MHC diversity and mate choice in the magellanic penguin, spheniscus magellanicus

Journal of Heredity

Volumn 103, Issue 6, 2012, Pages 759-768

  Knafler, Gabrielle J ^a   Clark, J Alan ^b   Boersma, P Dee ^c   Bouzat, Juan L ^a  

^a BOWLING GREEN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c FORDHAM UNIVERSITY   (United States)

Author keywords

disassortative mating; genetic diversity; major histocompatibilty complex

Indexed keywords

HLA DRB1 ANTIGEN; NUCLEOTIDE;

ALLELE; ARTICLE; BREEDING; CONTROLLED STUDY; FEMALE; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC DIFFERENCE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HETEROZYGOSITY; INFECTION RESISTANCE; MALE; MATE CHOICE; MOLECULAR CLONING; NATURAL SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PENGUIN; PHYLOGENY; POSITIVE SELECTION; PRIORITY JOURNAL; REPRODUCTIVE FITNESS; SEQUENCE ANALYSIS; SPHENISCUS MAGELLANICUS;

ANIMALS; ARGENTINA; FEMALE; GENES, MHC CLASS II; GENETIC VARIATION; GENETICS, POPULATION; HETEROZYGOTE; HLA-DRB1 CHAINS; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; REGRESSION ANALYSIS; SELECTION, GENETIC; SEXUAL BEHAVIOR, ANIMAL; SOFTWARE; SPHENISCIDAE;

SPHENISCIDAE; SPHENISCUS MAGELLANICUS; SPHENISCUS MENDICULUS;

EID: 84870530937     PISSN: 00221503     EISSN: 14657333     Source Type: Journal    
DOI: 10.1093/jhered/ess054     Document Type: Article

References (61)

