The role of demographic history and selection in shaping genetic diversity of the Galápagos penguin (Spheniscus mendiculus)


Autoři: Gabriella Arauco-Shapiro aff001;  Katelyn I. Schumacher aff001;  Dee Boersma aff002;  Juan L. Bouzat aff001
Působiště autorů: Department of Biological Sciences, Bowling Green State University, Bowling Green, Ohio, United States of America aff001;  Center for Ecosystem Sentinels and Department of Biology, University of Washington, Seattle, Washington, United States of America aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226439

Souhrn

Although many studies have documented the effects of demographic bottlenecks on the genetic diversity of natural populations, there is conflicting evidence of the roles that genetic drift and selection may play in driving changes in genetic variation at adaptive loci. We analyzed genetic variation at microsatellite and mitochondrial loci in conjunction with an adaptive MHC class II locus in the Galápagos penguin (Spheniscus mendiculus), a species that has undergone serial demographic bottlenecks associated with El Niño events through its evolutionary history. We compared levels of variation in the Galápagos penguin to those of its congener, the Magellanic penguin (Spheniscus magellanicus), which has consistently maintained a large population size and thus was used as a non-bottlenecked control. The comparison of neutral and adaptive markers in these two demographically distinct species allowed assessment of the potential role of balancing selection in maintaining levels of MHC variation during bottleneck events. Our analysis suggests that the lack of genetic diversity at both neutral and adaptive loci in the Galápagos penguin likely resulted from its restricted range, relatively low abundance, and history of demographic bottlenecks. The Galápagos penguin revealed two MHC alleles, one mitochondrial haplotype, and six alleles across five microsatellite loci, which represents only a small fraction of the diversity detected in Magellanic penguins. Despite the decreased genetic diversity in the Galápagos penguin, results revealed signals of balancing selection at the MHC, which suggest that selection can mitigate some of the effects of genetic drift during bottleneck events. Although Galápagos penguin populations have persisted for a long time, increased frequency of El Niño events due to global climate change, as well as the low diversity exhibited at immunological loci, may put this species at further risk of extinction.

Klíčová slova:

Alleles – Genetic drift – Genetic loci – Haplotypes – Natural selection – Penguins – Population genetics – Species diversity


Zdroje

1. Frankham R, Ballou JD, Briscoe DA. Introduction to Conservation Genetics. 1st ed. Cambridge: Cambridge University Press; 2002.

2. Bouzat JL. Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conserv Genet. 2010; 11: 463–478.

3. Wright S. Evolution in Mendelian populations. Genetics. 1931; 16: 97–159. 17246615

4. Nei M, Maruyama T, Chakraborty R. The bottleneck effect and genetic variability in populations. Evolution. 1975; 29: 1–10. doi: 10.1111/j.1558-5646.1975.tb00807.x 28563291

5. Frankham R. Relationship of genetic variation to population size in wildlife. Conserv Biol. 1996; 10: 1500–1508.

6. Gitzendanner MA, Soltis PS. Patterns of genetic variation in rare and widespread plant congeners. Am J Bot. 2000; 87: 783–792. 10860909

7. Reed DH. Albatrosses, eagles, and newts, Oh My: exceptions to the prevailing paradigm concerning genetic diversity and population viability? Anim Conserv. 2010; 13: 448–457.

8. O’Brien SJ, Johnson WE, Driscoll CA, Dobrynin P, Marker L. Conservation genetics of the cheetah: lessons learned and new opportunities. J Hered 2017; 671–677. doi: 10.1093/jhered/esx047 28821181

9. Hughes AL, Nei M. Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA. 1989; 86: 958–962. doi: 10.1073/pnas.86.3.958 2492668

10. Accolla RS, Adorini L, Sartoris S, Sinigaglia F, Guardiola J. MHC: Orchestrating the immune response. Immunol Today. 1995; 16: 8–11. doi: 10.1016/0167-5699(95)80063-8 7880390

11. Bollmer JL, Vargas FH, Parker PG. Low MHC variation in the endangered Galápagos penguin (Spheniscus mendiculus). Immunogenetics. 2007; 59: 593–602. doi: 10.1007/s00251-007-0221-y 17457582

