Female promiscuity is positively associated with neutral and selected genetic diversity in passerine birds

Evolution

Volumn 67, Issue 5, 2013, Pages 1406-1419

  Gohli, Jostein ^a   Anmarkrud, Jarl A ^a,b   Johnsen, Arild ^a   Kleven, Oddmund ^a,c   Borge, Thomas ^d   Lifjeld, Jan T ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c NORWEGIAN INSTITUTE FOR NATURE RESEARCH   (Norway)

^d Merck Serono Analytical Development Center of Expertise   (Norway)

Author keywords

Balancing selection; Compatible genes; Extrapair paternity; MHC; Pathogen mediated selection; Sperm competition

Indexed keywords

DNA BINDING PROTEIN;

EXTRA-PAIR COPULATION; FEMALE BEHAVIOR; GENETIC VARIATION; GOOD GENES HYPOTHESIS; INTERSPECIFIC VARIATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MATING BEHAVIOR; NATURAL SELECTION; PASSERINE; PATERNITY; PATHOGEN; SPERM COMPETITION;

ANIMAL; ARTICLE; FEMALE; GENE; GENE FREQUENCY; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; INTRON; MALE; MATE CHOICE; SPARROW;

ANIMALS; DNA-BINDING PROTEINS; FEMALE; GENE FREQUENCY; GENES, MHC CLASS II; GENETIC VARIATION; INTRONS; MALE; MATING PREFERENCE, ANIMAL; SELECTION, GENETIC; SPARROWS;

AVES; PASSERIFORMES;

EID: 84876843036     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12045     Document Type: Article

References (125)

