at the Red Sea coast of Arabia (Neubert irregularis (Figs 1D–E and 2), and its causes. Eremina d. de- 1998). The most diverse complex of Eremina taxa is found in sertorum differs from E. desertorum irregularis in several Egypt and adjacent Mediterranean regions, westwards characters (Kaltenbach 1934), but all show considerable through Libya to southern Tunisia and eastwards through variation within these taxa so that none of these characters the Sinai Peninsula to the Gaza strip and southern Israel. alone can be considered decisive. The shells of E. d. deser- Some authors included all these forms in a single, highly torum are usually smaller and more depressed than those of variable species, E. desertorum (e.g. Hesse 1915; Biggs 1959), E. desertorum irregularis. In the latter, the umbilicus is whereas others classify E. irregularis (Ferussac, 1821) (=Helix closed, whereas there is sometimes a narrow umbilicus in hasselquisti Ehrenberg, 1831 = Helix ehrenbergi Roth, 1839) E. d. desertorum. The shells of E. d. desertorum are often and E. kobelti (Westerlund, 1889) as separate species rib-striated, whereas those of E. desertorum irregularis are (Kaltenbach 1934, 1942; Heller 2009). smoother and only irregularly wrinkled. Some specimens A B C Fig. 1 Shell variability of Eremina desertorum in Egypt. —A. Eremina d. desertorum, Cairo (ZMH 45035). —B. D Eremina d. desertorum, El Alamein 100 km toward Cairo (ZMH 79772). —C. Eremina d. desertorum, El Alamein 65 km toward Cairo (ZMH 79776). —D. Eremina desertorum irregularis, Borg El Arab (ZMH 79768). —E. Eremina desertorum irregularis, Ezbet El-Sheik Sabir area S of El Hammam (ZMH 79769). Scale bar: E 10 mm. ª 2015 Royal Swedish Academy of Sciences, 45, 1, January 2016, pp 48–61 49 Differentiation in Eremina desertorum in Egypt R. F. Ali et al. of E. desertorum irregularis have a more or less wide, Cairo, because this area is especially interesting for the wrinkled accretion at the peristome (Fig. 2B–C), which interpretation of the relationship of these two taxa. does not occur in E. d. desertorum. Differences in the size Kaltenbach (1934) mentioned a wide hybrid zone between of the radula, the number of radular teeth and the number E. d. desertorum and E. desertorum irregularis with a high of ridges on the jaw (Kaltenbach 1934) are apparently percentage of specimens of intermediate shell size between correlated with the body size. Hesse (1915) has not found 110 and 190 km north-west of Cairo. In contrast, anatomical differences between E. d. desertorum from Cairo Kaltenbach (1942) reported an abrupt transition between and E. desertorum irregularis from Ar Raml in Alexandria. E. desertorum irregularis and E. d. desertorum about 20– Eremina d. desertorum occurs in the interior of northern 30 km south of the Mediterranean coast, where he found a Egypt, approximately from Alexandria southwards to form of E. desertorum that he described as E. desertorum Fayyum and eastwards to the Gaza strip and Israel, whereas mariuti. Therefore, we sampled Eremina populations along E. desertorum irregularis is distributed along the Mediter- the Mediterranean coast region of Egypt and along a ranean coast from southern Tunisia through Libya transect from the Mediterranean coast toward Cairo. We eastwards to Alexandria and occurs also south-east of analysed variables of the shell and the genitalia with statis- Cairo. We focus on the region between Alexandria and tical methods that allow the separation of size and shape A BC D F Fig. 2 Shell variability of Eremina desertorum irregularis in Egypt. —A. Specimen without peristomal accretion, El Dabaa (ZMH 79759). —B. Specimen with E H peristomal accretion, El Dabaa (ZMH 79759). —C. Specimen with wide peristomal accretion, El Sallum 183 km toward Mersa Matruh (ZMH 79767). —D–E. El Dabaa, recent (ZMH 79759). —F. El Dabaa, (sub-)fossil (ZMH 79872). —G–I. Mersa Matruh 180 km toward El G I Alamein (close to El Alamein) (ZMH 79764). Scale bar: 10 mm. 50 ª 2015 Royal Swedish Academy of Sciences, 45, 1, January 2016, pp 48–61 R. F. Ali et al. Differentiation in Eremina desertorum in Egypt components. Furthermore, we analysed the variation of biologically meaningful climatic variables (BIOCLIM data mitochondrial DNA in this region to characterize the two set; Nix 1986) were acquired from the WorldClim database taxa and their relationships and to investigate the causes of (http://www.worldclim.org; ca. 1 km2 resolution; Hijmans the morphological and genetic variation. et al. 2005). Precipitation of the driest month is 0 mm for all stations. Thus, this variable was not considered. Because Material and methods some of the other variables are highly correlated, we Study area and sampling converted them into a set of linearly uncorrelated variables We sampled Eremina populations along the Mediterranean using principal component analysis with varimax rotation as coast region of Egypt and along a transect from the implemented in the program SPSS Statistics version 21 Mediterranean coast toward Cairo (Fig. 3; see Supporting (IBM, Armonk, NY, USA). We investigated the influence information, Table S1). Specimens were killed in boiling of the environmental principal components on shell and water and preserved in 70% ethanol. Voucher specimens genital variables using stepwise multiple linear regression are kept in the Zoological Museum of the University Ham- analyses with SPSS. burg in Germany (ZMH).
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