Conservation Genetics

, Volume 18, Issue 2, pp 247–260 | Cite as

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

  • Yasuyuki Ishibashi
  • Toru Oi
  • Isao Arimoto
  • Takeshi Fujii
  • Kazuyori Mamiya
  • Nobusuke Nishi
  • Seigo Sawada
  • Hiroyuki Tado
  • Takaki Yamada
Research Article
First Online:
Received:
Accepted:
  • 380 Downloads

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.

Keywords

Balancing selection Genetic diversity Genetic drift Major histocompatibility complex Population bottleneck Threatened local populations 
This is a preview of subscription content, log in to check access.

Notes

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.

Compliance with ethical standards

Conflicts of Interest

The authors declare that they have no conflicts of interest.

References

  1. Allendorf FW, Luikart G, Aitken SN (2013) Conservation and the genetics of populations, 2nd edn. Wiley-Blackwell, ChichesterGoogle Scholar
  2. 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 9:323CrossRefPubMedPubMedCentralGoogle Scholar
  3. Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associations, SunderlandGoogle Scholar
  4. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. P Roy Soc Lond B 263:1619–1626CrossRefGoogle Scholar
  5. 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
  6. 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
  7. 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 145:421–433Google Scholar
  8. 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 16:5084–5097CrossRefPubMedGoogle Scholar
  9. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  10. Coy PL, Garshelis DL (1992) Reconstructing reproductive histories of black bears from the incremental layering in dental cementum. Can J Zool 70:2150–2160CrossRefGoogle Scholar
  11. 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 11:1043–1049CrossRefGoogle Scholar
  12. Ejsmond MJ, Radwan J (2011) MHC diversity in bottlenecked populations: a simulation model. Conserv Genet 12:129–137CrossRefGoogle Scholar
  13. Environment Agency (ed) (1991) Threatened wildlife of Japan —red data book— vertebrates. Japan Wildlife Research Center, Tokyo (in Japanese) Google Scholar
  14. 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 10:564–567CrossRefPubMedGoogle Scholar
  15. Frankham R, Ballou JD, Briscoe DA (2009) Introduction to conservation genetics, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  16. Fukui Prefectural Government (2012) Specified wildlife protection and management plan in Fukui Prefecture: the black bear. Fukui Prefectural Government, Fukui (in Japanese) Google Scholar
  17. Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722CrossRefPubMedGoogle Scholar
  18. 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
  19. Goudet J (1995) Fstat (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  20. Grant BR, Grant PR (1989) Evolutionary dynamics of a natural population: the large cactus finch of the Galapagos. University of Chicago Press, ChicagoGoogle Scholar
  21. Hedrick PW (1994) Evolutionary genetics of the major histocompatibility complex. Am Nat 143:945–964CrossRefGoogle Scholar
  22. Hedrick PW (2012) What is the evidence for heterozygote advantage selection? Trends Ecol Evol 27:698–704CrossRefPubMedGoogle Scholar
  23. Herrero S (ed) (1972) Bears—their biology and management. IUCN, MorgesGoogle Scholar
  24. 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 61–70CrossRefGoogle Scholar
  25. Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32:415–435CrossRefPubMedGoogle Scholar
  26. Hyogo Prefectural Government (2015) Protection plan for black bears. Hyogo Prefectural Government, Kobe (in Japanese)Google Scholar
  27. Ishibashi Y, Saitoh T (2004) Phylogenetic relationships among fragmented Asian black bear (Ursus thibetanus) populations in western Japan. Conserv Genet 5:311–323CrossRefGoogle Scholar
  28. 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
  29. IUCN/SSC (2013) Guidelines for reintroductions and other conservation translocations. Version 1.0. IUCN Species Survival Commission, GlandGoogle Scholar
  30. 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
  31. Johnson WE et al (2010) Genetic restoration of the Florida panther. Science 329:1641–1645CrossRefPubMedGoogle Scholar
  32. Kimura M (1968) Genetic variability maintained in a finite population due to mutational production of neutral and nearly neutral isoalleles. Genet Res 11:247–269CrossRefPubMedGoogle Scholar
  33. Kitahara E, Isagi Y, Ishibashi Y, Saitoh T (2000) Polymorphic microsatellite DNA markers in the Asiatic black bear Ursus thibetanus. Mol Ecol 9:1661–1662CrossRefPubMedGoogle Scholar
  34. Kyoto Prefectural Government (2015) First-class specified wildlife protection plan: the black bear (the 3rd period). Kyoto Prefectural Government, Kyoto (in Japanese) Google Scholar
  35. Larkin MA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  36. Loiseau C et al (2009) Diversifying selection on MHC class I in the house sparrow (Passer domesticus). Mol Ecol 18:1331–1340CrossRefPubMedGoogle Scholar
  37. Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  38. Luikart G, Allendorf FW, Cornuet J-M, Sherwin WB (1998) Distortion of allele frequency distributions provided a test for recent population bottlenecks. J Hered 83:238–247CrossRefGoogle Scholar
