Abstract
The screaming hairy armadillo (Chaetophractus vellerosus) is a mammal species containing disjunct and isolated populations. In order to assess the effect of habitat fragmentation and geographic isolation, we developed seven new microsatellite loci isolated from low-coverage genome shotgun sequencing data for this species. Among these loci, six microsatellites were found to be polymorphic with 8–26 alleles per locus detected across 69 samples analyzed from a relictual population of the species located in the northeast of the Buenos Aires Province (Argentina). Mean allelic richness and polymorphic information content were 15 and 0.75, with observed and expected heterozygosities ranging from 0.40 to 0.67 and 0.58 to 0.90, respectively. All loci showed departures from Hardy–Weinberg equilibrium. The analysis of population structure in this relictual population revealed three groups of individuals that are genetically differentiated. These newly developed microsatellites will constitute a very useful tool for the estimation of genetic diversity and structure, population dynamics, social structure, parentage and mating system in this little-studied armadillo species. Such genetic data will be particularly helpful for the development of conservation strategies for this isolated population and also for the endangered Bolivian populations previously recognized as a distinct species (Chaetophractus nationi).
References
Abba AM, Cassini MH (2010) Ecological differences between two sympatric species of armadillos (Xenarthra, Mammalia) in a temperate region of Argentina. Acta Theriol 55:35–44
Abba AM, Superina M (2010) The 2009/2010 armadillo Red List Assessment. Edentata 11:135–184
Abba AM, Cassini GH, Cassini MH, Vizcaíno SF (2011) Historia natural del piche llorón Chaetophractus vellerosus (Mammalia: xenarthra: Dasypodidae). Rev Chil Hist Nat 84:51–64
Abba AM, Cassini GH, Valverde G, Tilak MK, Vizcaíno SF, Superina M, Delsuc F (2015) Systematics of hairy armadillos and the taxonomic status of the Andean hairy armadillo (Chaetophractus nationi). J Mammal 96:673–689
Andrew RL, Bernatchez L, Bonin A, Buerkle CA, Carstens BC, Emerson BC, Garant D, Giraud T, Kane NC, Rogers SC (2013) A road map for molecular ecology. Mol Ecol 22:2605–2626
Arteaga MC, Piñero D, Eguiarte LE, Gasca J, Medellín RA (2012) Genetic structure and diversity of the nine-banded armadillo in Mexico. J Mammal 93:547–559
Avise JC (2004) Molecular markers, natural history, and evolution. Sinauer Associates Inc, Sunderland
Bilenca D, Codesido M, González Fischer C, Pérez Carusi L, Zufiaurre E, Abba AM (2012) Impactos de la transformación agropecuaria sobre la biodiversidad en la provincia de Buenos Aires. Revista del Museo Argentino de Ciencias Naturales, Nueva Serie 14:189–198
Carlini AA, Vizcaíno SF (1987) A new record of the armadillo Chaetophractus vellerosus in the Buenos Aires Province of Argentine: possible causes for the disjunct distribution. Stud Neotrop Fauna and Environ 22:53–56
Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentation. Mol Biol Evol 24:621–631
Chinchilla L, Woodard A, Loughry WJ, Brooks CP, Welch ME (2010) Microsatellite markers for the study of leprosy in nine-banded armadillos. Mol Ecol Resour 10:1098-1105
Collevatti RG, Leite KC, de Miranda GH, Rodrigues FH (2007) Evidence of high inbreeding in a population of the endangered giant anteater, Myrmecophaga tridactyla (Myrmecophagidae), from Emas National Park, Brazil. Genet Mol Biol 30:112–120
Crespo JA (1974) Comentarios sobre nuevas localidades para mamíferos de Argentina y Bolivia. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”. Zoología 11:1–31
Earl DA, vonHoldt M (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
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
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
Faircloth BC (2008) MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design. Mol Ecol Resour 8:92–94
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152
