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Genetic Differentiation and Demographic History of the Northern Rufous Mouse Lemur (Microcebus tavaratra) Across a Fragmented Landscape in Northern Madagascar

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Abstract

Phylogeographic barriers, together with habitat loss and fragmentation, contribute to the evolution of a species’ genetic diversity by limiting gene flow and increasing genetic differentiation among populations. Changes in connectivity can thus affect the genetic diversity of populations, which may influence the evolutionary potential of species and the survival of populations in the long term. We studied the genetic diversity of the little known Northern rufous mouse lemur (Microcebus tavaratra), endemic to Northern Madagascar. We focused on the population of M. tavaratra in the Loky–Manambato region, Northern Madagascar, a region delimited by two permanent rivers and characterized by a mosaic of fragmented forests. We genotyped 148 individuals at three mitochondrial loci (D-loop, cytb, and cox2) in all the major forests of the study region. Our analyses suggest that M. tavaratra holds average genetic diversity when compared to other mouse lemur species, and we identified two to four genetic clusters in the study region, a pattern similar to that observed in another lemur endemic to the region (Propithecus tattersalli). The main cluster involved samples from the two mountain forests in the study region, which were connected until recently. However, the river crossing the study region does not appear to be a strict barrier to gene flow in M. tavaratra. Finally, the inferred demographic history of M. tavaratra suggests no detectable departure from stationarity over the last millennia. Comparisons with codistributed species (P. tattersalli and two endemic rodents, Eliurus spp.) suggest both differences and similarities in the genetic clusters identified (i.e., barriers to species dispersal) and in the inferred demographic history. These comparisons suggest that studies of codistributed species are important to understand the effects of landscape features on species and to reconstruct the history of habitat changes in a region.

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Acknowledgements

We thank two anonymous reviewers and the editor for their constructive suggestions and comments. We thank the Direction Générale du Ministère de l’Environnement et des Forêts de Madagascar (Région Sava), Madagascar’s Ad Hoc Committee for Fauna and Flora and Organizational Committee for Environmental Research (CAFF/CORE), and the Fanamby NGO (especially S. Rajaobelina and V. Rasoloarison, P. Ranarison, S. Velomora, F. S. Tsialazo, and S. Wohlhauser). This study benefited from the continuous support of the Department of Animal Biology and Ecology, University of Mahajanga, and the Department of Animal Biology, University of Antananarivo. We also warmly thank the many local guides and cooks (in particular Amidou, Rostand, Amadou, Nicole et Fatomia) for sharing their incomparable expertise about the forest and without whom this work would not have been possible; A. Beck, M. Barnavon, S. V. Meyler, and A. Besolo for their help in fieldwork; and the inhabitants of the city of Daraina for their warm reception. This research was funded through the 2015-2016 BiodivERsA COFUND call for research proposals, with the national funders ANR (ANR-16-EBI3-0014), FCT (Biodiversa/0003/2015), and PT-DLR (01LC1617A). It also benefitted from several FCT (Fundação para a Ciência e a Tecnologia) projects whose references are PTDC/BIA-BEC/100176/2008, PTDC/BIA-BIC/4476/2012, SFRH/BD/64875/2009, and PD/BD/114343/2016. Financial support for this study was also provided by the Laboratoire d’Excellence (LabEx) project “TULIP” (ANR-10-LABX-41; ANR-11-IDEX-0002-02), the Rufford Small Grant Foundation (grant 10941-1), the Instituto Gulbenkian de Ciência, the LIA BEEG-B (Laboratoire International Associé – Bioinformatics, Ecology, Evolution, Genomics and Behaviour) (CNRS), and the Groupement de Recherche International (GDRI) Biodiversité et developpement durable – Madagascar.

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Authors and Affiliations

  1. Instituto Gulbenkian de Ciência, Rua da Quinta Grande, 6, P-2780-156, Oeiras, Portugal

    Gabriele Maria Sgarlata, Jordi Salmona, Isa Aleixo-Pais, Ana Priscila Sousa, Célia Kun-Rodrigues, Fabien Jan & Lounès Chikhi

  2. CNRS, Université Paul Sabatier, ENFA; UMR 5174 EDB (Laboratoire Évolution & Diversité Biologique), 118 route de Narbonne, F-31062, Toulouse, France

    Jordi Salmona & Lounès Chikhi

  3. Université Toulouse 3 Paul Sabatier, CNRS; UMR 5174 EDB, F-31062, Toulouse, France

    Jordi Salmona & Lounès Chikhi

  4. Organisms and Environment Division, Cardiff School of Biosciences, Cardiff University, CF10 3AX, Cardiff, UK

    Isa Aleixo-Pais

  5. Centre for Research in Anthropology (CRIA-FCSH/NOVA), 1069-061, Lisbon, Portugal

    Isa Aleixo-Pais

  6. Faculté des Sciences, Université de Mahajanga, BP 652 401, Mahanjanga, Madagascar

    Ando Rakotonanahary, Tantely Ralantoharijaona, Radavison Zaranaina, Emmanuel Rasolondraibe & Nicole Volasoa Andriaholinirina

  7. Département des Sciences de la Nature et de l’Environnement, Université d’Antsiranana, 201, Antsiranana, Madagascar

    John Rigobert Zaonarivelo

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  1. Gabriele Maria Sgarlata
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Correspondence to Gabriele Maria Sgarlata.

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Handling Editor: Joanna M. Setchell

Gabriele Maria Sgarlata, Jordi Salmona and Isa Aleixo-Pais shared first coauthors.

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Sgarlata, G.M., Salmona, J., Aleixo-Pais, I. et al. Genetic Differentiation and Demographic History of the Northern Rufous Mouse Lemur (Microcebus tavaratra) Across a Fragmented Landscape in Northern Madagascar. Int J Primatol 39, 65–89 (2018). https://doi.org/10.1007/s10764-018-0015-0

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