  39. Mamaev LV et al (1996) Canine distemper virus in Lake Baikal seals (Phoca sibirica). Vet Rec 138:437–439CrossRefPubMedGoogle Scholar
  40. Martel M, Baker S, Kavanagh I, May S (2007) Polymerases for PCR. In: Hughes S, Moody A (eds) PCR: methods express. Scion, Bloxham, pp 21–34Google Scholar
  41. Meyer D, Thomson G (2001) How selection shapes variation of the human major histocompatibility complex: a review. Ann Hum Genet 65:1–26CrossRefPubMedGoogle Scholar
  42. Ministry of the Environment (2010) Guideline for the specified wildlife protection and management: bears section. Ministry of the Environment, Tokyo (in Japanese) Google Scholar
  43. 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
  44. 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)
  45. 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
  46. Muirhead CA (2001) Consequences of population structure on genes under balancing selection. Evolution 55:1532–1541CrossRefPubMedGoogle Scholar
  47. 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 222–247Google Scholar
  48. Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218CrossRefPubMedGoogle Scholar
  49. O’Brien SJ, Evermann JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 3:254–259CrossRefPubMedGoogle Scholar
  50. Ohdachi SD, Ishibashi Y, Iwasa MA, Fukui D, Saitoh T (eds) (2015) The wild mammals of Japan, 2nd edn. Shoukadoh Book Sellers, KyotoGoogle Scholar
  51. 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 8:1331–1337CrossRefGoogle Scholar
  52. 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 102:579–589CrossRefPubMedGoogle Scholar
  53. 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 122–133Google Scholar
  54. Petit RJ, El Mousadik A, Pons O (1996) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  55. 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 90:502–503CrossRefGoogle Scholar
  56. Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544CrossRefGoogle Scholar
  57. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  58. 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 43:221–227CrossRefGoogle Scholar
  59. Schierup MH, Vekemans X, Charlesworth D (2000) The effect of subdivision on variation at multi-allelic loci under balancing selection. Genet Res 76:51–62CrossRefPubMedGoogle Scholar
  60. Servheen C, Herrero H, Peyton B (1999) Bears. Status survey and conservation action plan. IUCN, GlandGoogle Scholar
  61. 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
  62. Shimane Prefectural Government (2013) Specified wildlife (black bears) conservation and management plan. Shimane Prefectural Government, Matsue (in Japanese) Google Scholar
  63. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Frontiers in Zoology 2:16CrossRefPubMedPubMedCentralGoogle Scholar
  64. Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169CrossRefPubMedPubMedCentralGoogle Scholar
  65. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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 20:4408–4420CrossRefPubMedGoogle Scholar
  67. 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) CrossRefGoogle Scholar
  68. 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 60:2562–2574CrossRefPubMedGoogle Scholar
  69. 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 26:681–689CrossRefPubMedGoogle Scholar
  70. Wahlund S (1928) Zusammensetzung von populationen und korrelationserscheinungen vom standpunkt der vererbungslehre aus betrachtet. Hereditas 11:65–106 (in German) CrossRefGoogle Scholar
  71. Waples RS (2015) Testing for Hardy-Weinberg proportions: have we lost the plot? J Hered 106:1–19CrossRefPubMedGoogle Scholar
  72. Watterson GA (1986) The homozygosity test after a change in population size. Genetics 112:899–907PubMedPubMedCentralGoogle Scholar
  73. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  74. 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):e0136398CrossRefPubMedPubMedCentralGoogle Scholar
  75. 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 85:147–155CrossRefPubMedGoogle Scholar
  76. 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 12:230CrossRefPubMedPubMedCentralGoogle Scholar
  77. 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) CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Hokkaido Research CenterForestry and Forest Products Research InstituteSapporoJapan
  2. 2.Forestry and Forest Products Research InstituteTsukubaJapan
  3. 3.Hakusan Nature Conservation CenterHakusanJapan
  4. 4.Department of Natural EnvironmentsHiroshima Prefectural GovernmentHiroshimaJapan
  5. 5.Toyama Outdoor Nature MuseumToyamaJapan
  6. 6.Department of the Environment and Consumers AffairsTottori Prefectural GovernmentTottoriJapan
  7. 7.Shimane Prefecture Mountainous Region Research CenterIinanJapan
  8. 8.Bird and Animal Damage Consultation CenterYamaguchi Prefecture Agriculture and Forestry General Engineering CenterYamaguchiJapan
  9. 9.Shikoku Institute of Natural HistorySusakiJapan
  10. 10.Department of Environmental Science, Faculty of Bioresources and Environmental SciencesIshikawa Prefectural UniversityNonoichiJapan
  11. 11.Hakusan Fumoto KaiHakusanJapan
  12. 12.Agricultural Technology DivisionHiroshima Prefectural GovernmentHiroshimaJapan
  13. 13.Tottori Prefectural Forestry Research CenterTottoriJapan

Personalised recommendations