Skip to main content

The genetic structure of a mouse lemur living in a fragmented habitat in Northern Madagascar

Conservation Genetics volume 20, pages 229–243 (2019)Cite this article

Abstract

Habitat loss and fragmentation are major threats to biodiversity worldwide. Madagascar is among the top biodiversity hotspots and in the past 100 years several species became endangered on the island as a consequence of anthropogenic activities. In this study, we assessed the levels of genetic diversity and variation of a population of mouse lemurs (Microcebus tavaratra) inhabiting the degraded forests of the Loky-Manambato region (Northern Madagascar). We used a panel of 15 microsatellite markers to genotype 149 individuals. Our aim was to understand if the elements contributing to the heterogeneity of the landscape, such as forest fragmentation, roads, rivers and open habitat, influence the genetic structure of this population. The results showed that geographic distance along with open habitat, vegetation type and, to some extent, the Manankolana River, seem to be the main factors responsible for M. tavaratra population structure in this region. We found that this species still maintains substantial levels of genetic diversity within each forest patch and at the overall population, with low genetic differentiation observed between patches. This seems to suggest that the still existing riparian forest network connecting the different forest patches in this region, facilitates dispersal and maintains high levels of gene flow. We highlight that special efforts targeting riparian forest maintenance and reforestation might be a good strategy to reduce the effect of habitat fragmentation on the genetic diversity of extant M. tavaratra populations.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data availability

The complete microsatellite data set of all sampled individuals are available in electronic supplementary material (Online Resource 1).

References

  • Aguillon SM, Fitzpatrick JW, Bowman R, Schoech SJ, Clark AG, Coop G, Chen N (2017) Deconstructing isolation-by-distance: the genomic consequences of limited dispersal. PLoS Genet 13:e1006911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andriaholinirina N, Baden A, Blanco M, Chikhi L, Cooke A, Davies N et al (2014) Microcebus tavaratra. IUCN Red List Threat Species 2014:e.T41571A16113861. https://doi.org/10.2305/IUCN.UK.2014-1.RLTS.T41571A16113861.en

    Article  Google Scholar 

  • Bailey CA, McLain AT (2016) Evaluating the genetic diversity of three endangered lemur species (genus: Propithecus) from Northern Madagascar. J. Primatol 5:132

    Article  Google Scholar 

  • Barlow J, Lennox GD, Ferreira J, Berenguer E, Lees AC, Nally RM, Thomson JR, de Barros Ferraz B, Louzada J, Oliveira VHF et al (2016) Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation. Nature 535:144–147

    Article  CAS  PubMed  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France)

  • Blasco F (1965) Aperçu Geographique. In: Humbert H, Cours Darne G (eds) Notice de La Carte de Madagascar. Institut Francais de Pondichery, Pondicherry, pp. 4–13

    Google Scholar 

  • Burney DA (1999) Rates, patterns, and processes of landscape transformation and extinction in Madagascar. In: MacPhee RDE (ed) Extinctions in near time. Springer, Boston, pp 145–164

    Chapter  Google Scholar 

  • Chen L, Yang BL, Wu Y, Yee A, Yang BB (2003) G3 domains of aggrecan and PG-M/versican form intermolecular disulfide bonds that stabilize cell–matrix interaction. Biochem Mosc 42:8332–8341

    Article  CAS  Google Scholar 

  • Chen C, Durand E, Forbes F, François O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7:747–756

    Article  Google Scholar 

  • Craul M, Chikhi L, Sousa V, Olivieri G, Rabesandratana A, Zimmermann E, Radespiel U (2009) Influence of forest fragmentation on an endangered large-bodied lemur in northwestern Madagascar. Biol Cons 142:2862–2871. https://doi.org/10.1016/j.biocon.2009.05.026