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

13. Alcaide M, Edwards SV, Negro JJ, Serrano D, Tella JL. Extensive polymorphism and geographical variation at a positively selected MHC class II B gene of the lesser kestrel (Falco naumanni). Mol Ecol. 2008; 17: 2652–2665. doi: 10.1111/j.1365-294X.2008.03791.x 18489548

14. Hughes CR, Miles S, Walbroehl JM. Support for the minimal essential MHC hypothesis: A parrot with a single, highly polymorphic MHC class II B gene. Immunogenetics. 2008; 60: 219–231. doi: 10.1007/s00251-008-0287-1 18431567

15. Potts WK, Wakeland EK. Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. Trends Genet. 1993; 9: 408–412. doi: 10.1016/0168-9525(93)90103-o 8122307

16. Eimes JA, Bollmer JL, Whittingham LA, Johnson JA, Van Oosterhout C, Dunn PO. Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation. J Evol Biol. 2011; 24: 1847–1856. doi: 10.1111/j.1420-9101.2011.02311.x 21605219

17. Sutton JT, Nakagawa S, Robertson BC, Jamieson IG. Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol Ecol. 2011; 20: 4408–4420. doi: 10.1111/j.1365-294X.2011.05292.x 21981032

18. Spurgin LG, Richardson DS. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc Lond B. 2010; 277: 979–988.

19. Doherty PC, Zinkernagel RM. Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature. 1975; 256: 50–52. doi: 10.1038/256050a0 1079575

20. Hughes AL, Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988; 335: 167–170. doi: 10.1038/335167a0 3412472

21. Clarke BC, Kirby DRS. Maintenance of histocompatibility polymorphism. Nature. 1966; 211: 999–1000. doi: 10.1038/211999a0 6007869

22. Slade RW, McCallum H. Overdominant vs. frequency-dependent selection at MHC loci. Genetics. 1992; 132: 861–862. 1468635

23. Hill AVS. HLA associations with malaria in Africa: some implications for MHC evolution. In: Klein J, Klein D, editors. Molecular Evolution of the Major Histocompatibility Complex. NATO ASI Series (Series H: Cell Biology) vol 59. Berlin: Springer; 1991. pp 403–420.

24. Hedrick PW, Thomson G. Evidence for balancing selection at HLA. Genetics. 1983; 104: 449–456. 6884768

25. Miller HC, Lambert DM. Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol. 2004; 13: 3709–3721. doi: 10.1111/j.1365-294X.2004.02368.x 15548285

26. Campos JL, Posada D, Morán P. Genetic variation at MHC, mitochondrial and microsatellite loci in isolated populations of Brown trout (Salmo trutta). Conserv Genet. 2006; 7: 515–530.

27. Radwan J, Kawalko A, Wójcik JM, Babik W. MHC-DRB3 variation in a free-living population of the European bison, Bison bonasus. Mol Ecol. 2007; 16: 531–540. doi: 10.1111/j.1365-294X.2006.03179.x 17257111

28. Babik W, Pabijan M, Radwan J. Contrasting patterns of variation in MHC loci in the Alpine newt. Mol Ecol. 2008; 17: 2339–2355. doi: 10.1111/j.1365-294X.2008.03757.x 18422929

29. Maruyama T, Nei M. Genetic variability maintained by mutation and overdominant selection in finite populations. Genetics. 1984; 98: 441–459.

30. Ejsmond MJ, Radwan J. MHC diversity in bottlenecked populations: A simulation model. Conserv Genet. 2011; 12: 129–137.