1. Aguilar A. 2006. Patterns of variation in MHC class II beta loci of the little greenbul (Andropadus virens) with comments on MHC evolution in birds. J Hered. 97: 133-142.
2. Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK. 2004. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA. 101: 3490-3494.
3. Akst EP, Boersma PD, Fleischer RC. 2002. A comparison of genetic diversity between the Galapagos penguin and the Magellanic penguin. Conserv Genet. 3: 375-383.
4. Babik W, Durka W, Radwan J. 2005. Sequence diversity of the MHC DRB gene in the Eurasian beaver (Castor fiber). Mol Ecol. 14: 4249-4257.
5. Baker AJ, Pereira SL, Haddrath OP, Edge KA. 2006. Multiple gene evidence for expansion of extant penguins out of Antarctica due to global cooling. Proc R Soc Lond B Biol Sci. 273: 11-17.
6. Boersma PD, 2008. Penguins as marine sentinels. BioScience. 58: 597-607.
7. Boersma PD, Stokes, DL, Yorio P. 1990. Reproductive variability and historical change of Magellanic penguins (Spheniscus magellanicus) at Punta Tombo, Argentina. In: Davis L, Darby J, editors. Biology of Penguins. New York: Macmillan. p. 15-43.
8. Bollmer JL, Vargas FH, Parker PG. 2007. Low MHC variation in the endangered Galápagos penguin (Spheniscus mendiculus). Immunogenetics. 59: 593-602.
9. Brouwer L, Barr I, van de Pol M, Burke T, Komdeur J, Richardson DS. 2010. MHC-dependent survival in a wild population: evidence for hidden genetic benefits gained through extra-pair fertilizations. Mol Ecol. 19: 3444-3455.
10. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC. 1993. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature. 364: 33-39.
11. Burri R, Hirzel NH, Salamin N, Roulin A, Fumagalli L. 2008. Evolutionary patterns of MHC class II B in owls and their implications for the understanding of avian MHC evolution. Mol Biol Evol. 25: 1180-1191.
12. Consuegra S, de Leaniz CG. 2008. MHC-mediated mate choice increases parasite resistance in salmon. Proc Rl Soc Lond B Biol Sci. 275: 1397-1403.
13. Davies CJ, Andersson L, Ellis SA, Hensen EJ, Lewin HA, Mikko S, Muggli-Cockett NE, van der Poel JJ, Russell GC. 1997. Nomenclature for the factors of the BoLA system, 1996: report of the ISAG BoLA Nomenclature Committee. Anim. Genet. 28: 159-168.
14. Doherty PC, Zinkernagel RM. 1975. Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature. 256: 50-52.
15. Edwards SV, Hess CM, Gasper J, Garrigan J. 1999. Toward an evolutionary genomics of the avian Mhc. Immunol Rev. 167: 119-132.
16. Eizaguirre C, Yeates SE, Lenz TL, Kalbe, Milinski M. 2009. MHC-based mate choice combines good genes and maintenance of MHC polymorphism. Mol Ecol. 18: 3316-3329.
17. Ewald PW. 1994. The evolution of infectious disease. New York: Oxford University Press.
18. Felsenstein J. 2004. Inferring phylogenies. Sunderland (MA): Sinauer Associates.
19. Freeman-Gallant CR, Geguerdichian M, Wheelwright NT, Sollecito SV. 2003. Social-pairing and female fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. Mol Ecol. 12: 3077-3083.
20. Gandini PA, Frere E, Boersma PD. 1996. Status and conservation of Magellanic penguins (Spheniscus magellanicus) in Patagonia, Argentina. Bird Conserv Int. 6: 307-316.
21. Hall TA. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acid Sympos Series. 41: 95-98.
22. Hamilton WD, Zuk M. 1982. Heritable true fitness and bright birds: a role for parasites? Science. 218: 384-387.
23. Hawley DM, Fleischer RC. 2012. Contrasting epidemic histories reveal pathogen-mediated balancing selection on class II MHC diversity in a wild songbird. PLoS ONE 7(1): e30222, doi: 10.1371/journal.pone.0030222.
24. Hess CM, Edwards SV. 2002. The evolution of the major histocompatibility complex in birds. Bioscience. 52: 423-431.
25. Hughes AL, Yeager M. 1998. Natural selection at major histocompatibility complex of vertebrates. Annu Rev Genet. 32: 415-435.
26. Hughes CR, Miles S, Walbroehl JM. 2008. Support for the minimal essential MHC hypothesis: a parrot with a single, highly polymorphic MHC class II B gene. Immunogenetics. 60: 219-231.
27. Jukes TH, Cantor CR. 1969. Evolution of protein molecules. In: Munro HN, editor. Mammalian protein metabolism. New York: Academic Press. p. 21-123.
28. Kennedy LJ, Altet L, Angles JM, Barnes A, Carter SD, Francino O, Gerlach JA, Happ GM, Ollier WER, Polvi A, Thomson W, Wagner JL. 1999. Nomenclature for the factors of the Dog Major Histocompatibility system (DLA), 1998: first report of the ISAG DLA Nomenclature Committee. Tissue Antigens. 54: 312-321.
29. Kikkawa EF, Tsuda TT, Naruse TK, Sumiyama D, Fukuda M, Kurita M, Murata K, Wilson RP, LeMaho Y, Tsuda M, Kulski JK, Inoko H. 2005. Analysis of the sequence variations in the Mhc DRß1-like gene of the endangered Humboldt penguin (Spheniscus humboldti). Immunogenetics. 57: 99-107.
30. Kikkawa EF, Tsuda TT, Naruse TK, Sumiyama D, Fukuda M, Kurita M, Murata K, Wilson RP, LeMaho Y, Tsuda M, Kulski JK, Inoko H. 2009. Trans-species polymorphism of the Mhc class II DRB-like gene in banded penguins (genus Spheniscus). Immunogenetics. 61: 341-352.
