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Loss of allelic diversity in the MHC class II DQB gene in western populations of the Japanese black bear Ursus thibetanus japonicus

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Abstract

In Japan, the black bear, Ursus thibetanus, is distributed on Honshu and Shikoku Islands. Most populations in western Japan declined considerably during the twentieth century, but a few populations are now rebounding due to conservation efforts. Here, we examined the sequence variation in the second exon of the major histocompatibility complex class II DQB gene (270 bp), which is critical for pathogen recognition. We measured variation within six populations in western Japan, including two threatened populations in the Chugoku region on Honshu and one on Shikoku. Eight sequence variants were observed among the examined bears (n = 417), and two to eight variants were retained within populations. Our samples, collected in 2001–2013, retained a smaller number of sequence variants in each population compared with the allelic diversity in an earlier study that examined the same gene and used samples collected mainly during the last century. Many rare variants that were observed previously and may have been maintained by balancing selection have disappeared from recent populations. Although the earlier study suggested a loss of genetic diversity in western Japan, the present study shows that further loss of rare variants has occurred, probably due to genetic drift during the end of the last century.

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References

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

    Google Scholar 

  • Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a F st-outlier method. BMC Bioinformatics 9:323

    Article  PubMed  PubMed Central  Google Scholar 

  • Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associations, Sunderland

    Google Scholar 

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. P Roy Soc Lond B 263:1619–1626

    Article  Google Scholar 

  • Biodiversity Center of Japan (2004) The national survey on the natural environment: report of the distribution survey of Japanese animals (mammals). Biodiversity Center of Japan, Nature Conservation Bureau, Ministry of the Environment, Japan, Fujiyoshida (in Japanese)

    Google Scholar 

  • Biodiversity Center of Japan (2011) The national survey on the natural environment: report on the investigation of inhabiting situations of specific mammals and the operation to form task forces for investigation. Biodiversity Center of Japan, Fujiyoshida (in Japanese with English summary)

    Google Scholar 

  • Boyce WM, Hedrick PW, Muggli-Cockett NE, Kalinowski ST, Penedo MCT, Ramey RR II (1996) Genetic variation of major histocompatibility complex and microsatellite loci: a comparison in bighorn sheep. Genetics 145:421–433

    Google Scholar 

  • Bryja J, Charbonnel N, Berthier K, Galan M, Cosson J-F (2007) Density-related changes in selection pattern for major histocompatibility complex genes in fluctuating populations of voles. Mol Ecol 16:5084–5097

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coy PL, Garshelis DL (1992) Reconstructing reproductive histories of black bears from the incremental layering in dental cementum. Can J Zool 70:2150–2160

    Article  Google Scholar 

  • Cristescu R, Sherwin WB, Handasyde K, Cahill V, Cooper DW (2010) Detecting bottlenecks using BOTTLENECK 1.2.02 in wild populations: the importance of the microsatellite structure. Conserv Genet 11:1043–1049

    Article  Google Scholar 

  • Ejsmond MJ, Radwan J (2011) MHC diversity in bottlenecked populations: a simulation model. Conserv Genet 12:129–137

    Article  Google Scholar 

  • Environment Agency (ed) (1991) Threatened wildlife of Japan —red data book— vertebrates. Japan Wildlife Research Center, Tokyo (in Japanese)

    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 

  • Frankham R, Ballou JD, Briscoe DA (2009) Introduction to conservation genetics, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Fukui Prefectural Government (2012) Specified wildlife protection and management plan in Fukui Prefecture: the black bear. Fukui Prefectural Government, Fukui (in Japanese)

    Google Scholar 

  • Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722

    Article  CAS  PubMed  Google Scholar 

  • Garshelis DL, Steinmetz R, (IUCN SSC Bear Specialist Group) (2008) Ursus thibetanus. The IUCN Red List of Threatened Species 2008: eT22824A9391633 http://dx.doi.org/102305/IUCNUK2008RLTST22824A9391633en. Downloaded 05 October 2015

  • Goudet J (1995) Fstat (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Article  Google Scholar 

  • Grant BR, Grant PR (1989) Evolutionary dynamics of a natural population: the large cactus finch of the Galapagos. University of Chicago Press, Chicago

    Google Scholar 

  • Hedrick PW (1994) Evolutionary genetics of the major histocompatibility complex. Am Nat 143:945–964

    Article  Google Scholar 

  • Hedrick PW (2012) What is the evidence for heterozygote advantage selection? Trends Ecol Evol 27:698–704

    Article  PubMed  Google Scholar 

  • Herrero S (ed) (1972) Bears—their biology and management. IUCN, Morges

    Google Scholar 

  • Higuchi R (1989) Using PCR to engineer DNA. In: Erlich HA (ed) PCR technology: principles and applications for DNA amplification. Stockton Press, New York, pp 61–70