31. Elena SF, Cooper VS, Lenski RE. Punctuated evolution caused by selection of rare beneficial mutations. Science. 1996; 272: 1802–1804. doi: 10.1126/science.272.5269.1802 8650581

32. Satta Y, O’hUigin C, Takahata N, Klein J. Intensity of natural selection at the major histocompatibility complex loci. Proc Natl Acad Sci USA. 1994; 91: 7184–7188. doi: 10.1073/pnas.91.15.7184 8041766

33. Bos DH, Gopurenko D, Williams RN, DeWoody JA. Inferring population history and demography using microsatellites, mitochondrial DNA, and major histocompatibility complex (MHC) genes. Evolution. 2008; 62: 1458–1468. doi: 10.1111/j.1558-5646.2008.00364.x 18331461

34. Seddon JM, Baverstock PR. Variation on islands: major histocompatibility complex (Mhc) polymorphism in populations of the Australian bush rat. Mol Ecol. 1999; 8: 2071–2079. doi: 10.1046/j.1365-294x.1999.00822.x 10632858

35. Hedrick PW, Gutiérrez-Espeleta GA, Lee RN. Founder effect in an island population of bighorn sheep. Mol Ecol. 2001; 10: 851–857. doi: 10.1046/j.1365-294x.2001.01243.x 11348494

36. Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA. 2004; 101: 3490–3494. doi: 10.1073/pnas.0306582101 14990802

37. Van Oosterhout C, Joyce DA, Cummings SM, Blais J, Barson NJ, Ramnarine IW, et al. Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution. 2006; 60: 2562–2574. 17263117

38. Mona S, Crestanella B, Bankhead-Dronnet S, Pecchioli E, Ingrosso S, D’Amelio S, et al. Disentangling the effects of recombination, selection, and demography on the genetic variation at a major histocompatibility complex class II gene in the alpine chamois. Mol Ecol. 2008; 17: 4053–4067. doi: 10.1111/j.1365-294x.2008.03892.x 19238706

39. Oliver MK, Piertney SB. Selection maintains MHC diversity through a natural population bottleneck. Mol Biol Evol. 2012; 29: 1713–1720. doi: 10.1093/molbev/mss063 22323362

40. Schuster AC, Herde A, Mazzoni CJ, Eccard JA, Sommer S. Evidence for selection maintaining MHC diversity in a rodent species despite strong density fluctuations. Immunogenetics. 2016; 68: 429–437. doi: 10.1007/s00251-016-0916-z 27225422

41. Zhai T, Yang H-Q, Zhang R-C, Fang L-M, Zhong G-H, Fang S-G. Effects of population bottleneck and balancing selection on the Chinese alligator are revealed by locus-specific characterization of MHC genes. Sci Rep. 2017; 7: 5549. doi: 10.1038/s41598-017-05640-2 28717152

42. Hedrick PW, Kalinowski ST. Inbreeding depression in conservation biology. Annu Rev Ecol Syst. 2000; 31: 139–262.

43. Frankham R, Gilligan DM, Morris D, Briscoe DA. Inbreeding and extinction: effects of purging. Conserv Genet. 2001; 2: 279–285.

44. Radwan J. Inbreeding depression in fecundity and inbred line extinction in the bulb mite, Rhizoglyphus robini. Heredity. 2003; 371–376. doi: 10.1038/sj.hdy.6800254 12714982

45. Swindell WR, Bouzat JL. Ancestral inbreeding reduces the magnitude of inbreeding depression in Drosophila melanogaster. Evolution. 2006; 60: 762–767. 16739457

46. Swindell WR, Bouzat JL. Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging. J Evol Biol. 2006; 19: 1257–1264. doi: 10.1111/j.1420-9101.2005.01074.x 16780526

47. Boersma PD. Breeding patterns of Galapagos penguins as an indicator of oceanographic conditions. Science. 1978; 200: 1481–1483. doi: 10.1126/science.200.4349.1481 17757690

48. Vargas H, Lougheed C, Snell H. Population size and trends of the Galápagos Penguin Spheniscus mendiculus. Ibis. 2005; 147: 367–374.

49. Boersma PD, Frere E, Kane O, Pozzi LM, Pütz K, Raya Rey A, et al. Magellanic penguins. In: García Borboroglu P, Boersma PD, editors. Penguins: Natural History and Conservation. Seattle: University of Washington Press; 2013. pp 233–263.

50. Boersma PD. An ecological and behavioral study of the Galápagos penguin. Living Bird. 1976; 15: 43–93.

51. Valle CA. Status of the Galápagos penguin and flightless cormorant populations in 1985. Noticias de Galápagos. 1986; 43: 16–17.

