Abstract
The Japanese wild boar (Sus scrofa leucomystax) is one of the most widely distributed mammals in Japan. However, its population structure and pattern of gene flow at a regional level are poorly understood. In this study, we investigated the local-scale genetic structure of the Japanese wild boar. In total, 172 individuals sampled in Gifu Prefecture, central Japan, were genotyped for 29 autosomal microsatellite loci. Significant genetic differentiations (F ST = 0.020–0.128) were detected among some geographical areas. In addition, in the overall population (n = 172), all loci deviating from the Hardy–Weinberg equilibrium exhibited a significant deficit of heterozygotes. These results suggest the presence of genetic substructuring in the local population. Moreover, Bayesian cluster analysis revealed the presence of substructuring within the population, despite the relatively small study area (10,621 km2). Spatial Bayesian cluster analysis showed that the boundaries of subpopulations were generally consistent with landscape features (e.g. main rivers, urban areas and road and train networks). Our study implies that these landscape features play a significant role as a barrier to dispersal and gene flow in the local population of the Japanese wild boar.
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Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment polymorphisms. Am J Hum Genet 32:314–331
Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Cullingham CI, Kyle CJ, Pond BA, Rees EE, White BN (2009) Different permeability of rivers to raccoon gene flow corresponds to rabies incidence in Ontario, Canada. Mol Ecol 18:43–53
Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169
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
El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839
Epps CW, Palsbøll PJ, Wehausen JD, Roderick GK, Ramey RR II, McCullough DR (2005) Highways block gene flow and cause a rapid decline in genetic diversity of desert bighorn sheep. Ecol Lett 8:1029–1038
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
FAO (2011) Molecular genetic characterization of animal genetic resources. FAO Animal Production and Health Guidelines. No. 9. FAO. http://www.fao.org/docrep/014/i2413e/i2413e00.pdf Accessed 7 Dec 2012
Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) Version 3.6. Department of Genome Sciences, University of Washington, Seattle
Ferreira E, Souto L, Soares AMVM, Fonseca C (2009) Genetic structure of the wild boar population in Portugal: evidence of a recent bottleneck. Mamm Biol 74:274–285
Frantz AC, Cellina S, Krier A, Schley L, Burke T (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493–505
Frantz AC, Bertouille S, Eloy MC, Licoppe A, Chaumont F, Flamand MC (2012) Comparative landscape genetic analyses show a Belgian motorway to be a gene flow barrier for red deer (Cervus elaphus), but not wild boars (Sus scrofa). Mol Ecol 21:3445–3457
Gifu Prefectural Government (2012) Choujyu hogo-ku touichi-zu (wildlife protection area map). Otohime Insatusha, Ehime (in Japanese)
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www2.unil.ch/popgen/softwares/fstat.htm
Guillot G, Mortier F, Estoup A (2005) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715
Hajji GM, Zachos FE (2011) Mitochondrial and nuclear DNA analyses reveal pronounced genetic structuring in Tunisian wild boar Sus scrofa. Eur J Wildl Res 57:449–456
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 23:1801–1806
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Luetkemeier ES, Sodhi M, Schook LB, Malhi RS (2010) Multiple asian pig origins revealed through genomic analyses. Mol Phylogenet Evol 54:680–686
Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170
Okumura N, Ishiguro N, Nakano M, Hirai K, Matsui A, Sahara M (1996) Geographic population structure and sequence divergence in the mitochondrial DNA control region of the Japanese wild boar (Sus scrofa leucomystax), with reference to those of domestic pigs. Biochem Genet 34:179–189
Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation based exploration of accuracy and power. Mol Ecol 13:55–65
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-Espona S, Pérez-Barbería FJ, McLeod JE, Jiggins CD, Gordon IJ, Pemberton JM (2008) Landscape features affect gene flow of Scottish highland red deer (Cervus elaphus). Mol Ecol 17:981–996
Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503
Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci 94:9197–9201
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Scandura M, Iacolina L, Cossu A, Apollonio M (2011) Effects of human perturbation on the genetic make-up of an island population: the case of the Sardinian wild boar. Heredity 106:1012–1020
Watanobe T, Ishiguro N, Nakano M (2003) Phylogeography and population structure of the Japanese wild boar Sus scrofa leucomystax: mitochondrial DNA variation. Zool Sci 20:1477–1489
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wilson RE, Farley SD, McDonough TJ, Talbot SL, Barboza PS (2015) A genetic discontinuity in moose (Alces alces) in Alaska corresponds with fenced transportation infrastructure. Conserv Genet 16:791–800
Acknowledgments
The authors thank the members of hunting clubs in Gifu Prefecture and Mr. Takahiro Yokota (Gifu Prefectural Government) for providing wild boar samples. We thank Shobudani Farm (Ibigawa, Gifu, Japan) for providing pig samples. We are also grateful to Mr. Satoshi Wada (Gifu Prefectural Government) for assistance in making the figures. Helpful comments from two anonymous reviewers improved the manuscript. This work was supported in part by the 2015 grant from Gifu University to R. Tadano.
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Tadano, R., Nagai, A. & Moribe, J. Local-scale genetic structure in the Japanese wild boar (Sus scrofa leucomystax): insights from autosomal microsatellites. Conserv Genet 17, 1125–1135 (2016). https://doi.org/10.1007/s10592-016-0848-z
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DOI: https://doi.org/10.1007/s10592-016-0848-z