1. Akcay, E., and J. Roughgarden. 2007. Extra-pair paternity in birds: review of the genetic benefits. Evol. Ecol. Res. 9:855-868.
2. Albrecht, T., J. Scnitzer, J. Kreisinger, A. Exnerová, J. Bryja, and P. Munclinger. 2007. Extra-pair paternity and the opportunity for sexual selection in long-distant migratory passerines. Behav. Ecol. 18:477-486.
3. Alcaide, M., S. V. Edwards, and J. J. Negro. 2007. Characterization, polymorphism, and evolution of MHC class II B genes in birds of prey. J. Mol. Evol. 65:541-554.
4. Alcaide, M., S. V. Edwards, J. J. Negro, D. Serrano, and J. L. Tella. 2008. Extensive polymorphism and geographical variation at a positively selected MHC class II B gene of the lesser kestrel (Falco naumanni). Mol. Ecol. 17:2652-2665.
5. Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ.
6. Anmarkrud, J. A., A. Johnsen, L. Bachmann, and J. T. Lifjeld. 2010. Ancestral polymorphism in exon 2 of bluethroat (Luscinia svecica) MHC class II B genes. J. Evol. Biol. 23:1206-1217.
7. Arnqvist, G., and M. Kirkpatrick. 2005. The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females. Am. Nat. 165:26-37.
8. Babik, W., P. Taberlet, M. J. Ejsmond, and J. Radwan. 2009. New generation sequencers as a tool for genotyping of highly polymorphic multilocus MHC system. Mol. Ecol. Res. 9:713-719.
9. Balakrishnan, C., R. Ekblom, M. Volker, H. Westerdahl, R. Godinez, H. Kotkiewicz, D. Burt, T. Graves, D. Griffin, W. Warren, et al. 2010. Gene duplication and fragmentation in the zebra finch major histocompatibility complex. BMC Biol. 8:29.
10. Birkhead, T. R., and T. Pizzari. 2002. Postcopulatory sexual selection. Nat. Rev. Genet. 3:262-273.
11. Blomqvist, D., M. Andersson, C. Kupper, I. C. Cuthill, J. Kis, R. B. Lanctot, B. K. Sandercock, T. Szekely, J. Wallander, and B. Kempenaers. 2002. Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419:613-615.
12. Bollmer, J., F. Vargas, and P. Parker. 2007. Low MHC variation in the endangered Galápagos penguin (Spheniscus mendiculus). Immunogenetics 59:593-602.
13. Bollmer, J. L., P. O. Dunn, L. A. Whittingham, and C. Wimpee. 2010. Extensive MHC class II B gene duplication in a passerine, the common yellowthroat (Geothlypis trichas). J. Hered. 101:448-460.
14. Bonneaud, C., O. Chastel, P. Federici, H. Westerdahl, and G. Sorci. 2006. Complex Mhc-based mate choice in a wild passerine Proc. R. Soc. Lond. B 273:1111-1116.
15. Borge, T., M. T. Webster, G. Andersson, and G. P. Saetre. 2005. Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species. Genetics 171:1861-1873.
16. Brouwer, L., I. Barr, M. Van De Pol, T. Burke, J. A. N. Komdeur, and D. S. Richardson. 2010. MHC-dependent survival in a wild population: evidence for hidden genetic benefits gained through extra-pair fertilizations. Mol. Ecol. 19:3444-3455.
17. Brown, J. H., T. S. Jardetzky, J. C. Gorga, L. J. Stern, R. G. Urban, J. L. Strominger, and D. C. Wiley. 1993. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33-39.
18. Burri, R., H. N. Hirzel, N. Salamin, A. Roulin, and L. Fumagalli. 2008a. 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.
19. Burri, R., H. Niculita-Hirzel, A. Roulin, and L. Fumagalli. 2008b. Isolation and characterization of major histocompatibility complex (MHC) class II B genes in the barn owl (Aves: Tyto alba). Immunogenetics 60:543-550.
20. Calhim, S., S. Immler, and T. R. Birkhead. 2007. Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS ONE 2:e413.
21. Canal, D., M. Alcaide, J. A. Anmarkrud, and J. Potti. 2010. Towards the simplification of MHC typing protocols: targeting classical MHC class II genes in a passerine, the pied flycatcher Ficedula hypoleuca. BMC Res. Notes 3:236.
22. Chapman, J. R., S. Nakagawa, D. W. Coltman, J. Slate, and B. C. Sheldon. 2009. A quantitative review of heterozygosity-fitness correlations in animal populations. Mol. Ecol. 18:2746-2765.
23. Charlesworth, B. 2009. Effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10:195-205.
24. Charlesworth, B., and D. Charlesworth. 2010. Elements of evolutionary genetics. Roberts and Co. Publishers, Greenwood Village, CO.