52. Valle CA, Coulter MC. Present status of the flightless cormorant, Galápagos penguin and greater flamingo populations in the Galápagos Islands, Ecuador, after the 1982–83 El Niño. Condor. 1987; 89: 276–281.

53. Vargas FH, Harrison S, Rea S, Macdonald DW. Biological effects of El Niño on the Galápagos penguin. Biol Conserv. 2006; 127: 107–114.

54. Boersma PD. Population trends of the Galápagos penguin: impacts on El Niño and La Niña. Condor. 1998; 100: 245–253.

55. Vargas FH, Lacy RC, Johnson PJ, Macdonald D. Modelling the effect of El Niño on the persistence of small populations: the Galápagos penguin as a case study. Biol Conserv. 2007; 137: 138–148.

56. Boersma PD, Cappello CD, Merlen G. First observations of post-fledging care in Galapagos penguins (Spheniscus mendiculus). Wilson J of Ornithol. 2017; 129: 186–191.

57. Pütz K, Schiavini A, Rey AR, Lüthi BH. Winter migration of Magellanic penguins (Spheniscus magellanicus) from the southernmost distributional range. Mar Biol. 2007; 152: 1227–1235.

58. Stokes DL, Boersma PD, Lopez de Casenave J, García-Borboroglu P. Conservation of migratory Magellanic penguins requires marine zoning. Biol Conserv. 2014; 170: 151–161.

59. Rebstock GA, Boersma PD, García-Borboroglu P. Changes in habitat use and nesting density in a declining seabird colony. Popul Ecol. 2016; 58: 105–119.

60. Dantas GPM, Maria GC, Marasco ACM, Castro LT, Almeida VS, Santos FR, et al. Demographic history of the Magellanic penguin (Spheniscus magellanicus) on the Pacific and Atlantic coasts of South America. J Ornithol. 2018; 159: 643–655.

61. Gandini P, Frere E, Boersma PD. Status and conservation of Magellanic penguins Spheniscus magellanicus in Patagonia, Argentina. Bird Conserv Int. 1996; 6: 307–316.

62. Pozzi LM, García Borboroglu P, Boersma PD, Pascual MA. Population regulation in Magellanic penguins: what determines changes in colony size? PLoS One. 2015; 10: e0119002. doi: 10.1371/journal.pone.0119002 25786254

63. Kimura M. The Neutral Theory of Molecular Evolution. Cambridge: Cambridge University Press; 1983.

64. Bouzat JL, Lewin HA, Paige KN. The ghost of genetic diversity past: historical DNA analysis of the Greater Prairie Chicken. Am Nat. 1998; 152: 1–6. doi: 10.1086/286145 18811397

65. Akst EP, Boersma PD, Fleischer RC. A comparison of genetic diversity between the Galápagos penguin and the Magellanic penguin. Conserv Genet. 2002; 3: 375–383.

66. Frankham R. Conservation genetics. Annu Rev Genet. 1995; 29: 305–327. doi: 10.1146/annurev.ge.29.120195.001513 8825477

67. Frankham R, Lees K, Montgomery ME, England PR, Lowe EH, Briscoe DA. Do population size bottlenecks reduce evolutionary potential? Anim Conserv. 1999; 2: 255–260.

68. Vrijenhoek RC. Genetic diversity and fitness in small populations. In: Loeschcke V, Jain SK, Tomiuk J, editors. Conservation Genetics. EXS, vol 68. Basel: Birkhäuser; 1994. pp 37–53.

69. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I. Inbreeding and extinction in a butterfly metapopulation. Nature. 1998; 392: 491–494.

70. Frankham R. Genetics and extinction. Biol Conserv. 2005; 126: 131–140.

71. Paterson S, Wilson K, Pemberton JM. Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proc Natl Acad Sci USA. 1998; 95: 3714–3719. doi: 10.1073/pnas.95.7.3714 9520432

72. Seutin G, White BN, Boag TP. Preservation of avian blood and tissue samples for DNA analysis. Can J Zool. 1991; 69: 82–90.