Gibb GC, Condamine FL, Kuch M, Enk J, Moraes-Barros N, Superina M, Poinar HN, Delsuc F (2016) Shotgun mitogenomics provides a reference phylogenetic framework and timescale for living xenarthrans. Mol Biol Evol. doi:10.1093/molbev/msv250
Hedrick PW (2001) Conservation genetics: where are we now? Trends Ecol Evol 16:629–636
Loughry WJ, Truman RW, McDonough CM, Tilak MK, Garnier S, Delsuc F (2009) Is leprosy spreading among nine-banded armadillos in the southeastern United States? J Wild Dis 45:144–152
Manel S, Berthier P, Luikart G (2002) Detecting wildlife poaching: identifying the origin of individuals with Bayesian assignment tests and multilocus genotypes. Conserv Biol 16:650–659
Miller MP (2005) Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96:722–724
Moss WE, Pauli JN, Gutiérrez GA, Young AM, Vaughan C, Herrera G, Peery MZ (2011) Development and characterization of 16 microsatellites for Hoffmann’s two-toed sloth, Choloepus hoffmanni. Conserv Genet Res 3:625–627
Moss WE, Peery MZ, Gutiérrez-Espeleta GA, Vaughan C, Herrera G, Pauli JN (2012) Isolation and characterization of 18 microsatellite markers for the brown-throated three-toed sloth, Bradypus variegatus. Conserv Genet Res 4:1037–1039
Pagnutti N, Gallo J, Superina M, Vizcaíno SF, Abba AM (2014) Patrones estacionales de distribución espacial y área de acción del piche llorón, Chaetophractus vellerosus (Cingulata: Dasypodidae), en Magdalena, Buenos Aires, Argentina. Mastozool Neotrop 21:59–65
Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. PhD thesis, University of Dublin
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
Pérez-Zubieta JC (2011) Intensidad de uso de hábitat del quirquincho andino (Chaetophractus nationi) en zonas aledañas a asentamientos humanos de la provincia de Sur Carangas, Oruro, Bolivia. Edentata 12:28–35
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Prodöhl PA, Loughry WJ, Mcdonough CM, Nelson WS, Avise JC (1996) Molecular documentation of polyembryony and the micro-spatial dispersion of clonal sibships in the nine-banded armadillo, Dasypus novemcinctus. Proc R Soc Lond B 263:1643–1649
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Press, New York
Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19:1117–1123
Superina M, Pagnutti N, Abba AM (2014) What do we know about armadillos? An analysis of four centuries of knowledge about a group of South American mammals, with emphasis on their conservation. Mammal Rev 44:69–80
Viglizzo EF, Frank FC, Carreño LV, Jobbágy EG, Pereyra H, Clatt J, Pincén D, Ricard MF (2011) Ecological and environmental footprint of 50 years of agricultural expansion in Argentina. Glob Change Biol 17:959–973
Waples RS (2015) Testing for Hardy-Weinberg proportions: have we lost the plot? J Hered 106:1–19
You FM, Huo N, Gu YQ, Luo MC, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinf 9:253
Acknowledgments
We thank L.G. Pagano and M.C. Ezquiaga for their invaluable assistance during fieldwork. Our thanks also extend to the farm owners (Landa Family) and workers that allowed access to their property. Stéphane Garnier and two anonymous reviewers provided comments that helped improved a previous version of the manuscript.
Funding
This work has been financially supported by the Centre National de la Recherche Scientifique, Consejo Nacional de Investigaciones Científicas y Técnicas of Argentina (PIP No. 11420100100189), Agencia Nacional de Promoción Científica y Tecnológica of Argentina (PICT-2010-1978), Universidad Nacional de Luján, Argentina (Fondos Finalidad 3.5), and Universidad Nacional de La Plata. This study has benefited from an “Investissements d’Avenir” grant managed by Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01). This is contribution ISEM 2016-124-S of the Institut des Sciences de l’Evolution de Montpellier.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nardelli, M., Ibáñez, E.A., Dobler, D. et al. Genetic structuring in a relictual population of screaming hairy armadillo (Chaetophractus vellerosus) in Argentina revealed by a set of novel microsatellite loci. Genetica 144, 469–476 (2016). https://doi.org/10.1007/s10709-016-9915-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-016-9915-0