25. Charlesworth, D. 2006. Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet. 2:e64.
26. Chenoweth, S. F., and K. McGuigan. 2010. The genetic basis of sexually selected variation. Ann. Rev. Ecol. Evol. Syst. 41:81-101.
27. Corl, A., and H. Ellegren. 2012. The genomic signature of sexual selection in the genetic diversity of the sex chromosomes and autosomes. Evolution 66:2138-2149.
28. David, P. 1998. Heterozygosity-fitness correlations: new perspectives on old problems. Heredity 80:531-537.
29. Dunn, P. O., J. L. Bollmer, C. R. Freeeman-Gallant, and L. A. Whittingham. 2012. MHC variation is related to a sexually selected ornament, survival and parasite resistance in common yellowthroats. Evolution. DOI: 10.1111/j.1558-5646.2012.01799.x.
30. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
31. Eizaguirre, C., T. L. Lenz, M. Kalbe, and M. Milinski. 2012. Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat. Comm. 3:621.
32. Ekblom, R., S. A. Saether, P. A. R. Jacobsson, P. Fiske, T. Sahlman, M. Grahn, J. A. Kalas, and J. Höglund. 2007. Spatial pattern of MHC class II variation in the great snipe (Gallinago media). Mol. Ecol. 16:1439-1451.
33. Foerster, K., K. Delhey, A. Johnsen, J. T. Lifjeld, and B. Kempenaers. 2003. Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714-717.
34. Fossøy, F., A. Johnsen, and J. T. Lifjeld. 2008. Multiple genetic benefits of female promiscuity in a socially monogamous passerine. Evolution 62:145-156.
35. Freckleton, R. P., P. H. Harvey, and M. Pagel. 2002. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160:712-726.
36. Freeman-Gallant, C. R., M. Meguerdichian, N. T. Wheelwright, and S. V. Sollecito. 2003. Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. J. Mol. Evol. 12:3077-3083.
37. Freeman-Gallant, C. R., N. T. Wheelwright, K. E. Meiklejohn, S. L. States, and S. V. Sollecito. 2005. Little effect of extrapair paternity on the opportunity for sexual selection in savannah sparrows (Passerculus sandwichensis). Evolution 59:422-430.
38. Freeman-Gallant, C. R., N. T. Wheelwright, K. E. Meiklejohn, and S. V. Sollecito. 2006. Genetic similarity, extrapair paternity, and offspring quality in Savannah sparrows (Passerculus sandwichensis). Behav. Ecol. 17:952-958.
39. Garamszegi, L. Z., and C. L. Nunn. 2011. Parasite-mediated evolution of the functional part of the MHC in primates. J. Evol. Biol. 24:184-195.
40. Garvin, J. C., B. Abroe, M. C. Pedersen, P. O. Dunn, and L. A. Whittingham. 2006. Immune response of nestling warblers varies with extra-pair paternity and temperature. Mol. Ecol. 15:3833-3840.
41. Gaudieri, S., R. L. Dawkins, K. Habara, J. K. Kulski, and T. Gojobori. 2000. SNP profile within the human major histocompatibility complex reveals an extreme and interrupted level of nucleotide diversity. Genome Res. 10:1579-1586.
42. Gerlach, N. M., J. W. McGlothlin, P. G. Parker, and E. D. Ketterson. 2011. Promiscuous mating produces offspring with higher lifetime fitness. Proc. R. Soc. Lond. B 279:860-866.
43. Gillespie, J. H. 1991. The causes of molecular evolution. Oxford Univ. Press, New York.
44. Goüy De Bellocq, J., N. Charbonnel, and S. Morand. 2008. Coevolutionary relationship between helminth diversity and MHC class II polymorphism in rodents. J. Evol. Biol. 21:1144-1150.
45. Gowaty, P. A. 1996. Battles of the sexes and origins of monogamy. Pp. 21-52 in J. M. Black, ed. Partnerships in birds: the study of monogamy. Oxford Univ. Press, Oxford, UK.
46. Griffith, S. C., I. P. F. Owens, and K. A. Thuman. 2002. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11:2195-2212.
47. Hansson, B., and L. Westerberg. 2002. On the correlation between heterozygosity and fitness in natural populations. Mol. Ecol. 11:2467-2474.
48. Hasselquist, D., S. Bensch, and T. Von Schantz. 1995. Low frequency of extrapair paternity in the polygynous great reed warbler, Acrocephalus arundinaceus. Behav. Ecol. 6:27-38.
49. Hawley, D. M., and R. C. Fleischer. 2012. Contrasting epidemic histories reveal pathogen-mediated balancing selection on class II MHC diversity in a wild songbird. PLoS ONE 7:e30222.
