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Phylogeography and Evolutionary History of the Crocidura Olivieri

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Phylogeography and Evolutionary History of the Crocidura Olivieri Phylogeography and evolutionary history of the Crocidura olivieri complex (Mammalia, Soricomorpha): from a forest origin to broad ecological expansion across Africa François Jacquet, Christiane Denys, Erik Verheyen, Josef Bryja, Rainer Hutterer, Julian C. Kerbis Peterhans, William T. Stanley, Steven M. Goodman, Arnaud Couloux, Marc Colyn, et al. To cite this version: François Jacquet, Christiane Denys, Erik Verheyen, Josef Bryja, Rainer Hutterer, et al.. Phylogeog- raphy and evolutionary history of the Crocidura olivieri complex (Mammalia, Soricomorpha): from a forest origin to broad ecological expansion across Africa. BMC Evolutionary Biology, BioMed Central, 2015, 15 (1), pp.71. 10.1186/s12862-015-0344-y. hal-01151637 HAL Id: hal-01151637 https://hal-univ-rennes1.archives-ouvertes.fr/hal-01151637 Submitted on 13 May 2015 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Jacquet et al. BMC Evolutionary Biology (2015) 15:71 DOI 10.1186/s12862-015-0344-y RESEARCH ARTICLE Open Access Phylogeography and evolutionary history of the Crocidura olivieri complex (Mammalia, Soricomorpha): from a forest origin to broad ecological expansion across Africa François Jacquet1*, Christiane Denys1, Erik Verheyen2,3, Josef Bryja4,5, Rainer Hutterer6, Julian C Kerbis Peterhans7,8, William T Stanley8, Steven M Goodman8,9, Arnaud Couloux10, Marc Colyn11 and Violaine Nicolas1 Abstract Background: This study aims to reconstruct the evolutionary history of African shrews referred to the Crocidura olivieri complex. We tested the respective role of forest retraction/expansion during the Pleistocene, rivers (allopatric models), ecological gradients (parapatric model) and anthropogenic factors in explaining the distribution and diversification within this species complex. We sequenced three mitochondrial and four nuclear markers from 565 specimens encompassing the known distribution of the complex, i.e. from Morocco to Egypt and south to Mozambique. We used Bayesian phylogenetic inference, genetic structure analyses and divergence time estimates to assess the phylogenetic relationships and evolutionary history of these animals. Results: The C. olivieri complex (currently composed of C. olivieri, C. fulvastra, C. viaria and C. goliath) can be segregated into eight principal geographical clades, most exhibiting parapatric distributions. A decrease in genetic diversity was observed between central and western African clades and a marked signal of population expansion was detected for a broadly distributed clade occurring across central and eastern Africa and portions of Egypt (clade IV). The main cladogenesis events occurred within the complex between 1.37 and 0.48 Ma. Crocidura olivieri sensu stricto appears polyphyletic and C. viaria and C. fulvastra were not found to be monophyletic. Conclusions: Climatic oscillations over the Pleistocene probably played a major role in shaping the genetic diversity within this species complex. Different factors can explain their diversification, including Pleistocene forest refuges, riverine barriers and differentiation along environmental gradients. The earliest postulated members of the complex originated in central/eastern Africa and the first radiations took place in rain forests of the Congo Basin. A dramatic shift in the ecological requirements in early members of the complex, in association with changing environments, took place sometime after 1.13 Ma. Some lineages then colonized a substantial portion of the African continent, including a variety of savannah and forest habitats. The low genetic divergence of certain populations, some in isolated localities, can be explained by their synanthropic habits. This study underlines the need to revise the taxonomy of the C. olivieri complex. Keywords: Crocidura olivieri, Diversification, Forest refuge, Molecular dating, Phylogeography, Pleistocene climate changes, Riverine barrier, Soricidae, Systematics * Correspondence: [email protected] 1Institut de Systématique, Évolution, Biodiversité, ISYEB UMR 7205 - CNRS, MNHN, UPMC, EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités, 57 rue Cuvier, CP 51, 75005 Paris, France Full list of author information is available at the end of the article © 2015 Jacquet et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Jacquet et al. BMC Evolutionary Biology (2015) 15:71 Page 2 of 15 Background alternative to allopatric models [17]. It suggests that Climatic oscillations during the Pleistocene are known strong environmental gradients result in adaptive diver- to have had a dramatic role in shaping the diversity and gence and speciation for taxa tolerant of a broad range distribution of many African plant and animal species of habitats. A recent study has emphasized the role of [1,2]. Several large-scale studies that tested this hypoth- habitat gradients in lineage diversification in the African esis have been carried out on large African mammals rodent Cricetomys [7]. [3-5]. However, these animals are vagile and often The taxonomy of the C. olivieri complex has been dis- broadly disperse or have large home ranges. Therefore, cussed for almost a century but uncertainties remain. Spe- small mammals are excellent models for testing patterns cies currently considered valid within the C. olivieri of pan-African biogeography. There have been a few complex are distributed across different habitats: C. studies on sub-Saharan rodents [6-8], but shrews goliath Thomas, 1906 is endemic to rain forests of the (Soricidae), a group known to have been used elsewhere Congo Basin, C. viaria (I. Geoffroy, 1834) and C. to test Pleistocene climate oscillation models [9], have fulvastra (Sundevall, 1843) are encountered in the not been examined across broad ecological areas on the Sudanian savannah from Morocco to Kenya and from continent. These animals have short life spans, rapid Mali to Ethiopia, respectively, and C. olivieri is wide- reproduction cycles, low dispersal abilities and respond spread across portions of the African continent [12]. quickly to environmental changes [10], and are therefore The specific aims of this study are: 1) to provide a a good model to investigate climate-driven models of di- greater understanding of the systematics of African giant versification. All available genetic studies of African shrews of the C. olivieri complex, specifically specimens shrews focussed on taxa with relatively small geographical identified based on morphology as C. olivieri, C. viaria, distributions (e.g. [9]). Members of the Crocidura olivieri C. fulvastra or C. goliath; 2) to test for the respective (Lesson, 1827) complex [11], which have notably large roles of forest retraction/expansion, rivers (allopatric body size for shrews and can weigh up to 65 g [12], are a models), ecological gradients (parapatric model) and an- rare example of a widespread Afrotropical soricid taxon. thropogenic factors in explaining the diversification and Members of the C. olivieri complex occur in a variety of current distribution of the different lineages. In order to habitats, including tropical rain forests, marshes, savannah infer biogeographical scenarios at the scale of the African and montane areas [12]. Therefore, this group is a poten- continent and to answer questions concerning possible fac- tially excellent model to test how climatic oscillations and tors promoting diversification within the complex, we used associated changes in vegetation during the Pleistocene in- data from three mitochondrial and four nuclear markers fluenced their distribution and diversification. and conducted phylogenetic and population genetics ana- Models employed to understand diversification events lyses on animals originating from most of its geographical within vertebrates faunas are too numerous to review in range (Figure 1). detail here. By and large, hypotheses concerning factors that promote speciation in tropical faunas have been Results preoccupied with the geographical context of speciation Phylogenetic relationships and fall into two categories: allopatric and parapatric Based on Bayesian Inference of combined data from the models. With allopatric models, extrinsic barriers to seven markers (Figure 2 and Additional file 1) the C. olivieri gene flow lead to the separation of sub-populations, complex (specimens morphologically identified as C. which evolve differently associated with genetic drift and olivieri, C. viaria, C. fulvastra C. goliath or C. somalica) natural selection. For example, the “Pleistocene forest forms a highly supported monophyletic group (pp = poster- refuge” hypothesis, originally formulated for tropical ior
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