    Article  Google Scholar 

  • Crooks KR, Burdett CL, Theobald DM, King SRB, Di Marco M, Rondinini C, Boitani L (2017) Quantification of habitat fragmentation reveals extinction risk in terrestrial mammals. Proc Natl Acad Sci 114:7635–7640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dewar RE, Radimilahy C, Wright HT, Jacobs Z, Kelly GO, Berna F (2013) Stone tools and foraging in northern Madagascar challenge Holocene extinction models. Proc Natl Acad Sci 110:12583–12588

    Article  PubMed  PubMed Central  Google Scholar 

  • Dufils JM (2003) Remaining forest cover. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. The University of Chicago Press, Chicago, pp 88–96

    Google Scholar 

  • Durand E, Jay F, Gaggiotti OE, Francois O (2009) Spatial inference of admixture proportions and secondary contact zones. Mol Biol Evol 26:1963–1973

    Article  CAS  PubMed  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Epperson BK (2005) Estimating dispersal from short distance spatial autocorrelation. Heredity 95:7–15

    Article  CAS  PubMed  Google Scholar 

  • Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A, Nekaris KA-I, Nijman V, Heymann EW, Lambert JE et al (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3:e1600946

    Article  PubMed  PubMed Central  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • FANAMBY (2010) Plan de gestion environnementale et de sauvegarde sociale (PGESS) etude d’impact environnemental et social (EIES) de la Nouvelle Aire Protegee Loky-Manambato

  • Fitzpatrick BM (2009) Power and sample size for nested analysis of molecular variance. Mol Ecol 18:3961–3966

    Article  PubMed  Google Scholar 

  • Ganzhorn JU, Lowry PP, Schatz GE, Sommer S (2001) The biodiversity of Madagascar: one of the world’s hottest hotspots on its way out. Oryx 35:346–348

    Article  Google Scholar 

  • Gautier L, Ranirison P, Nusbaumer L, Wohlhauser S (2006) Aperçu des massifs forestiers de la région Loky-Manambato. In: Inventaires de La Faune et de La Flore Du Nord de Madagascar Dans La Région Loky-Manambato, Analamerana et Andavakoera. Rech. Développement. Sér Sci Biol, pp 81–99

  • Goodman SM, Benstead JP (2005) Updated estimates of biotic diversity and endemism for Madagascar. Oryx 39:73–77

    Article  Google Scholar 

  • Goodman SM, Wilmé L (2006) Inventaires de la faune et de la flore du nord de Madagascar dans la région Loky-Manambato, Analamerana et Andavakoera. Recherches pour le Développement Sér Sci Biol

  • Green GM, Sussman RW (1990) Deforestation history of the eastern rain forests of madagascar from satellite images. Science 248:212–215

    Article  CAS  PubMed  Google Scholar 

  • Hapke A, Eberle M, Zischler H (2003) Isolation of new microsatellite markers and application in four species of mouse lemurs (Microcebus sp.). Mol Ecol Notes 3:205–208

    Article  CAS  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  CAS  Google Scholar 

  • Harper GJ, Steininger MK, Tucker CJ, Juhn D, Hawkins F (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Environ Conserv 34:325–333

    Article  Google Scholar 

  • Holmes SM, Baden AL, Brenneman RA, Engberg SE, Louis EE Jr, Johnson SE (2013) Patch size and isolation influence genetic patterns in black-and-white ruffed lemur (Varecia variegata) populations. Conserv Genet 14:615–624

    Article  Google Scholar 

  • Hotaling S, Foley ME, Lawrence NM, Bocanegra J, Blanco MB, Rasoloarison R, Kappeler PM, Barrett MA, Yoder AD, Weisrock DW (2016) Species discovery and validation in a cryptic radiation of endangered primates: Coalescent-based species delimitation in Madagascar’s mouse lemurs. Mol Ecol 25:2029–2045

    Article  CAS  PubMed  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801

    Article  CAS  PubMed  Google Scholar 

  • Jaquiéry J, Broquet T, Hirzel AH, Yearsley J, Perrin N (2011) Inferring landscape effects on dispersal from genetic distances: how far can we go?: inferring landscape effects on dispersal. Mol Ecol 20:692–705