50. Heath, L., E. van der Walt, A. Varsani, and D. P. Martin. 2006. Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J. Virol. 80:11827-11832.
51. Hill, W. G., and A. Robertson. 1966. The effect of linkage on limits to artificial selection. Genet. Res. 8:269-294.
52. Hogner, S., S. A. Sæther, T. Borge, T. Bruvik, A. Johnsen, and G.-P. Sætre. 2012. Increased divergence but reduced variation on the Z chromosome relative to autosomes in Ficedula flycatchers: differential introgression or the faster-Z effect?. Ecol. Evol. 2:379-396.
53. Hughes, C., S. Miles, and J. Walbroehl. 2008. Support for the minimal essential MHC hypothesis: a parrot with a single, highly polymorphic MHC class II B gene. Immunogenetics 60:219-231.
54. Jenkins, T., G. H. Thomas, O. Hellgren, and I. P. F. Owens. 2012. Migratory behavior of birds affects their coevolutionary relationship with blood parasites. Evolution 66:740-751.
55. Jennions, M. D., and M. Petrie. 2000. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75:21-64.
56. Johnsen, A., and J. T. Lifjeld. 2003. Ecological constraints on extra-pair paternity in the bluethroat. Oecologia 136:476-483.
57. Johnsen, A., V. Andersen, C. Sunding, and J. T. Lifjeld. 2000. Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296-299.
58. Kalbe, M., C. Eizaguirre, I. Dankert, T. B. H. Reusch, R. D. Sommerfeld, K. M. Wegner, and M. Milinski. 2009. Lifetime reproductive success is maximized with optimal major histocompatibility complex diversity. Proc. R. Soc. Lond. B 276:925-934.
59. Kaufman, J., S. Milne, T. W. F. Gobel, B. A. Walker, J. P. Jacob, C. Auffray, R. Zoorob, and S. Beck. 1999. The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923-925.
60. Kempenaers, B. 2007. Mate choice and genetic quality: a review of the heterozygosity theory. Adv. Study Behav. 37:189-278.
61. Kikkawa, E., T. Tsuda, D. Sumiyama, T. Naruse, M. Fukuda, M. Kurita, R. Wilson, Y. LeMaho, G. Miller, M. Tsuda, et al. 2009. Trans-species polymorphism of the Mhc class II DRB-like gene in banded penguins (genus Spheniscus). Immunogenetics 61:341-352.
62. Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge Univ. Press, New York.
63. Kirkpatrick, M., and D. W. Hall. 2004. Sexual selection and sex linkage. Evolution 58:683-691.
64. Kirkpatrick, M., and M. J. Ryan. 1991. The evolution of mating preferences and the paradox of the lek. Nature 350:33-38.
65. Klein, J. 1986. Natural history of the histocompatibility complex. Wiley, New York.
66. Kleven, O., T. Laskemoen, F. Fossøy, R. J. Robertson, and J. T. Lifjeld. 2008. Intraspecific variation in sperm length is negatively related to sperm competition in passerine birds. Evolution 62:494-499.
67. Kokko, H., M. D. Jennions, and R. Brooks. 2006. Unifying and testing models of sexual selection. Ann. Rev. Ecol. Evol. Syst. 37:43-66.
68. Kotiaho, J. S., N. R. LeBas, M. Puurtinen, and J. L. Tomkins. 2008. On the resolution of the lek paradox. Trends Ecol. Evol. 23:1-3.
69. Lampila, S., M. Orell, and L. Kvist. 2011. Willow tit Parus montanus extrapair offspring are more heterozygous than their maternal half-siblings. J. Avian Biol. 42:355-362.
70. Laskemoen, T., T. Albrecht, A. Bonisoli-Alquati, J. Cepak, F. Lope, I. G. Hermosell, L. E. Johannessen, O. Kleven, A. Marzal, T. A. Mousseau, et al. 2013. Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations. Behav. Ecol. Sociobiol.: In press. DOI: 10.1007/s002652013012-145020130.
71. Leffler, E. M., K. Bullaughey, D. R. Matute, W. K. Meyer, L. Ségurel, A. Venkat, P. Andolfatto, and M. Przeworski. 2012. Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol. 10:e1001388.
72. Lenz, T. L., and S. Becker. 2008. Simple approach to reduce PCR artefact formation leads to reliable genotyping of MHC and other highly polymorphic loci-implications for evolutionary analysis. Gene 427:117-123.
73. Librado, P., and J. Rozas. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
74. Lifjeld, J. T., T. Laskemoen, O. Kleven, T. Albrecht, and R. J. Robertson. 2010. Sperm length variation as a predictor of extrapair paternity in passerine birds. PLoS ONE 5:e13456.
