Immunogenetics

, Volume 65, Issue 1, pp 47–61 | Cite as

Evolution of the MHC-DQB exon 2 in marine and terrestrial mammals

  • María José Villanueva-Noriega
  • Charles Scott Baker
  • Luis Medrano-González
Original Paper

Abstract

On the basis of a general low polymorphism, several studies suggest that balancing selection in the class II major histocompatibility complex (MHC) is weaker in marine mammals as compared with terrestrial mammals. We investigated such differential selection among Cetacea, Artiodactyla, and Primates at exon 2 of MHC-DQB gene by contrasting indicators of molecular evolution such as occurrence of transpecific polymorphisms, patterns of phylogenetic branch lengths by codon position, rates of nonsynonymous and synonymous substitutions as well as accumulation of variable sites on the sampling of alleles. These indicators were compared between the DQB and the mitochondrial cytochrome b gene (cytb) as a reference of neutral expectations and differences between molecular clocks resulting from life history and historical demography. All indicators showed that the influence of balancing selection on the DQB is more variable and overall weaker for cetaceans. In our sampling, ziphiids, the sperm whale, monodontids and the finless porpoise formed a group with lower DQB polymorphism, while mysticetes exhibited a higher DQB variation similar to that of terrestrial mammals as well as higher occurrence of transpecific polymorphisms. Different dolphins appeared in the two groups. Larger variation of selection on the cetacean DQB could be related to greater stochasticity in their historical demography and thus, to a greater complexity of the general ecology and disease processes of these animals.

Keywords

Major histocompatibility complex DQB Cytochrome b Nonsynonymous nucleotide substitution Transpecific polymorphism Marine mammals 

Notes

Acknowledgments

We are grateful to all people who, at the labs and/or in the sea, have contributed to this work. In particular, we acknowledge the technical work of M. Dalebout, J. Murrell, M.R. Robles, and D. Steel as well as the review and advice from M.L. Fanjul, D. Heimeier, and M. Uribe, and the scholar orientation by G. Vilaclara. We appreciate the assistance of J. Zúñiga on statistical tests as well as the comments of two anonymous reviewers who greatly improved this article. Institutional, academic, legal, and funding supports were received from The Marsden Foundation, University of Auckland, Consejo Nacional de Ciencia y Tecnología, Facultad de Ciencias-Universidad Nacional Autónoma de México, Posgrado en Ciencias del Mar y Limnología-Universidad Nacional Autónoma de México, Secretaría del Medio Ambiente y Recursos Naturales, Instituto Nacional de Ecología, and Convention on International Trade in Endangered Species of Wild Fauna and Flora.

Supplementary material

251_2012_647_MOESM1_ESM.xlsx (90 kb)
ESM 1 (XLSX 89 kb)