    Article  PubMed  Google Scholar 

  • Johansson M, Primmer CR, Merila J (2007) Does habitat fragmentation reduce fitness and adaptability? A case study of the common frog (Rana temporaria). Mol Ecol 16:2693–2700

    Article  PubMed  Google Scholar 

  • Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalinowski ST (2005) hp-rare 1.0: a computer program for performing rarefaction analysis on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kappeler PM, Rasoloarison RM (2003) Microcebus, mouse lemurs, Tsidy. In: Goodman SM, Benstead J (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1310–1315

    Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Keller D, Holderegger R, van Strien MJ, Bolliger J (2015) How to make landscape genetics beneficial for conservation management? Conserv Genet 16:503–512

    Article  Google Scholar 

  • Lawler RR (2011) Historical demography of a wild lemur population (Propithecus verreauxi) in southwest Madagascar. Popul Ecol 53:229–240

    Article  Google Scholar 

  • Lewis SL, Edwards DP, Galbraith D (2015) Increasing human dominance of tropical forests. Science 349:827–832

    Article  CAS  PubMed  Google Scholar 

  • Lindenmayer DB, Fischer J (2006) Habitat fragmentation and landscape change. Island Press, Washington, DC

    Google Scholar 

  • Lorenzen ED, Nogués-Bravo D, Orlando L, Weinstock J, Binladen J, Marske KA, Ugan A, Borregaard MK, Gilbert MTP, Nielsen R et al (2011) Species-specific responses of Late Quaternary megafauna to climate and humans. Nature 479:359–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051

    Article  PubMed  Google Scholar 

  • Malecot G (1948) Les Mathématiques de l’hérédité. Masson. et Cie, Paris

    Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209

    CAS  PubMed  Google Scholar 

  • Martin RD (1972) A preliminary field-study of the lesser mouse lemur (Microcebus murinus J.F. Miller 1777). Z Tierpsychol 9:43–89

    Google Scholar 

  • Meyers DM, Wright PC (1993) Resource tracking: food availability and propithecus seasonal reproduction. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Springer, USA, pp 179–192

    Chapter  Google Scholar 

  • Meyler SV, Salmona J, Ibouroi MT, Besolo A, Rasolondraibe E, Radespiel U, Rabarivola C, Chikhi L (2012) Density estimates of two endangered nocturnal lemur species from Northern Madagascar: new results and a comparison of commonly used methods. Am J Primatol 74:414–422

    Article  PubMed  Google Scholar 

  • Mittermeier RA, Hawkins F, Kappeler PM, Langrand O, Louis EE, MacKinnon J, Mittermeier CG, Rajaobelina S, Rasoloarison R, Ratsimbazafy J et al (2010) Lemurs of Madagascar. Conservation International, Arlington

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nunziata SO, Wallenhorst P, Barrett MA, Junge RE, Yoder AD, Weisrock DW (2016) Population and conservation genetics in an endangered Lemur, Indri, across three forest reserves in Madagascar. Int J Primatol 37:688–702

    Article  Google Scholar 

  • Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res 22:201–204

    Article  CAS  PubMed  Google Scholar 

  • Olivieri GL, Sousa V, Chikhi L, Radespiel U (2008) From genetic diversity and structure to conservation: genetic signature of recent population declines in three mouse lemur species (Microcebus spp.). Biol Conserv 141:1257–1271

    Article  Google Scholar 

  • Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945

    CAS  PubMed  PubMed Central  Google Scholar 

  • Quéméré E, Louis EE, Ribéron A, Chikhi L, Crouau-Roy B (2010a) Non-invasive conservation genetics of the critically endangered golden-crowned sifaka (Propithecus tattersalli): high diversity and significant genetic differentiation over a small range. Conserv Genet 11:675–687

