Female house sparrows "count on" male genes: Experimental evidence for MHC-dependent mate preference in birds

BMC Evolutionary Biology

Volumn 11, Issue 1, 2011, Pages

  Griggio, Matteo ^a,b   Biard, Clotilde ^a,c   Penn, Dustin J ^a,b   Hoi, Herbert ^a,b  

^a KONRAD LORENZ INSTITUTE FOR ETHOLOGY   (Austria)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; EXPERIMENTAL STUDY; FISH; FITNESS; MAJOR HISTOCOMPATIBILITY COMPLEX; MAMMAL; MATE CHOICE; OLFACTORY CUE; PASSERINE; POLYMORPHISM; SECONDARY SEXUAL CHARACTERISTICS; SELECTION;

AVES; MAMMALIA; PASSER DOMESTICUS;

ANIMAL; ARTICLE; FEMALE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENETICS; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MATE CHOICE; PHYSIOLOGY; SPARROW; SPECIES DIFFERENCE;

ANIMALS; FEMALE; GENETIC VARIATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MATING PREFERENCE, ANIMAL; POLYMORPHISM, GENETIC; SPARROWS; SPECIES SPECIFICITY;

EID: 79851510396     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-11-44     Document Type: Article

References (61)

1. The Descent of Man, and Selection in Relation to Sex. C Darwin, London: J. Murray 1871
2. A theory of mate choice based on heterozygosity. JL Brown, Behav Ecol 1997 8 60 65 10.1093/beheco/8.1.60
3. Parental investment and sexual selection. R Trivers, Sexual Selection and the Descent of Man (Aldine, Chicago), Campbell B, 1972 136 179
4. Parasites and sexual selection. WD Hamilton M Zuk, Nature 1989 341 289 290 10.1038/341289b0 2797147
5. The evolution of polyandry II: post-copulatory defences against genetic incom (Pubitemid 27067932)
6. Control of mating preferences in mice by genes in the major histocompatibility complex. K Yamazaki EA Boyse V Mike HT Thaler BJ Mathieson J Abbott J Boyse ZA Zayas, J Exp Med 1976 144 1324 1335 10.1084/jem.144.5.1324 1032893
7. Mating patterns in seminatural populations of mice influenced by MHC genotype. WK Potts CJ Manning EK Wakeland, Nature 1991 352 619 621 10.1038/352619a0 1865924 (Pubitemid 21912392)
8. MHC heterozygosity confers a selective advantage against multiple-strain infections. DJ Penn K Damjanovich WK Potts, Proc Natl Acad Sci USA 2002 99 11260 11264 10.1073/pnas.162006499 12177415 (Pubitemid 34920913)
9. Diverse MHC IIB allele repertoire increases parasite resistance and body condition in the Long-tailed giant rat (Leopoldamys sabanus). TL Lenz K Wells M Pfeiffer S Sommer, BMC Evol Biol 2009 9 269 10.1186/1471-2148-9-269 19930637
10. Parasite-mediated heterozygote advantage in an outbred songbird population. EA MacDougall-Shackleton EP Derryberry J Foufopoulos AP Dobson TP Hahn, Biol Lett 2005 1 105 107 10.1098/rsbl.2004.0264 17148140 (Pubitemid 41529995)
11. Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches. DM Hawley KV Sydenstricker GV Kollias AA Dhondt, Biol Lett 2005 1 326 329 10.1098/rsbl.2005.0303 17148199 (Pubitemid 41374895)
12. Inbreeding effects in wild populations. LF Keller DM Waller, Trends Ecol Evol 2002 17 230 241 10.1016/S0169-5347(02)02489-8 (Pubitemid 34270584)
13. The evolution of mating preferences and major histocompatibility genes. D Penn W Potts, Am Nat 1999 153 145 164 10.1086/303166 (Pubitemid 29139433)
14. 'Good genes as heterozygosity': the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). C Landry D Garant P Duchesne L Bernatchez, Proc R Soc Lond B 2001 268 1279 1285 10.1098/rspb.2001.1659 (Pubitemid 32622382)
15. Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. PB Aeschlimann MA Häberli TB Reusch T Boehm M Milinski, Behav Ecol Sociobiol 2003 54 119 126 (Pubitemid 36844447)
16. Influence of genetic dissimilarity in the reproductive success and mate choice of brown trout - females fishing for optimal MHC dissimilarity. LA Forsberg J Dannewitz E Petersson M Grahn, J Evol Biol 2007 20 1859 69 10.1111/j.1420-9101.2007.01380.x 17714303 (Pubitemid 47262855)
17. Mate choice for non-additive genetic benefits correlate with MHC dissimilarity in the rose bitterling (Rhodeus ocellatus). M Agbali M Reichard A Bryjov J Bryja C Smith, Evolution 2010 64 1683 1696 10.1111/j.1558-5646.2010. 00961.x 20148959
18. Major histocompatibility complex and mate choice in sand lizards. M Olsson T Madsen J Nordby E Wapstra B Ujvari H Wittsell, Proc R Soc Lond B 2003 270 254 S256 10.1098/rsbl.2003.0079
19. Opposites attract: MHC-associated mate choice in a polygynous primate. JM Setchell MJE Charpentier KM Abbott EJ Wickings LA Knapp, J Evol Biol 2010 23 136 148 10.1111/j.1420-9101.2009.01880.x 19891747
20. MHC and preferences for male odour in the bank vole. J Radwan A Tkacz A Kloch, Ethology 2008 114 827 833 10.1111/j.1439-0310.2008.01528.x