References

  1. Acevedo-Whitehouse K, Cunningham AA (2006) Is MHC enough for understanding wildlife immunogenetics? Trends Ecol Evol 21(8):433–438PubMedCrossRefGoogle Scholar
  2. Amills M, Ramiya V, Norimine J, Lewin HA (1998) The major histocompatibility complex of ruminants. Rev Sci Tech Off Int Epiz 17(1):108–120Google Scholar
  3. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179–224PubMedCrossRefGoogle Scholar
  4. Árnason Ú (1972) The role of chromosomal rearrangement in mammalian speciation with special reference to Cetacea and Pinnipedia. Hereditas 70:113–118PubMedCrossRefGoogle Scholar
  5. Baker CS, Vant MD, Dalebout ML, Lento GM, O'Brien SJ, Yuhki N (2006) Diversity and duplication of DQB and DRB-like genes of the MHC in baleen whales (suborder: Mysticeti. Immunogenetics 58:283–296PubMedCrossRefGoogle Scholar
  6. Beck S, Trowsdale J (1999) Sequence organization of the class II region of the human MHC. Immunol Rev 167:201–210PubMedCrossRefGoogle Scholar
  7. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2005) GenBank. Nucleic Acids Res 33:34–38CrossRefGoogle Scholar
  8. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years. J Evol Biol 16:363–377PubMedCrossRefGoogle Scholar
  9. Boisserie JR, Lihoreau F, Brunet M (2005) The position of Hippopotamidae within Cetartiodactyla. Proc Natl Acad Sci USA 102:1531–1537CrossRefGoogle Scholar
  10. Bowen L, Aldridge BM, DeLong R, Melin S, Godinez C, Zavala A, Gulland F, Lowenstine L, Stott JL, Johnson ML (2006) MHC gene configuration variation in geographically disparate populations of California sea lions (Zalophus californianus). Mol Ecol 15:529–533PubMedCrossRefGoogle Scholar
  11. Bush GL, Case SM, Wilson AC, Patton JL (1977) Rapid speciation and chromosomal evolution in mammals. Proc Natl Acad Sci USA 74:3942–3946PubMedCrossRefGoogle Scholar
  12. Castro-Prieto A, Watcher B, Sommer S (2011) Cheetah paradigm revisited: MHC diversity in the world's largest free-ranging population. Mol Biol Evol 28(4):1455–1468PubMedCrossRefGoogle Scholar
  13. Cutrera AP, Lacey EA (2007) Trans-species polymorphism and evidence of selection on class II MHC in tuco-tucos (Rodentia: Ctenomyidae). Immunogenetics 59(12):937–948PubMedCrossRefGoogle Scholar
  14. Edwards SV, Hedrick PW (1998) Evolution ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13(8):305–311PubMedCrossRefGoogle Scholar
  15. Ellegren H, Hartaman G, Johansson M, Andersson L (1993) Major histocompatibilty complex monomorphism low levels of DNA fingerprinting variability in a reintroduced rapidly expanding population of beavers. Proc Natl Acad Sci USA 90:8150–8153PubMedCrossRefGoogle Scholar
  16. Gatesy J (1997) More DNA support for a Cetacea/Hippopotamidae clade: the blood-clotting protein gene γ-fibrinogen. Mol Biol Evol 14:537–543PubMedCrossRefGoogle Scholar
  17. Goldsby RA, Kindt TJ, Osborne BA, Kuby J (2003) Immunology, 5th edn. Freeman, New YorkGoogle Scholar
  18. Gu X, Nei M (1999) Locus specificity of polymorphic alleles evolution by a birth-and-death process in mammalian MHC genes. Mol Biol Evol 16(2):147–156PubMedCrossRefGoogle Scholar
  19. Gutierrez-Espeleta G, Hedrick PW, Kalinowski ST, Garrigan D, Óbice WM (2001) Is the decline of the desert bighorn sheep from infectious disease the result of low MHC variation? Heredity 86:439–445PubMedCrossRefGoogle Scholar
  20. Harwood J, Hall A (1990) Mass mortality in marine mammals: its implications for population dynamics genetics. Trends Ecol Evol 5(8):254–257PubMedCrossRefGoogle Scholar
  21. Hassanin A, Douzery EJP (2003) Molecular and morphological phylogenies of Ruminantia and the alternative position of the Moschidae. Syst Biol 52(2):206–228PubMedCrossRefGoogle Scholar
