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Out of Africa: Demographic and Colonization History of the Algerian Mouse (Mus Spretus Lataste)

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Out of Africa: Demographic and Colonization History of the Algerian Mouse (Mus Spretus Lataste) Heredity (2019) 122:150–171 https://doi.org/10.1038/s41437-018-0089-7 ARTICLE Out of Africa: demographic and colonization history of the Algerian mouse (Mus spretus Lataste) 1 1,2 3 4 5 6 Aude Lalis ● Stefano Mona ● Emmanuelle Stoetzel ● François Bonhomme ● Karim Souttou ● Ali Ouarour ● 7 1 1 Stéphane Aulagnier ● Christiane Denys ● Violaine Nicolas Received: 13 November 2017 / Revised: 28 February 2018 / Accepted: 16 April 2018 / Published online: 23 May 2018 © The Genetics Society 2018 Abstract North Africa is now recognized as a major area for the emergence and dispersal of anatomically modern humans from at least 315 kya. The Mediterranean Basin is thus particularly suited to study the role of climate versus human-mediated changes on the evolutionary history of species. The Algerian mouse (Mus spretus Lataste) is an endemic species from this basin, with its distribution restricted to North Africa (from Libya to Morocco), Iberian Peninsula and South of France. A rich paleontological record of M. spretus exists in North Africa, suggesting hypotheses concerning colonization pathways, and the demographic and morphologic history of this species. Here we combined genetic (3 mitochondrial DNA loci and 18 1234567890();,: 1234567890();,: microsatellites) and climatic niche modeling data to infer the evolutionary history of the Algerian mouse. We collected 646 new individuals in 51 localities. Our results are consistent with an anthropogenic translocation of the Algerian mouse from North Africa to the Iberian Peninsula via Neolithic navigators, probably from the Tingitane Peninsula. Once arrived in Spain, suitable climatic conditions would then have favored the dispersion of the Algerian mice to France. The morphological differentiation observed between Spanish, French and North African populations could be explained by a founder effect and possibly local adaptation. This article helps to better understand the role of climate versus human-mediated changes on the evolutionary history of mammal species in the Mediterranean Basin. Introduction Electronic supplementary material The online version of this article The Mediterranean Basin, between southern Europe and (https://doi.org/10.1038/s41437-018-0089-7) contains supplementary North Africa, is particularly suited to study the role of cli- material, which is available to authorized users. mate versus human-mediated changes on the evolutionary * Violaine Nicolas history of species for several reasons. First, this area has [email protected] yielded a rich paleontological record allowing a better understanding of the morphological evolution of small 1 Institut de Systématique, Evolution, Biodiversité, ISYEB - UMR 7205 - CNRS, MNHN, UPMC, EPHE, Sorbonne Universités, mammal species and of community assemblages over time Paris, France in relation to Quaternary climatic changes (Stoetzel 2013). 2 EPHE, PSL Research University, Paris, France Second, North Africa is now recognized as a major area for the emergence and dispersal of anatomically modern 3 Histoire Naturelle de l’Homme Préhistorique, HNHP—UMR 7194 —CNRS, MNHN, UPVD, Sorbonne Universités, Paris, France humans from at least 315 kya (Garcea 2012; Hublin et al. 2017; Richter et al. 2017). It thus constitutes a region of 4 Institut des Sciences de l’Evolution, ISEM—UMR 4554, CNRS, IRD, EPHE, Université de Montpellier, Montpellier, France interest for investigating how the arrival of early repre- 5 sentatives of Homo sapiens and their recent impact on the Department of Agronomy, Faculty of Natural Science and Life, fl University Ziane Achour, Djelfa, Algeria environment in uenced faunal genetic diversity and dis- tribution. During the Neolithic and after, numerous contacts 6 Laboratoire de Biologie et Santé, Faculté des Sciences, Université Abdelmalek Essâadi, Tétouan, Morocco between the two shores of the Mediterranean Sea occurred, due to the development of navigation (Mulazzani et al. 7 Institut National de la Recherche Agronomique, UR35 Comportement et Ecologie de la Faune Sauvage, Caytanet- 2010; Souville 1998; Zilhão 2014). This led to the Tolosan, France Out of Africa: demographic and colonization history of the Algerian mouse (Mus spretus Lataste) 151 translocation (Dobson 1998) and an almost complete turn- Darviche et al. 2006; Khammes-El Homsi and Aulagnier over of mammal species in the Mediterranean islands 2010; Palomo et al. 1983; Palomo et al. 1985; Stoetzel et al. (Vigne 1992). 