73. Frere E, Gandini P. Distribución reproductiva y abundancia de las aves marinas de Santa Cruz. Parte 2: de Bahía Laura a Punta Dungeness. In: Yorio P, Frere E, Gandini P, Harris G., editors. Atlas de la distribución reproductiva de aves marinas en el litoral Patagónico Argentino. Buenos Aires: Society Instituto Salesiano de Artes Gráficas; 1998. pp 153–177.

74. Bouzat JL, Lyons AC, Knafler GJ, Boersma PD. Environmental determinants of genetic structure in Magellanic Penguin breeding colonies of the Atlantic and Pacific Oceans. Poster session presented at the VIII International Penguin Conference; 2013 Sep 2–6; Bristol, United Kingdom.

75. Bouzat JL, Walker BG, Boersma PD. Regional genetic structure in the Magellanic penguin (Spheniscus magellanicus) suggests metapopulation dynamics. Auk. 2009; 126: 326–334.

76. Nims BD, Vargas FH, Merkel J, Parker PG. Low genetic diversity and lack of population structure in the endangered Galápagos penguin (Spheniscus mendiculus). Conserv Genet. 2008; 9: 1413–1420.

77. BirdLife International and Handbook of the Birds of the World. Bird species distribution maps of the world, version 2018.1. Available at: http://datazone.birdlife.org/species/requestdis.

78. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 1989.

79. Kikkawa EF, Tsuda TT, Naruse TK, Sumiyama D, Fukuda M, Kurita M, et al. Analysis of the sequence variations in the Mhc DRB1-like gene of the endangered Humboldt penguin (Spheniscus humboldti). Immunogenetics. 2005; 57: 99–107. doi: 10.1007/s00251-005-0774-6 15714307

80. Kikkawa EF, Tsuda TT, Sumiyama D, Naruse TK, Fukuda M, Kurita M, et al. Trans-species polymorphism of the Mhc class II DRB-like gene in banded penguins (genus Spheniscus). Immunogenetics. 2009; 61: 341–352. doi: 10.1007/s00251-009-0363-1 19319519

81. Knafler GJ, Clark JA, Boersma PD, Bouzat JL. MHC diversity and mate choice in the Magellanic penguin, Spheniscus magellanicus. J Hered. 2012; 103: 759–768. doi: 10.1093/jhered/ess054 22952272

82. Bollmer JL, Dunn PO, Whittingham LA, Wimpee C. Extensive MHC class II B gene duplication in a passerine, the common yellowthroat (Geothlypis trichas). J Hered. 2010; 101: 448–460. doi: 10.1093/jhered/esq018 20200139

83. Davies CJ, Andersson L, Ellis SA, Hensen EJ, Lewin HA, Mikko S, et al. Nomenclature for the factors of the BoLA system, 1996: report of the ISAG BoLA Nomenclature Committee. Anim Genet. 1997; 28: 159–168.

84. Kennedy LJ, Altet L, Angles JM, Barnes A, Carter SD, Francino O, et al. Nomenclature for the factors of the dog major histocompatibility system (DLA), 1998: first report of the ISAG DLA Nomenclature Committee. Tissue Antigens. 1999; 54: 312–321. doi: 10.1034/j.1399-0039.1999.540319.x 10519375

85. Marsh SG, Bodmer JG, Albert ED, Bodmer WF, Bontrop RE, Dupont B, et al. Nomenclature for factors of the HLA system, 2000. Tissue Antigens. 2001; 57: 236–283. doi: 10.1034/j.1399-0039.2001.057003236.x 11285132

86. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012; 28: 1647–1649. doi: 10.1093/bioinformatics/bts199 22543367

87. Wright S. The genetical structure of populations. Ann Eugen. 1949; 15: 323–354.

88. Raymond M, Rousset F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered. 1995; 86: 248–249.

89. Rousset F. Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour. 2008; 8: 103–106. doi: 10.1111/j.1471-8286.2007.01931.x 21585727

90. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003; 19: 2496–2497. doi: 10.1093/bioinformatics/btg359 14668244

91. Excoffier L, Lischer HEL. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010; 10: 564–567. doi: 10.1111/j.1755-0998.2010.02847.x 21565059

92. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989; 123: 585–595. 2513255

