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Genomic diversity and geographical structure of the Pyrenean desman

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Abstract

The Pyrenean desman (Galemys pyrenaicus) is a small semi-aquatic mammal endemic to the Iberian Peninsula. The species has recently experienced a strong decline and some of its populations are severely threatened with extinction. To help in the preservation of this species, it is critical to understand its genetic structure and main evolutionary units, as these may have specific local adaptations and could be of great conservation value. Sequencing reduced representation libraries (ddRAD) from 26 specimens selected from across its entire range, we obtained around 45,000 loci per specimen and 1185 single nucleotide polymorphisms. Heterozygosity varied substantially among individuals from different areas. Interestingly, specimens from the southeastern Pyrenees had some of the lowest proportions of heterozygous positions inferred from genome-wide data in mammals so far. In addition, we estimated a tree reflecting genomic divergence, performed a principal component analysis, and carried out a Bayesian analysis of the population structure. Combined evidence supported the existence of five distinct genomic clusters largely coincident with the main mountain ranges where the species occurs, with few specimens presenting relevant admixture levels. There was good correspondence between these populations and the mitochondrial lineages detected in a previous study, yet substantial differences in some areas demonstrate the importance of performing genomic analysis to reveal the whole population history. Although the analysis of further specimens is necessary to better characterize the distribution of the different evolutionary units, the distinctive geographical structure of this species revealed by the genomic data should be considered in future conservation plans.

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References

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709. doi:10.1038/nrg2844

    Article  CAS  PubMed  Google Scholar 

  • Allendorf FW, Luikart G, Aitken SN (2013) Conservation and the genetics of populations, 2nd edn. Wiley, Hoboken

    Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aymerich P, Gosálbez J (2014) El desmán ibérico Galemys pyrenaicus (É. Geoffroy Saint-Hilaire, 1811) en los Pirineos meridionales. In: Conservation and Management of semi-aquatic mammals of South-western Europe. Munibe Monographs. Nature Series 3. Aranzadi Society of Sciences, San Sebastian, pp 37–77

  • Aymerich P, Casadesús F, Gosálbez J (2001) Distribució de Galemys pyrenaicus (Insectivora, Talpidae) a Catalunya. Orsis 16:93–110

    Google Scholar 

  • Buerkle CA, Gompert Z (2013) Population genomics based on low coverage sequencing: how low should we go? Mol Ecol 22:3028–3035. doi:10.1111/mec.12105

    Article  Google Scholar 

  • Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. Genes Genom Genet 1:171–182. doi:10.1534/g3.111.000240

    CAS  Google Scholar 

  • Catchen JM, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140. doi:10.1111/mec.12354

    Article  PubMed  PubMed Central  Google Scholar 

  • Charbonnel A (2015) Influence multi-échelle des facteurs environnementaux dans la répartition du Desman des Pyrénées (Galemys pyrenaicus) en France. Dissertation, Université de Toulouse

  • Cho YS, Hu L, Hou H et al (2013) The tiger genome and comparative analysis with lion and snow leopard genomes. Nat Commun 4:2433. doi:10.1038/ncomms3433

    PubMed  PubMed Central  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace G, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  Google Scholar 

  • Dobrynin P, Liu S, Tamazian G et al (2015) Genomic legacy of the African cheetah, Acinonyx jubatus. Genome Biol 16:277. doi:10.1186/s13059-015-0837-4

    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. doi:10.1111/j.1365-294X.2005.02553.x

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1989) PHYLIP-phylogeny inference package (version 3.4). Cladistics 5:164–166

    Google Scholar 

  • Fernandes M, Herrero J, Aulagnier S, Amori G (2011) Galemys pyrenaicus. IUCN Red List of Threatened Species Version 20112 1–3

  • Freedman AH, Gronau I, Schweizer RM et al (2014) Genome sequencing highlights the dynamic early history of dogs. PLoS Genet 10:e1004016. doi:10.1371/journal.pgen.1004016

    Article  PubMed  PubMed Central  Google Scholar 

  • Funk WC, Mckay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496. doi:10.1016/j.tree.2012.05.012

    Article  PubMed  PubMed Central  Google Scholar 

  • Gillet F (2015) Génétique et biologie de la conservation du desman des Pyrénées (Galemys pyrenaicus) en France. Dissertation, Université de Liège

  • Gisbert J, Garcia-Perea R (2014) Historia de la regresión del desmán ibérico Galemys pyrenaicus (É. Geoffroy Saint-Hilaire, 1811) en el Sistema Central (Península Ibérica). In: Conservation and Management of semi-aquatic mammals of South-western Europe. Munibe Monographs. Nature Series 3. Aranzadi Society of Sciences, San Sebastian, pp 19–35

  • Godinho R, Crespo EG, Ferrand N (2008) The limits of mtDNA phylogeography: complex patterns of population history in a highly structured Iberian lizard are only revealed by the use of nuclear markers. Mol Ecol 17:4670–4683. doi:10.1111/j.1365-294X.2008.03929.x

    Article  CAS  PubMed  Google Scholar 

  • Gomez A, Lunt DH (2007) Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. Phylogeography of Southern European Refugia, pp 155–188