2013; Valenzuela-Lamas et al. 2011). The modern geo- The Algerian mouse, Mus spretus Lataste, is an emble- graphical variation was hypothesized to be due to relative matic species endemic to the Mediterranean Basin. It occurs isolation between populations leading to divergence and in North Africa, from Morocco through northern Algeria possibly local adaptation. The differentiation of Algerian and Tunisia to northern Libya, and in south-west Europe mice from a pool corresponding to Morocco and Southern (southern France, most of the Iberian Peninsula and the Europe (Boursot et al. 1985; Khammes-El Homsi and Balearic Islands; Palomo et al. 2009). The oldest fossil of Aulagnier 2010) may have been triggered by North African M. spretus is dated from the Middle Pleistocene, about mice populations being fragmented by places where the 600 kyr BP, in Tunisia (Jebel Ressas 2, 3; Stoetzel 2013). desert reaches the sea or in altitude, isolating favorable This species is also known from several sites in Morocco in places (“continental islands”) for the mice (Stoetzel et al. the Middle-Late Pleistocene, early Holocene and middle- 2013). However, even at a local scale, great morphological late Holocene (Stoetzel 2013), while it is reported from variation is observed between present day Moroccan Europe only in the Neolithic (Palomo et al. 2009). Fossil populations that cannot be attributed to such large-scale evidence thus suggests a North African origin of the species biogeographical structure (Stoetzel et al. 2013). The three and recent spreading to southwestern Europe via Neolithic last millennia are known as a period of important environ- navigators (Dobson 1998). Based on restriction fragment mental perturbations, with an increase of aridity (Hassan length polymorphism (RFLP) data, Boursot et al. (1985) 1997; Le Houérou 1997) enhanced by the progressive showed a strong genetic isolation between European and increase in anthropogenic activities (Brun 1989; Brun 1991; North African populations, but they could not characterize Stambouli-Essassi et al. 2007) and concomitant introduction the tempo and mode of such divergence. Based on few D- of commensal rodents such as the house mouse, and the loop mitochondrial DNA sequences (mtDNA), Desmarais black and brown rats (Audoin-Rouzeau and Vigne 1994; (1989) showed the absence of actual gene flow between Bonhomme et al. 2011; Cucchi and Vigne 2006). The European and African populations, and a probable recent competition and possible hybridization with the house colonization event of Europe from North Africa with a mouse Mus musculus domesticus, together with anthro- strong founder effect. He also proposed that during an pogenic changes in landscape, may have particularly unfavorable climatic period, allopatric diversification impacted the local evolution of M. spretus by restricting its occurred in two refugia in North Africa (Tunisia and habitat, triggering divergence of isolated populations, which Morocco). were previously interconnected. The anthropogenic action The Late Pleistocene to middle Holocene succession of may also have modified the environment in a more global El Harhoura 2 cave (Morocco, region of Témara), yields an way. By the fact, among other effects, it was observed a exceptionally rich small vertebrate assemblage and showed significant size decrease of several wild animals during a continuous fossil record for M. spretus from 107 ± 7 kyr historical time (Sheridan and Bickford 2011). The size BP to 5800 years BP, with nonsignificant change in abun- decrease of the Western Mediterranean mouse during his- dance through time, despite pronounced environmental torical times may be the discrete signature of a perturbed changes (glacial–interglacial cycles, Stoetzel et al. 2011b). ecosystem, pushing the species away from its previous The morphology of the molars of Algerian mouse through stasis as it was evidenced in islands for other species this fossil record was also surprisingly stable (Stoetzel et al. (Sondaar 2000). 2013). The authors proposed that such evolutionary stability In the present study, we combined mitochondrial and despite environmental changes could be explained by the nuclear data to infer the evolutionary history of the Algerian fact that preferred habitats (grasslands, dry shrubland and mouse. Specifically, we wanted to answer the following open woodland) persisted in the surroundings of El Har- questions: (1) When and how did the Algerian mouse arrive houra 2 throughout the record as a “mosaic” of habitats in Europe? (2) Can we detect a recent population bottleneck despite variations in their extension. In addition, the coastal in North African populations linked to the development of location of this cave probably reduced the impact of global anthropogenic activities and/or the arrival of the house climatic variation compared with further inland. This long- mouse? (3) Is the high morphological variability observed term morphological stability contrasts with the molar size in present day populations due to isolation? Moreover, we decrease observed between the last El Harhoura 2 Holocene
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