    Article  Google Scholar 

  • Quéméré E, Crouau-Roy B, Rabarivola C, Louis EE Jr, Chikhi L (2010b) Landscape genetics of an endangered lemur (Propithecus tattersalli) within its entire fragmented range. Mol Ecol 19:1606–1621

    Article  PubMed  Google Scholar 

  • Quéméré E, Amelot X, Pierson J, Crouau-Roy B, Chikhi L (2012) Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region. Proc Natl Acad Sci 109:13028–13033

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. https://www.R-project.org/

  • Radespiel U (2000) Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. Am J Primatol 51:21–40

    Article  CAS  PubMed  Google Scholar 

  • Radespiel U, Cepok S, Zietemann V, Zimmermann E (1998) Sexspecific usage patterns of sleeping sites in gray mouse lemurs (Microcebus murinus) in northwestern Madagascar. Am J Primatol 46:77–84

    Article  CAS  PubMed  Google Scholar 

  • Radespiel U, Funk SM, Zimmermann E, Bruford MW (2001) Isolation and characterization of microsatellite loci in the grey mouse lemur (Microcebus murinus) and their amplification in the family Cheirogaleidae. Mol Ecol Notes 1:16–18

    Article  CAS  Google Scholar 

  • Radespiel U, Lutermann H, Schmelting B, Bruford MW, Zimmermann E (2003) Patterns and dynamics of sex-biased dispersal in a nocturnal primate, the grey mouse lemur, Microcebus murinus. Anim Behav 65:707–719

    Article  Google Scholar 

  • Radespiel U, Rakotondravony R, Chikhi L (2008) Natural and anthropogenic determinants of genetic structure in the largest remaining population of the endangered golden-brown mouse lemur, Microcebus ravelobensis. Am J Prim 70:860–870. https://doi.org/10.1002/ajp.20574

    Article  Google Scholar 

  • Rakotoarisoa J-E, Raheriarisena M, Goodman SM (2013) A phylogeographic study of the endemic rodent Eliurus carletoni (Rodentia: Nesomyinae) in an ecological transition zone of northern Madagascar. J Hered 104:23–35

    Article  PubMed  Google Scholar 

  • Rakotondravony R, Radespiel U (2009) Varying patterns of coexistence of two mouse lemur species (Microcebus ravelobensis and M. murinus) in a heterogeneous landscape. Am J Primatol 71:928–938

    Article  PubMed  Google Scholar 

  • Randrianarisoa P, Rasamison A, Rakotozafy L (1999) Les lemuriens de la region de Daraina: Foret d’Analamazava, forest de Bekaraoka et foret de Sahaka. Lemur News 4:19–21

    Google Scholar 

  • Ranirison P (2006) Les massifs forestiers de la region de la Loky-Manambato (Daraina), écorégion de transition Nord: caractéristiques floristiques et structurales. Essai de modélisation des groupements végétaux. Université d’Antananarivo

  • Rasoloarison RM, Goodman SM, Ganzhorn JU (2000) Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int J Primatol 21:963–1019

    Article  Google Scholar 

  • Raymond M, Rousset F (2004) GENEPOP version 3.4. Softw. User Man. Available Httpwbiomed Curtin Edu Augenepop

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  PubMed  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Salmona J, Rakotonanahary A, Ibouroi MT, Zaranaina R, Ralantoharijaona T, Jan F, Rasolondraibe E, Barnavon M, Beck A, Wohlhauser S et al (2014) Estimation des densités et tailles de population du Microcèbe Roux du Nord de (Microcebus tavaratra) dans la région Loky-Manambato (Daraina). Lemur News 18:73–75

    Google Scholar 

  • Salmona J, Heller R, Quéméré E, Chikhi L (2017) Climate change and human colonization triggered habitat loss and fragmentation in Madagascar. Mol Ecol 26:5203–5222