  • González-Esteban J, Castién E, Gosálbez J (1999) Morphological and colour variation in the pyrenean desman galemys pyrenaicus (Geoffroy, 1811). Z Säugetierkunde 64:1–11

    Google Scholar 

  • Green RE, Briggs AW, Krause J, Prüfer K, Burbano HA, Siebauer M, Lachmann M, Pääbo S (2009) The Neandertal genome and ancient DNA authenticity. EMBO J 28:2494–2502. doi:10.1038/emboj.2009.222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gronau I, Hubisz MJ, Gulko B, Danko CG, Siepel A (2011) Bayesian inference of ancient human demography from individual genome sequences. Nat Genet 43:1031–1034. doi:10.1038/ng.937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. doi:10.1038/35016000

    Article  CAS  PubMed  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. doi:10.1093/molbev/msj030

    Article  CAS  PubMed  Google Scholar 

  • Igea J, Aymerich P, Fernández-González A, González-Esteban J, Gómez A, Alonso R, Gosálbez J, Castresana J (2013) Phylogeography and postglacial expansion of the endangered semi-aquatic mammal Galemys pyrenaicus. BMC Evol Biol 13:115. doi:10.1186/1471-2148-13-115

    Article  PubMed  PubMed Central  Google Scholar 

  • Igea J, Aymerich P, Bannikova AA, Gosálbez J, Castresana J (2015) Multilocus species trees and species delimitation in a temporal context: application to the water shrews of the genus Neomys. BMC Evol Biol 15:209. doi:10.1186/s12862-015-0485-z

    Article  PubMed  PubMed Central  Google Scholar 

  • Irwin DE (2002) Phylogeographic breaks without geographic barriers to gene flow. Evolution 56:2383–2394

    Article  PubMed  Google Scholar 

  • Kjeldsen SR, Zenger KR, Leigh K, Ellis W, Tobey J, Phalen D, Melzer A, FitzGibbon S, Raadsma HW (2015) Genome-wide SNP loci reveal novel insights into koala (Phascolarctos cinereus) population variability across its range. Conserv Genet 17:337–353. doi:10.1007/s10592-015-0784-3

    Article  Google Scholar 

  • Lanier HC, Massatti R, He Q, Olson LE, Knowles LL (2015) Colonization from divergent ancestors: glaciation signatures on contemporary patterns of genomic variation in Collared Pikas (Ochotona collaris). Mol Ecol 24:3688–3705. doi:10.1111/mec.13270

    Article  PubMed  Google Scholar 

  • Li R, Fan W, Tian G et al (2010) The sequence and de novo assembly of the giant panda genome. Nature 463:311–317. doi:10.1038/nature08696

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Fuster MJ, Garcia-Perea R, Fernández-Salvador R, Gisbert J, Ventura J (2006) Craniometric variability of the Iberian desman, Galemys pyrenaicus (Mammalia: Erinaceomorpha: Talpidae). Folia Zool 55:29–42

    Google Scholar 

  • Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629

    Article  Google Scholar 

  • Melero Y, Aymerich P, Luque-Larena JJ, Gosálbez J (2012) New insights into social and space use behaviour of the endangered Pyrenean desman (Galemys pyrenaicus). Eur J Wildl Res 58:185–193. doi:10.1007/s10344-011-0561-7

    Article  Google Scholar 

  • Morin PA, Martien KK, Taylor BL (2009) Assessing statistical power of SNPs for population structure and conservation studies. Mol Ecol Resour 9:66–73. doi:10.1111/j.1755-0998.2008.02392.x

    Article  CAS  PubMed  Google Scholar 

  • Nater A, Nietlisbach P, Arora N, van Schaik CP, van Noordwijk MA, Willems EP, Singleton I, Wich SA, Goossens B, Warren KS, Verschoor EJ, Perwitasari-Farajallah D, Pamungkas J, Krützen M (2011) Sex-biased dispersal and volcanic activities shaped phylogeographic patterns of extant Orangutans (genus: Pongo). Mol Biol Evol 28:2275–2288. doi:10.1093/molbev/msr042

    Article  CAS  PubMed  Google Scholar 

  • Nores C, Queiroz AI, Gisbert J (2007) Galemys pyrenaicus. Atlas y libro rojo de los mamíferos terrestres de España, pp 92–98

  • Orsini L, Vanoverbeke J, Swillen I, Mergeay J, De Meester L (2013) Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Mol Ecol 22:5983–5999. doi:10.1111/mec.12561

    Article  PubMed  Google Scholar 

  • Ouborg NJ, Pertoldi C, Loeschcke V, Bijlsma RK, Hedrick PW (2010) Conservation genetics in transition to conservation genomics. Trends Genet 26:177–187. doi:10.1016/j.tig.2010.01.001