  22. Hayashi K, Nishida S, Yoshida H, Goto M, Pastene LA, Koike H (2003) Sequence variation of the DQB allele in the cetacean MHC. Mamm Stud 28(2):89–96CrossRefGoogle Scholar
  23. Hoelzel AR, Claiborne Stephens J, O'brien SJ (1999) Molecular genetic diversity: evolution at the MHC DQB locus in four species of pinnipeds. Mol Biol Evol 16(5):611–618PubMedCrossRefGoogle Scholar
  24. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167–170PubMedCrossRefGoogle Scholar
  25. Hutchings K (2009) Parasite-mediated selection in an island endemic, the Seychelles warbler (Acrocephalus sechellensis). PhD thesis, University of East Anglia, LondonGoogle Scholar
  26. Irwin DM, Árnason Ú (1994) Cytochrome b gene of marine mammals: phylogeny and evolution. J Mamm Evol 2:37–55CrossRefGoogle Scholar
  27. Jackson JA, Baker CS, Vant M, Steel DJ, Medrano-González L, Palumbi SR (2009) Big and slow: phylogenetic estimates of molecular evolution in baleen whales (Suborder Mysticeti). Mol Biol Evol 26(11):2427–2440PubMedCrossRefGoogle Scholar
  28. Klein J, Figueroa F (1986) Evolution of the major histocompatibility complex. Crit Rev Immunol 6:295–386PubMedGoogle Scholar
  29. Kryazhimskiy S, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4(12):e1000304PubMedCrossRefGoogle Scholar
  30. Kumánovics A, Takada T, Fischer Lindahl K (2003) Genomic organization of the mammalian MHC. Annu Rev Immunol 21:629–657PubMedCrossRefGoogle Scholar
  31. Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9(4):299–306PubMedCrossRefGoogle Scholar
  32. Maddison DR, Maddison WP (2000) MacClade 4: analysis of phylogeny and character evolution. Version 4.0. Sinauer, SunderlandGoogle Scholar
  33. McCallum HI, Kuris A, Harvell CD, Lafferty KD, Smith GW, Porter J (2004) Does terrestrialepidemiologyapplyto marine systems? Trends Ecol Evol 19(11):585–591CrossRefGoogle Scholar
  34. Montgelard C, Catzeflis FM, Douzery E (1997) Phylogenetic relationships of artiodactyls and cetaceans as deduced from the comparison of cytochrome b and 12S rRNA mitochondrial sequences. Mol Biol Evol 14(5):550–559PubMedCrossRefGoogle Scholar
  35. Munguía-Vega A, Esquer-Garrigós Y, Rojas-Bracho L, Vázquez-Juárez R, Castro-Prieto A, Flores-Ramírez S (2007) Genetic drift vs. natural selection in a long-term small isolated population: major histocompatibility complex class II variation in the Gulf of California endemic porpoise Phocoena sinus. Mol Ecol 16:4051–4065PubMedCrossRefGoogle Scholar
  36. Murphy WJ, Elzirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409:614–618PubMedCrossRefGoogle Scholar
  37. Murray BW, Malik S, White BN (1995) Sequence variation at the major histocompatibility complex locus DQβ in beluga whales (Delphinapterus leucas). Mol Biol Evol 12(4):582–593PubMedGoogle Scholar
  38. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  39. Nielsen R, Yang Z (2003) Estimating the distribution of selection coefficients from phylogenetic data with applications to mitochondrial and viral DNA. Mol Biol Evol 20(8):1231–1239PubMedCrossRefGoogle Scholar
  40. Nigenda-Morales S, Flores-Ramírez S, Urbán-R J, Vázquez-Juárez R (2008) MHC DQB-1 polymorphism in the Gulf of California fin whale (Balaenoptera physalus) population. J Hered 99(1):14–21PubMedCrossRefGoogle Scholar
  41. Nikaido M, Rooney AP, Okada N (1999) Phylogenetic relationships among cetartiodactyls based on insertions of short and long interspaced elements: hippopotamuses are the closest extant relative of whales. Proc Natl Acad Sci USA 96:10261–10266PubMedCrossRefGoogle Scholar
  42. O'Brien SJ, Roelke ME, Marker L, Newman A, Winkler CA, Meltzer D, Colly L, Evermann JF, Bush M, Wildt DE (1985) Genetic basis for species vulnerability in the cheetah. Science 227(4693):1428–1434PubMedCrossRefGoogle Scholar