    Chapter  Google Scholar 

  • Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32:415–435

    Article  CAS  PubMed  Google Scholar 

  • Hyogo Prefectural Government (2015) Protection plan for black bears. Hyogo Prefectural Government, Kobe (in Japanese)

    Google Scholar 

  • Ishibashi Y, Saitoh T (2004) Phylogenetic relationships among fragmented Asian black bear (Ursus thibetanus) populations in western Japan. Conserv Genet 5:311–323

    Article  CAS  Google Scholar 

  • Ishikawa Prefectural Government (2014) Protection and management plan for the black bear in Ishikawa Prefecture: the 3rd period (revised). Ishikawa Prefectural Government, Kanazawa (in Japanese)

    Google Scholar 

  • IUCN/SSC (2013) Guidelines for reintroductions and other conservation translocations. Version 1.0. IUCN Species Survival Commission, Gland

    Google Scholar 

  • Japan Bear Network (ed) (2014) Reports: project for the current status survey about the expansion/reduction of distribution areas of black and brown bears, the prevention of conflicts with them, and the recovery of threatened populations. Japan Bear Network, Ibaraki (in Japanese)

    Google Scholar 

  • Johnson WE et al (2010) Genetic restoration of the Florida panther. Science 329:1641–1645

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1968) Genetic variability maintained in a finite population due to mutational production of neutral and nearly neutral isoalleles. Genet Res 11:247–269

    Article  CAS  PubMed  Google Scholar 

  • Kitahara E, Isagi Y, Ishibashi Y, Saitoh T (2000) Polymorphic microsatellite DNA markers in the Asiatic black bear Ursus thibetanus. Mol Ecol 9:1661–1662

    Article  CAS  PubMed  Google Scholar 

  • Kyoto Prefectural Government (2015) First-class specified wildlife protection plan: the black bear (the 3rd period). Kyoto Prefectural Government, Kyoto (in Japanese)

    Google Scholar 

  • Larkin MA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Loiseau C et al (2009) Diversifying selection on MHC class I in the house sparrow (Passer domesticus). Mol Ecol 18:1331–1340

    Article  PubMed  Google Scholar 

  • Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet J-M, Sherwin WB (1998) Distortion of allele frequency distributions provided a test for recent population bottlenecks. J Hered 83:238–247

    Article  Google Scholar 

  • Mamaev LV et al (1996) Canine distemper virus in Lake Baikal seals (Phoca sibirica). Vet Rec 138:437–439

    Article  CAS  PubMed  Google Scholar 

  • Martel M, Baker S, Kavanagh I, May S (2007) Polymerases for PCR. In: Hughes S, Moody A (eds) PCR: methods express. Scion, Bloxham, pp 21–34

    Google Scholar 

  • Meyer D, Thomson G (2001) How selection shapes variation of the human major histocompatibility complex: a review. Ann Hum Genet 65:1–26

    Article  CAS  PubMed  Google Scholar 

  • Ministry of the Environment (2010) Guideline for the specified wildlife protection and management: bears section. Ministry of the Environment, Tokyo (in Japanese)

    Google Scholar 

  • Ministry of the Environment (2014) Red data book 2014. —threatened wildlife of Japan— volume 1, Mammalia. Gyosei Corporation, Tokyo (in Japanese with English summary)

    Google Scholar 

  • Ministry of the Environment (2015) Statistics on wildlife. Ministry of the Environment. https://www.env.go.jp/nature/choju/docs/docs2.html. Accessed 07 Oct 2015 (in Japanese)

  • Ministry of the Environment (ed) (2002) Threatened wildlife of Japan —red data book— volume 1, Mammalia, 2nd edn. Japan Wildlife Research Center, Tokyo (in Japanese with English summary)

    Google Scholar 

  • Muirhead CA (2001) Consequences of population structure on genes under balancing selection. Evolution 55:1532–1541

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Hughes AL (1990) Polymorphism and evolution of the major histocompatibility complex loci in mammals. In: Selander RK, Clark AG, Whittam TS (eds) Evolution at the molecular level. Sinauer Associations, Sunderland, pp 222–247

    Google Scholar 

  • Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218

    Article  CAS  PubMed  Google Scholar 

  • O’Brien SJ, Evermann JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 3:254–259

    Article  PubMed  Google Scholar 

  • Ohdachi SD, Ishibashi Y, Iwasa MA, Fukui D, Saitoh T (eds) (2015) The wild mammals of Japan, 2nd edn. Shoukadoh Book Sellers, Kyoto

    Google Scholar 

  • Ohnishi N, Saitoh T, Ishibashi Y, Oi T (2007) Low genetic diversities in isolated populations of the Asian black bear (Ursus thibetanus) in Japan, in comparison with large stable populations. Conserv Genet 8:1331–1337