    Article  PubMed  Google Scholar 

  • Scheel BM, Henke-von der Malsburg J, Giertz P, Rakotondranary SJ, Hausdorf B, Ganzhorn JU (2015) Testing the influence of habitat structure and geographic distance on the genetic differentiation of mouse lemurs (Microcebus) in Madagascar. Int J Primatol 36:823–838

    Article  Google Scholar 

  • Schipper J, Chanson JS, Chiozza F, Cox NA, Hoffmann M, Katariya V, Lamoreux J, Rodrigues ASL, Stuart SN, Temple HJ et al (2008) The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science 322:225–230

    Article  CAS  PubMed  Google Scholar 

  • Schliehe-Diecks S, Eberle M, Kappeler PM (2012) Walk the line-dispersal movements of gray mouse lemurs (Microcebus murinus). Behav Ecol Sociobiol 66:1175–1185

    Article  PubMed  PubMed Central  Google Scholar 

  • Schneider N, Chikhi L, Currat M, Radespiel U (2010) Signals of recent spatial expansions in the grey mouse lemur (Microcebus murinus). BMC Evol Biol 10:105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwitzer C, Mittermeier R, Johnson S, Donati G, Irwin M, Peacock H, Ratsimbazafy J, Razafindramanana J, Louis EE, Chikhi L (2014) Averting Lemur extinctions amid Madagascar’s political crisis. Science 343:842–843

    Article  CAS  PubMed  Google Scholar 

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90

    Article  CAS  Google Scholar 

  • Sgarlata GM, Salmona J, Aleixo-Pais I, Rakotonanahary A, Sousa AP, Kun-Rodrigues C, Ralantoharijaona T, Jan F, Zaranaina R, Rasolondraibe E et al (2018) 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

    Article  Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279

    Article  PubMed  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Vargas A, Jiménez I, Palomares F, Palacios MJ (2002) Distribution, status, and conservation needs of the golden-crowned sifaka (Propithecus tattersalli). Biol Conserv 108:325–334

    Article  Google Scholar 

  • Virah-Sawmy M, Willis KJ, Gillson L (2010) Evidence for drought and forest declines during the recent megafaunal extinctions in Madagascar. J Biogeogr 37:506–519

    Article  Google Scholar 

  • Vitousek PM (1997) Human domination of earth’s ecosystems. Science 277:494–499

    Article  CAS  Google Scholar 

  • Wahlund S (1928) Zusammensetzung von populationen und korrelationserscheinungen vom standpunkt der vererbungslehre aus betrachtet. Hereditas 11:65–106

    Article  Google Scholar 

  • Wang IJ, Savage WK, Bradley Shaffer H (2009) Landscape genetics and least-cost path analysis reveal unexpected dispersal routes in the California tiger salamander (Ambystoma californiense). Mol Ecol 18:1365–1374

    Article  PubMed  Google Scholar 

  • Weir BS (1979) Inferences about linkage disequilibrium. Biometrics 35:235–254

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  • Wimmer B, Tautz D, Kappeler P (2002) The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behav Ecol Sociobiol 52:166–175

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmermann E, Radespiel U, Mestre-Francés N, Verdier J-M (2016) Life history variation in mouse lemurs (Microcebus murinus, M. lehilahytsara): the effect of environmental and phylogenetic determinants. In: Lehman SM, Radespiel U, Zimmermann E (eds) The dwarf and mouse lemurs of Madagascar. Cambridge University Press, Cambridge, pp 174–194