  43. Paterson S, Wilson K, Pemberton JM (1998) 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 95:3714–3719PubMedCrossRefGoogle Scholar
  44. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818PubMedCrossRefGoogle Scholar
  45. Potts WK, Wakeland EK (1990) Evolution of diversity at the major histocompatibility complex. Trends Ecol Evol 5:181–187PubMedCrossRefGoogle Scholar
  46. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  47. Schwaiger F-W, Weyers E, Buitkamp J, Ede AJ, Crawford A, Epplen JT (1994) Interdependent MHC-DRB exon-plus-intron evolution in artiodactyls. Mol Biol Evol 11(2):239–249PubMedGoogle Scholar
  48. Sigurdardóttir S, Borsch C, Gustafsson K, Andersson L (1992) Gene duplications and sequence polymorphism of bovine class II DQB genes. Immunogenetics 35:205–213PubMedCrossRefGoogle Scholar
  49. Slade RW (1992) Limited MHC polymorphism in the southern elephant seal: implications for MHC evolution marine mammal population biology. Proc R Soc Lond B 249(1325):163–171CrossRefGoogle Scholar
  50. Smith DM, Lunney JK, Ho CS, Martens GW, Ando A, Lee JH, Schook L, Renard C, Chardon P (2005) Nomenclature for factors of the swine leukocyte antigen class II system 2005. Tissue Antigens 66:623–639PubMedCrossRefGoogle Scholar
  51. Swarbrick PA, Crawford AM (1997) The red deer (Cervus elaphus) contains two expressed major histocompatibility complex class II DQB genes. Anim Genet 28:49–51PubMedCrossRefGoogle Scholar
  52. Swofford DL (2001) PAUP*: phylogenetic analysis using parsimony (and other methods). Versión 4.0. Sinauer, SunderlandGoogle Scholar
  53. Takahashi K, Rooney AP, Nei M (2000) Origins and divergence times of mammalian class II MHC gene clusters. J Hered 91:198–204PubMedCrossRefGoogle Scholar
  54. Takahata N (1990) A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Proc Natl Acad Sci USA 87:2419–2423PubMedCrossRefGoogle Scholar
  55. Takahata N, Satta Y, Klein J (1992) Polymorphism and balancing selection at major histocompatibility complex loci. Genetics 130:925–938PubMedGoogle Scholar
  56. Thewissen JGM, Cooper LN, Clementz MT, Bajpai S, Tiwari BN (2007) Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 450:1190–1194PubMedCrossRefGoogle Scholar
  57. Tovo-Rodrigues L, Rhode LA, Roman T, Schmitz M, Polanczyk G, Zeni C, Marques FZC, Contini V, Grevet EH, Belmonte-de-Abreu P, Bau CHD, Hutz MH (2011) Is there a role for rare variants in DRD4 gene in the susceptibility for ADHD? Searching for an effect of allelic heterogeneity. Mol Psychiatry 17(5):520–526PubMedCrossRefGoogle Scholar
  58. Trowsdale J, Groves V, Arnason A (1989) Limited MHC polymorphism in whales. Immunogenetics 29:19–24PubMedCrossRefGoogle Scholar
  59. Vassilakos D, Natoli A, Dahlheim M, Hoelzel AR (2009) Balancing and directional selection at exon-2 of the MHC DQB1among populations of odontocete cetaceans. Mol Biol Evol 26(3):681–689PubMedCrossRefGoogle Scholar
  60. Xu S, Sun P, Zhou K, Yang G (2007) Sequence variability at three MHC loci of finless porpoises (Neophocaena phocoenoides). Immunogenetics 59:581–592PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • María José Villanueva-Noriega
    • 1
    • 3
  • Charles Scott Baker
    • 2
    • 4
  • Luis Medrano-González
    • 1
    • 2
  1. 1.Departamento de Biología Evolutiva, Facultad de CienciasUniversidad Nacional Autónoma de MéxicoMéxicoMéxico
  2. 2.School of Biological SciencesUniversity of AucklandAucklandNew Zealand
  3. 3.Posgrado en Ciencias del Mar y LimnologíaUniversidad Nacional Autónoma de MéxicoMéxicoMéxico
  4. 4.Marine Mammal InstituteOregon State UniversityNewportUSA

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