31. Klein J, 1986. Natural history of the major histocombatibility complex. New York: John Wiley and Sons.
32. Klein J, Satta Y, Takahata N, O'hUigin C. 1993. Trans-specific MHC polymorphism and the origin of species in primates. J Med Primatol. 22: 57-64.
33. Landry C, Garant D, Duchesne P, Bernatchez L. 2001. "Good genes as heterozygosity": the major histocompatibility complex and mate choice in the Atlantic salmon (Salmo salar). Proc R Soc Lond B Biol Sci. 268: 1279-1285.
34. Lenz T, Becker S. 2008. Simple approach to reduce PCR artifact formation leads to reliable genotyping of MHC and other highly polymorphic loci-Implications for evolutionary analysis. Gene 427: 117-123.
35. Loisel DA, Alberts SC, Ober C. 2007. Functional significance of MHC variation in mate choice, reproductive outcome, and disease risk. In: Stearns SC, editor. Evolution in health and disease (2nd ed). Oxford, UK: Oxford University Press. p. 241-252.
36. Marsh SG, Bodmer JG, Albert ED, Bodmer WF, Bontrop RE, Dupont B, Erlich HA, Hansen JA, Mach B, Mayr WR, et al. 2001. Nomenclature for factors of the HLA system, 2000. Tissue Antigens. 57: 236-283.
37. Milinski M. 2006. The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol Syst. 37: 159-186.
38. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 3: 418-426.
39. Penn DJ, Potts WK. 1999. The evolution of mating preferences and major histocompatibility genes. Am Nat. 153: 145-164.
40. Penn DJ, Damjanovich K, Potts WK. 2002. MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc Nat Acad Sci. 99: 11260-11264.
41. Potti J, Moreno J, Yorio P, Briones V, Garci'a-Borborglu P, Villar S, Ballesteros C. 2002. Bacteria divert resources from growth for Magellanic penguin chicks. Ecol Lett. 5: 709-714.
42. Potts WK, Wakeland EK. 1993. The evolution of MHC genetic diversity: a tale of incest, pestilence, and sexual preference. Trends Genet. 9: 408-412.
43. Rozas J, Sanchez-DelBarrio C, Messeguer X, Rozas R. 2003. DnaSP, DNApolymorphism analyses by the coalescent and other methods. Bioinformatics. 19: 2496-2497.
44. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual (2nd ed). New York: Cold Spring Harbor Laboratory Press.
45. Schiavini AP, Yorio P, Gandini P, Rey A, Boersma PD. 2005. Los pingüinos de las costas argentinas: estado poblacional y conservación. Hornero. 20: 5-23.
46. Schneider SD, Rosseli D, Excoffier L. 2000. ARLEQUIN: a software for population genetic data analysis. University of Geneva, Geneva Switzerland. Available from: http://lgb.unige.ch/arlequin/.
47. Seutin G, White BN, Boag PT. 1991. Preservation of avian blood and tissue samples for DNA analyses. Can J Zool. 69: 82-90.
48. Snell GD. 1968. The H-2 locus of the mouse: observations and speculations concerning its comparative genetics and its polymorphism. Folia Biologica (Prague). 14: 335-358.
49. Stokes DL, Boersma PD. 1998. Nest-site characteristics and reproductive success in Magellanic penguins (Spheniscus magellanicus). Auk. 115: 34-49.
50. Takahata N, Nei M. 1990. Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics. 124: 967-978.
51. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 24: 1596-1599.
52. Tella JL, Forero MG, Bertellotti M, Donázar JA, Blanco G, Ceballos O. 2001. Offspring body condition and immunocompetence are negatively affected by high breeding densities in a colonial seabird: a multiscale approach. Proc R Soc Lond B Biol Sci. 268: 1455-1461.
53. Trivers RL. 1972. Parental investment and sexual selection. In: Campbell BG, editor. Sexual selection and the descent of man. Chicago: Aldine-Atherton. p. 136-179.
54. Trowsdale J. 1993. Genomic structure and function in the MHC. Trends Genet. 9: 117-122.
55. Tsuda TT, Tsuda M, Naruse T, Kawata H, Ando A, Shiina T, Fukuda M, Kurita M, LeMaho I, Kulski JK, Inoko, H. 2001. Phylogenetic analysis of penguin (Spheniscidae) species based on sequence variation in Mhc class II gene. Immunogenetics. 53: 712-716.
56. Van Buskirk RW, Nevitt GA. 2007. Evolutionary arguments for olfactory behavior in modern birds. ChemoSense. 10: 1-10.
57. von Schantz T, Wittzell H, Goransson G, Grahn M. 1997. Mate choice, male condition-dependent ornamentation and MHC in the pheasant. Hereditas (Lund). 127: 133-140.
58. Wakeland EK, Boehme S, She JX. 1990. The generation and maintenance of MHC class II gene polymorphism in rodents. Immunol Rev. 113: 39-46.
59. Wenzel B. 2006. Olfactory sensation in the Kiwi and other birds. Annals N.Y. Acad Sci. 188: 183-193.
60. Williams TD, Boersma PD. 1995. Magellanic penguin. In: Williams TD, editor. Bird families of the world, the penguins. Oxford, UK: Oxford University Press. p. 249-258.
61. Worley K, Collet J, Spurgin LG, Cornwallis C, Pizzari T, Richardson DS. 2010. MHC heterozygosity and survival in red junglefowl. Mol Ecol. 19(15): 3064-3075.