    Chapter  Google Scholar 

Download references

Acknowledgements

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) for permission and support to perform this study. We also thank the NGO “Fanamby” (especially S. Rajaobelina and V. Rasoloarison, P. Ranarison, S. Velomora, F. S. Tsialazo, and S. Wohlhauser) and the local communities of Daraina for their warm reception and support. 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 warmly thank the many local guides and cooks (in particular Amidou, Rostand, Ismael, Nicole and Fatomia), as well as the local KMT responsible for sharing their incomparable expertise about the forest and help in the field, misaotra anareo jiaby. We also thank A. Beck, M. Barnavon, S. V. Meyler, and A. Besolo for their help in fieldwork. We thank the Genomics Unit at the Instituto Gulbenkian de Ciência for the genotyping service, in particular to Susana Ladeiro. We are very thankful to Tiago Maié, Rita Monteiro and Inês Carvalho for their invaluable help during data analyses and comments that greatly improved the manuscript quality. 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 was also partly funded by the Fundação para a Ciência e Tecnologia - FCT (ref. PTDC/BIA-BEC/100176/ 2008 and PTDC/BIA-BIC/4476/2012 to L.C., SFRH/BD/64875/2009 to J.S., PD/BD/114343/2016 to G.S. and SFRH/BD/118444/2016 to I.P.), the LabEx entitled TULIP (ANR-10LABX-41; ANR-11-IDEX-0002-02), the LIA BEEG-B (Laboratoire International Associé – Bioinformatics, Ecology, Evolution, Genomics and Behaviour, CNRS), the Rufford Small Grant Foundation (Grant 10941-1 to JS) and the Groupement de Recherche International (GDRI) Biodiversité et developpement durable – Madagascar.

Author information

Author notes

  1. Isa Aleixo-Pais and Jordi Salmona shared first co-authors.

Authors and Affiliations

  1. Instituto Gulbenkian de Ciência, 2780-156, Oeiras, Portugal

    Isa Aleixo-Pais, Jordi Salmona, Gabriele Maria Sgarlata, Ana Priscilla Sousa, Bárbara Parreira, Célia Kun-Rodrigues, Fabien Jan, Tânia Minhós & Lounès Chikhi

  2. Laboratoire Évolution & Diversité Biologique (EDB UMR 5174), Université de Toulouse Midi-Pyrénées, CNRS, IRD, UPS, 31062, Toulouse, France

    Jordi Salmona, Nicole Volasoa Andriaholinirina & Lounès Chikhi

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

    Jordi Salmona & Lounès Chikhi

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

    Isa Aleixo-Pais

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

    Isa Aleixo-Pais & Tânia Minhós

  6. Department of Anthropology, School of Social Sciences and Humanities, Universidade Nova de Lisboa, 1069-061, Lisbon, Portugal

    Tânia Minhós

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

    Ando Rakotonanahary, Tantely Ralantoharijaona & Emmanuel Rasolondraibe

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

    John Rigobert Zaonarivelo

Authors
  1. Isa Aleixo-Pais
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jordi Salmona
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gabriele Maria Sgarlata
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ando Rakotonanahary
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ana Priscilla Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bárbara Parreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Célia Kun-Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tantely Ralantoharijaona
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fabien Jan
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Emmanuel Rasolondraibe
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Tânia Minhós
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. John Rigobert Zaonarivelo
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Nicole Volasoa Andriaholinirina
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Lounès Chikhi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Isa Aleixo-Pais, Jordi Salmona or Lounès Chikhi.

Ethics declarations

Conflict of interest

The authors also declare that they have no conflict of interest.

Ethical approval

We conducted this study in agreement with the laws of the International Primatological Society Code of Best Practices for Field Primatology, and with the countries of Madagascar, Portugal and France. The research authorisations [218/10][220/10][113/011][118/011]/MEF/SG/DCB.SAP/SCB were obtained in Madagascar and, the export and import CITES permits 485C-EA09/MG10 and 593C-EA10/MG11 were requested from both Malagasy and Portuguese authorities.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 483 KB)

Supplementary material 2 (XLSX 36 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Aleixo-Pais, I., Salmona, J., Sgarlata, G.M. et al. The genetic structure of a mouse lemur living in a fragmented habitat in Northern Madagascar. Conserv Genet 20, 229–243 (2019). https://doi.org/10.1007/s10592-018-1126-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-018-1126-z

Keywords

  • Microcebus tavaratra
  • Microsatellites
  • Population genetics
  • Habitat fragmentation