    Article  CAS  PubMed  Google Scholar 

  • Palmeirim JM, Hoffmann RS (1983) Galemys pyrenaicus. Mamm Species 207:1–5

    Article  Google Scholar 

  • Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135. doi:10.1371/journal.pone.0037135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prado-Martinez J, Sudmant PH, Kidd JM et al (2013) Great ape genetic diversity and population history. Nature 499:471–475. doi:10.1038/nature12228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson JA, Ortega-Del Vecchyo D, Fan Z, Kim BY, Vonholdt BM, Marsden CD, Lohmueller KE, Wayne RK (2016) Genomic flatlining in the endangered Island Fox. Curr Biol 26:1183–1189. doi:10.1016/j.cub.2016.02.062

    Article  CAS  PubMed  Google Scholar 

  • Shafer ABA, Wolf JBW, Alves PC et al (2015) Genomics and the challenging translation into conservation practice. Trends Ecol Evol 30:78–87. doi:10.1016/j.tree.2014.11.009

    Article  PubMed  Google Scholar 

  • Sovic MG, Fries AC, Gibbs HL (2015) AftrRAD: a pipeline for accurate and efficient de novo assembly of RADseq data. Mol Ecol Resour 15:1163–1171. doi:10.1111/1755-0998.12378

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi:10.1093/bioinformatics/btl446

    Article  CAS  PubMed  Google Scholar 

  • Steiner CC, Putnam AS, Hoeck PEA, Ryder OA (2013) Conservation genomics of threatened animal species. Annu Rev Anim Biosci 1:261–281. doi:10.1146/annurev-animal-031412-103636

    Article  PubMed  Google Scholar 

  • Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496. doi:10.1016/j.tree.2004.07.003

    Article  PubMed  Google Scholar 

  • Toews DPL, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930. doi:10.1111/j.1365-294X.2012.05664.x

    Article  CAS  PubMed  Google Scholar 

  • Vonholdt BM, Pollinger JP, Earl DA, Knowles JC, Boyko AR, Parker H, Geffen E, Pilot M, Jedrzejewski W, Jedrzejewska B, Sidorovich V, Greco C, Randi E, Musiani M, Kays R, Bustamante CD, Ostrander EA, Novembre J, Wayne RK (2011) A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Res 21:1294–1305. doi:10.1101/gr.116301.110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue Y, Prado-Martinez J, Sudmant PH, Narasimhan V, Ayub Q, Szpak M, Frandsen P, Chen Y, Yngvadottir B, Cooper DN, de Manuel M, Hernandez-Rodriguez J, Lobon I, Siegismund HR, Pagani L, Quail MA, Hvilsom C, Mudakikwa A, Eichler EE, Cranfield MR, Marques-Bonet T, Tyler-Smith C, Scally A (2015) Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science 348:242–245. doi:10.1126/science.aaa3952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng X, Levine D, Shen J, Gogarten SM, Laurie C, Weir BS (2012) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28:3326–3328. doi:10.1093/bioinformatics/bts606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank the BTVS-ICNF collection (Banco de Tecidos de Vertebrados Selvagens—Instituto da Conservação da Natureza e das Florestas), Xunta de Galicia, Gobierno de Navarra, Diputación Foral de Gipuzkoa, Gobierno de La Rioja, Parque Nacional de Picos de Europa, Julio Gisbert and Rosa García-Perea (Proyecto Galemia) for Galemys pyrenaicus samples from their respective biological collections, and Henrique Carvalho, Carla Marisa Quaresma and Carlos P. Santos (Instituto da Conservação da Natureza e das Florestas) for their help with the access to the BTVS-ICNF collection. We also thank all the people of the Genomics Core Facility at the Pompeu Fabra University for help with the library preparation and sequencing. This work was financially supported by research Projects CGL2011-22640 and CGL2014-53968-P of the “Plan Nacional I + D+I del Ministerio de Economía y Competitividad” (Spain) to J.C. with contribution of project 014/2008 of the “Convocatoria de ayudas a proyectos de investigación en la Red de Parques Nacionales” (Spain) to J.G. M.Q. was supported by fellowship BES-2012-057135 of the Ministerio de Economía y Competitividad (Spain).

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Authors and Affiliations

  1. Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37, 08003, Barcelona, Spain

    Marina Querejeta, Lídia Escoda, Javier Igea & Jose Castresana

  2. Desma Estudios Ambientales S.L, Ukulu 11, 31791, Sunbilla, Navarra, Spain

    Jorge González-Esteban

  3. Tragsatec, Área de Biodiversidad, Calle Julián Camarillo 6, 28037, Madrid, Spain

    Asunción Gómez

  4. Biosfera Consultoría Medioambiental S.L, Calle Candamo 5, 33012, Oviedo, Spain

    Angel Fernández-González

  5. Departament de Biologia Animal, Universitat de Barcelona, Avinguda Diagonal 643, 08028, Barcelona, Spain

    Pere Aymerich & Joaquim Gosálbez

  6. Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK

    Javier Igea

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  1. Marina Querejeta
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Correspondence to Jose Castresana.

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Querejeta, M., González-Esteban, J., Gómez, A. et al. Genomic diversity and geographical structure of the Pyrenean desman. Conserv Genet 17, 1333–1344 (2016). https://doi.org/10.1007/s10592-016-0865-y

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