75. Lively, C. M., and M. F. Dybdahl. 2000. Parasite adaptation to locally common host genotypes. Nature 405:679-681.
76. Lombardo, M. P. 1998. On the evolution of sexually transmitted diseases in birds. J. Avian Biol. 29:314-321.
77. Malnati, M., M. Peruzzi, K. Parker, W. Biddison, E. Ciccone, A. Moretta, and E. Long. 1995. Peptide specificity in the recognition of MHC class I by natural killer cell clones. Science 267:1016-1018.
78. Marshall, R. C., K. L. Buchanan, and C. K. Catchpole. 2003. Sexual selection and individual genetic diversity in a songbird. Proc. R. Soc.Lond. B 270:S248-S250.
79. Masters, B. S., B. G. Hicks, L. S. Johnson, and L. A. Erb. 2003. Genotype and extra-pair paternity in the house wren: a rare-male effect? Proc. R. Soc. Lond. B 270:1393-1397.
80. Neff, B. D., and T. E. Pitcher. 2005. Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol. Ecol. 14:19-38.
81. Nei, M., and T. Gojobori. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3:418-426.
82. Nowak, M. A., K. Tarczy-Hornoch, and J. M. Austyn. 1992. The optimal number of major histocompatibility complex molecules in an individual Proc. Natl. Acad. Sci. USA 89:10896-10899.
83. Nunney, L. 1993. The influence of mating systems and overlapping generations on effective population size. Evolution 47:1329-1341.
84. Øigarden, T., T. Borge, and J. T. Lifjeld. 2010. Extrapair paternity and genetic diversity: the white-throated dipper Cinclus cinclus. J. Avian Biol. 41:248-257.
85. Olano-Marin, J., J. C. Mueller, and B. Kempenaers. 2011. Correlations between heterozygosity and reproductive success in the blue tit (Cyanistes caeruleus): an analysis of inbreeding and single locus effects. Evolution 65:3175-3194.
86. Ortego, J., G. Calabuig, R. Bonal, A. Munoz, J. M. Aparicio, and P. J. Cordero. 2009. Temporal variation of heterozygosity-based assortative mating and related benefits in a lesser kestrel population. J. Evol. Biol. 22:2488-2495.
87. Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature 401:877-884.
88. Paradis, E., J. Claude, and K. Strimmer. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290.
89. Penn, D. J., and W. K. Potts. 1999. The evolution of mating preferences and major histocompatibility complex genes. Am. Nat. 153:145-164.
90. Petrie, M., C. Doums, and A. P. Møller. 1998. The degree of extra-pair paternity increases with genetic variability. Proc. Natl. Acad. Sci. USA 95:9390-9395.
91. Petrie, M., and B. Kempenaers. 1998. Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol. Evol. 13:52-58.
92. Piertney, S. B., and M. K. Oliver. 2005. The evolutionary ecology of the major histocompatibility complex. Heredity 96:7-21.
93. Primmer, C. R., T. Borge, J. Lindell, and G. P. Sætre. 2002. Single-nucleotide polymorphism characterization in species with limited available sequence information: high nucleotide diversity revealed in the avian genome. Mol. Ecol. 11:603-612.
94. Promerová, M., M. Vinkler, J. Bryja, R. Poláková, J. Schnitzer, P. Munclinger, and T. Albrecht. 2011. Occurrence of extra-pair paternity is connected to social male's MHC-variability in the scarlet rosefinch Carpodacus erythrinus.J. Avian Biol. 42:5-10.
95. Pryke, S. R., L. A. Rollins, and S. C. Griffith. 2010. Females use multiple mating and genetically loaded sperm competition to target compatible genes. Science 329:964-967.
96. Qvarnström, A., A. M. Rice, and H. Ellegren. 2010. Speciation in Ficedula flycatchers. Phil. Trans. R. Soc. Lond. B 365:1841-1852.
97. R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria, ISBN 3-900051-00-3.
98. Reeve, H. K., and D. W. Pfennig. 2003. Genetic biases for showy males: are some genetic systems especially conductive to sexual selection? Proc. Natl. Acad. Sci. USA 100:1089-1094.
99. Revell, L. J. 2009. Size-correction and principal components for interspecific comparative studies. Evolution 63:3258-3268.
100. Richardson, D. S., F. L. Jury, K. Blaakmeer, J. Komdeur, and T. Burke. 2001. Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Mol. Ecol. 10:2263-2273.