93. Ewens WJ. The sampling theory of selectively neutral alleles. Theor Popul Biol. 1972; 3: 87–112. doi: 10.1016/0040-5809(72)90035-4 4667078

94. Watterson G. The homozygosity test of neutrality. Genetics. 1978; 88: 405–417. 17248803

95. Slatkin M. An exact test for neutrality based on the Ewens sampling distribution. Genet Res. 1994; 68: 71–74.

96. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016; 33: 1870–1874. doi: 10.1093/molbev/msw054 27004904

97. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986; 3: 418–426. doi: 10.1093/oxfordjournals.molbev.a040410 3444411

98. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, et al. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature. 1993; 364: 33–39. doi: 10.1038/364033a0 8316295

99. Leigh JW, Bryant D. POPART: full-feature software for haplotype network construction. Methods Ecol Evol. 2015; 6: 1110–1116.

100. Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000; 9: 1657–1659. doi: 10.1046/j.1365-294x.2000.01020.x 11050560

101. Slatkin M. A measure of population subdivision based on microsatellite allele frequencies. Genetics. 1995; 139: 457–462. 7705646

102. Cornuet JM, Luikart G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics. 1996; 144: 2001–2014. 8978083

103. Piry S, Luikart G, Cornuet JM. BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered. 1999; 90: 502–503.

104. Kimura M, Ohta T. Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA. 1978; 75: 2868–2872. doi: 10.1073/pnas.75.6.2868 275857

105. DiRienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB. Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA. 1994; 91: 3166–3170. doi: 10.1073/pnas.91.8.3166 8159720

106. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB. Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered. 1998; 89: 238–247. doi: 10.1093/jhered/89.3.238 9656466

107. Simonsen KL, Churchill GA, Aquadro CF. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics. 1995; 141: 413–429. 8536987

108. Maruyama T, Fuerst PA. Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics. 1985; 111: 675–689. 4054612

109. Garrigan D, Hedrick PW. Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution. 2003; 57: 1707–1722. doi: 10.1111/j.0014-3820.2003.tb00580.x 14503614

110. Miller HC, Miller KA, Daugherty CH. Reduced MHC variation in a threatened tuatara species. Anim Conserv. 2008; 11: 206–214.

111. Hedrick PW, Lee RN, Garrigan D. Major histocompatibility complex variation in red wolves: evidence for common ancestry with coyotes and balancing selection. Mol Ecol. 2002; 11: 1905–1913. doi: 10.1046/j.1365-294x.2002.01579.x 12296935

112. Ellegren H, Hartman G, Johansson M, Andersson L. Major histocompatibility complex monomorphism and low levels of DNA fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proc Natl Acad Sci USA. 1993; 90: 8150–8153. doi: 10.1073/pnas.90.17.8150 8367476

113. Hedrick PW, Parker KM, Lee RN. Using microsatellite and MHC variation to identify species, ESUs, and MUs in the endangered Sonoran topminnow. Mol Ecol. 2001; 10: 1399–1412. doi: 10.1046/j.1365-294x.2001.01289.x 11412363

114. Weber DS, Stewart BS, Schienman J, Lehman N. Major histocompatibility complex variation at three class II loci in the northern elephant seal. Mol Ecol. 2004; 13: 711–718. doi: 10.1111/j.1365-294x.2004.02095.x 14871373

115. O’Brien SJ, Evermann JF. Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol. 1988; 3: 254–259. doi: 10.1016/0169-5347(88)90058-4 21227241

116. Slade RW. Limited MHC polymorphism in the southern elephant seal: implications for MHC evolution and marine mammal population biology. Proc R Soc Lond B. 1992; 249: 163–171.

117. Hedrick PW, Parker KM, Gutiérrez-Espeleta GA, Rattink A, Lievers K. Major histocompatibility complex variation in the Arabian oryx. Evolution. 2000; 5: 2145–2151.

118. Levin II, Outlaw DC, Vargas FH, Parker PG. Plasmodium blood parasite found in endangered Galápagos penguins (Spheniscus mendiculus). Biol Conserv. 2009; 142: 3191–3195.


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