    Article  Google Scholar 

  • Ohnishi N, Uno R, Ishibashi Y, Tamate HB, Oi T (2009) The influence of climatic oscillations during the Quaternary Era on the genetic structure of Asian black bears in Japan. Heredity 102:579–589

    Article  CAS  PubMed  Google Scholar 

  • Oi T, Yamazaki K (eds) (2006) The status of Asiatic black bears in Japan. In: Japan Bear Network (compiler) Understanding Asian bears to secure their future. Japan Bear Network, Ibaraki. pp 122–133

  • Petit RJ, El Mousadik A, Pons O (1996) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reduction in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544

    Article  Google Scholar 

  • Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Saitoh T, Ishibashi Y, Kanamori H, Kitahara E (2001) Genetic status of fragmented populations of the Asian black bear Ursus thibetanus in western Japan. Popul Ecol 43:221–227

    Article  Google Scholar 

  • Schierup MH, Vekemans X, Charlesworth D (2000) The effect of subdivision on variation at multi-allelic loci under balancing selection. Genet Res 76:51–62

    Article  CAS  PubMed  Google Scholar 

  • Servheen C, Herrero H, Peyton B (1999) Bears. Status survey and conservation action plan. IUCN, Gland

    Google Scholar 

  • Shiga Prefectural Government (2012) Black bears in Shiga Prefecture: specified wildlife protection and management plan (the 2nd period). Shiga Prefectural Government, Otsu (in Japanese)

    Google Scholar 

  • Shimane Prefectural Government (2013) Specified wildlife (black bears) conservation and management plan. Shimane Prefectural Government, Matsue (in Japanese)

    Google Scholar 

  • Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Frontiers in Zoology 2:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutton J, Nakagawa S, Robertson BC, Jamieson IG (2011) Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol Ecol 20:4408–4420

    Article  PubMed  Google Scholar 

  • Takahashi S (1979) Changes in the distribution of the Japanese black bear in the West Chugoku Mountains in relation to changes of vegetation. Geogr Rev Japan 52:635–642 (in Japanese with English abstract)

    Article  Google Scholar 

  • van Oosterhout C, Joyce DA, Cummings SM et al (2006) Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60:2562–2574

    Article  PubMed  Google Scholar 

  • Vassilakos D, Natoli A, Dahlheim M, Hoelzel AR (2009) Balancing and directional selection at exon-2 of the MHC DQB1 locus among populations of odontocete cetaceans. Mol Biol Evol 26:681–689

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Waples RS (2015) Testing for Hardy-Weinberg proportions: have we lost the plot? J Hered 106:1–19

    Article  PubMed  Google Scholar 

  • Watterson GA (1986) The homozygosity test after a change in population size. Genetics 112:899–907

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Wu J, Kohno N, Mano S, Fukumoto Y, Tanabe H, Hasegawa M, Yonezawa T (2015) Phylogeographic and demographic analysis of the Asian black bear (Ursus thibetanus) based on mitochondrial DNA. PLoS ONE 10(9):e0136398

    Article  PubMed  PubMed Central  Google Scholar 

  • Yasukochi Y, Kurosaki T, Yoneda M, Koike H (2010) Identification of the expressed MHC class II DQB gene of the Asiatic black bear, Ursus thibetanus, in Japan. Genes Genet Syst 85:147–155

    Article  CAS  PubMed  Google Scholar 

  • Yasukochi Y, Kurosaki T, Yoneda M, Koike H, Satta Y (2012) MHC class II DQB diversity in the Japanese black bear, Ursus thibetanus japonicus. BMC Evol Biol 12:230

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoneda M (2001) Local population and conservation of Asian black bear; habitat preference and minimum area size. J Jpn Inst Landscape Archit 64:314–317 (in Japanese)

    Article  Google Scholar 

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Acknowledgments

We thank Dr. Yoshiki Yasukochi (University of Tokyo) for kindly providing the information about the samples used in their study. We also thank the late Atsushi Katayama and other staff members of the Wildlife Management Office, Shuji Wada (Hiroshima Environment and Health Association), Dr. Eiji Hosoi (Yamaguchi University), and members of the Kyoto Hunting Association for kindly sending bear samples. This work was supported by JSPS KAKENHI Grant Number JP23310170.

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Correspondence to Yasuyuki Ishibashi.

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Ishibashi, Y., Oi, T., Arimoto, I. et al. Loss of allelic diversity in the MHC class II DQB gene in western populations of the Japanese black bear Ursus thibetanus japonicus . Conserv Genet 18, 247–260 (2017). https://doi.org/10.1007/s10592-016-0897-3

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