101. Richardson, D. S., J. Komdeur, and T. Burke. 2004. Inbreeding in the Seychelles warbler: environment-depending maternal effects. Evolution 58:2037-2048.
102. Richardson, D. S., J. Komdeur, T. Burke, and T. von Schantz. 2005. MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc. R. Soc. Lond. B 272:759-767.
103. Robinson, J., M. J. Waller, P. Parham, N. de Groot, R. Bontrop, L. J. Kennedy, P. Stoehr, and S. G. E. Marsh. 2003. IMGT/HLA and IMGT/MHC: sequence databases for the study of the major histocompatibility complex. Nucleic. Acids Res. 31:311-314.
104. Rozas, J., J. C. Sánche-DelBarrio, X. Messeguer, and R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497.
105. Sætre, G. P., T. Borge, K. Lindroos, J. Haavie, B. C. Sheldon, C. Primmer, and A. C. Syvanen. 2003. Sex chromosome evolution and speciation in Ficedula flycatchers. Proc. R. Soc. Lond. B 270:53-59.
106. Sellis, D., B. J. Callahan, D. A. Petrov, and P. W. Messer. 2011. Heterozygote advantage as a natural consequence of adaptation in diploids. Proc. Natl. Acad. Sci. USA 108:20666-20671.
107. Sheldon, B. C. 1993. Sexually transmitted disease in birds: occurrence and evolutionary significance. Phil. Trans. R. Soc. Lond. B 339:491-497.
108. Šimková, A., E. Ottová, and S. Morand. 2006. MHC variability, life-traits and parasite diversity of European cyprinid fish. Evol. Ecol. 20:465-477.
109. Slatkin, M. 1995. Hitchhiking and associative overdominance at a microsatellite locus. Mol. Biol. Evol. 12:473-480.
110. Spottiswoode, C., and A. P. Møller. 2004. Extrapair paternity, migration, and breeding synchrony in birds. Behav. Ecol. 15:41-57.
111. Spurgin, L. G., and D. S. Richardson. 2010. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc. R. Soc. Lond. B 277:979-988.
112. Stapleton, M. K., O. Kleven, J. T. Lifjeld, and R. J. Robertson. 2007. Female tree swallows (Tachycineta bicolor) increase offspring heterozygosity through extrapair mating. Behav. Ecol. Sociobiol. 61:1725-1733.
113. Strand, T., H. Westerdahl, J. Höglund, R.V. Alatalo, and H. Siitari. 2007. The Mhc class II of the black grouse (Tetrao tetrix) consists of low numbers of B and Y genes with variable diversity and expression. Immunogenetics 59:725-734.
114. Sundstrõm, H., M. T. Webster, and H. Ellegren. 2004. Reduced variation on the chicken Z chromosome. Genetics 167:377-385.
115. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
116. Tarvin, K. A., M. S. Webster, E. M. Tuttle, and S. Pruett-Jones. 2005. Genetic similarity of social mates predicts the level of extrapair paternity in splendid fairy-wrens. Anim. Behav. 70:945-955.
117. Tong, J., J. Bramson, D. Kanduc, S. Chow, A. Sinha, and S. Ranganathan. 2006. Modeling the bound conformation of pemphigus vulgaris-associated peptides to MHC Class II DR and DQ Alleles. Immunome Research 2:1.
118. Trivers, R. L. 1972. Parental investment and sexual selection. Pp. 136-179 in B. Campbell, ed. Sexual selection and the descent of man 1871-1971. Aldine, Chicago.
119. Westerdahl, H. 2004. No evidence of an MHC-based female mating preference in great reed warblers. Mol. Ecol. 13:2465-2470.
120. Westerdahl, H. 2007. Passerine MHC: genetic variation and disease resistance in the wild. J. Ornithol. 148:469-477.
121. Westneat, D. F., and P. W. Sherman. 1997. Density and extra-pair fertilizations in birds: a comparative analysis. Behav. Ecol. Sociobiol. 41:205-215.
122. Westneat, D. F., and I. R. K. Stewart. 2003. Extra-pair paternity in birds: causes, correlates, and conflict. Annu. Rev. Ecol. Evol. Syst. 34:365-396.
123. Wetzel, D. P., I. R. Stewart, and D. F. Westneat. 2012. Heterozygosity predicts clutch and egg size but not plasticity in a house sparrow population with no evidence of inbreeding. Mol. Ecol. 21:406-420.
124. Zagalska-Neubauer, M., W. Babik, M. Stuglik, L. Gustafsson, M. Cichon, and J. Radwan. 2010. 454 sequencing reveals extreme complexity of the class II major histocompatibility complex in the collared flycatcher. BMC Evol. Biol. 10:395.
125. Ziegler, A., H. Kentenich, and B. Uchanska-Ziegler. 2005. Female choice and the MHC. Trends Immunol. 26:496-502.