21. The major histocompatibility complex, sexual selection and mate choice. M Milinski, Ann Rev Ecol Syst 2006 37 159 186 10.1146/annurev.ecolsys.37.091305. 110242 (Pubitemid 44907616)
22. An Mhc Component to Kin Recognition and Mate Choice in Birds: Predictions, Progress, and Prospects. B Zelano SV Edwards, Am Nat 2002 160 Suppl 6 225 237 10.1086/342897 18707479
23. A female signal reflects MHC genotype in a social primate. E Huchard M Raymond J Benavides H Marshall LA Knapp G Cowlishaw, BMC Evol Biol 2010 10 96 10.1186/1471-2148-10-96 20374634
24. Major histocompatibility complex variation and mate choice in a lekking bird, the great snipe (Gallinago media). R Ekblom SA Saether M Grahn P Fiske JA Kalas J Hoglund, Mol Ecol 2004 13 3821 3828 10.1111/j.1365-294X.2004.02361.x 15548294 (Pubitemid 39569057)
25. No evidence of an MHC-based female mating preference in great reed warblers. H Westerdahl, Mol Ecol 2004 13 2465 2470 10.1111/j.1365-294X.2004. 02238.x 15245418 (Pubitemid 38946434)
26. MHC genotype and male ornamentation: genetic evidence for the Hamilton-Zuk model. T von Schantz H Wittzell G Göransson M Grahn K Persson, Proc R Soc Lond B 1996 263 265 271 10.1098/rspb.1996.0041 (Pubitemid 26100972)
27. Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. CR Freeman-Gallant M Meguerdichian NT Wheelwright SV Sollecito, Mol Ecol 2003 12 3077 3083 10.1046/j.1365-294X.2003.01968.x 14629387 (Pubitemid 37425077)
28. Complex Mhc-based mate choice in a wild passerine. C Bonneaud O Chastel P Federici H Westerdahl G Sorci, Proc R Soc Lond B 2006 273 1111 1116 10.1098/rspb.2005.3325 (Pubitemid 47324480)
29. MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. DS Richardson J Komdeur T Burke T von Schantz, Proc R Soc Lond B 2005 272 759 767 10.1098/rspb.2004.3028 (Pubitemid 41411134)
30. Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. N Schwensow M Eberle S Sommer, Proc R Soc Lond B 2008 275 555 564 10.1098/rspb.2007.1433 (Pubitemid 351156528)
31. Atlantic salmon eggs favour sperm in competition that have similar major histocompatibility alleles. SE Yeates S Einum IA Fleming HJ Megens RJM Stet K Hindar WV Holt KJW Van Look MJG Gage, Proc R Soc Lond B 2009 276 559 566 10.1098/rspb.2008.1257
32. Is the peacock's train an honest signal of genetic quality at the major histocompatibility complex? ML Hale MH Verduijn AP Møller K Wolff M Petrie, J Evol Biol 2009 22 1284 1294 10.1111/j.1420-9101.2009.01746.x 19453370
33. Cryptic preference for MHC-dissimilar females in male red junglefowl, Gallus gallus. MAF Gillingham DS Richardson H Løvlie A Moynihan K Worley T Pizzari, Proc R Soc Lond B 2009 276 1083 1092 10.1098/rspb.2008.1549
34. Disentangling the role of MHC-dependent 'good genes' and 'compatible genes' in mate-choice decisions of three-spined sticklebacks Gasterosteus aculeatus under semi-natural conditions. TL Lenz C Eizaguirre JP Scharsack M Kalbe M Milinski, J Fish Biol 2009 75 2122 2142 10.1111/j.1095-8649.2009.02410.x 20738677
35. Parasite selection for immunogenetic optimality. KM Wegner M Kalbe J Kurtz TB Reusch M Milinski, Science 2003 301 1343 10.1126/science.1088293 12958352 (Pubitemid 37075801)
36. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. T Reusch M Häberli P Aeschlimann M Milinski, Nature 2001 414 300 302 10.1038/35104547 11713527 (Pubitemid 33097804)
37. Comment on "Parasite selection for immunogenetic optimality". PW Hedrick, Science 2004 303 957 author reply 957 10.1126/science.1092163 14963312
38. An Mhc class I allele associated to the expression of T-dependent immune response in the house sparrow. C Bonneaud M Richard B Faivre H Westerdahl G Sorci, Immunogenetics 2005 57 782 789 10.1007/s00251-005-0046-5 16189664 (Pubitemid 41598624)
39. Sexual selection and condition-dependent mate preferences. S Cotton J Small A Pomiankowski, Curr Biol 2006 16 755 765 10.1016/j.cub.2006.08.022 16631582
40. Variation in female choice of mates: condition influences selectivity. NT Burley VS Foster, Anim Behav 2006 72 713 719 10.1016/j.anbehav.2006.01.017 (Pubitemid 44311100)
41. Condition-related mate choice in sticklebacks. TCM Bakker R Kunzler D Mazzi, Nature 1999 401 234 10.1038/45727 (Pubitemid 29444269)
42. Low-quality females prefer low-quality males when choosing a mate. MJ Holveck K Riebel, Proc R Soc Lond B 2010 277 153 160 10.1098/rspb.2009.1222
43. Females prefer the scent of outbred males: good-genes-as-heterozygosity? P Ilmonen G Stundner M Thoss DJ Penn, BMC Evol Biol 2009 9 104 10.1186/1471-2148-9-104 19445699
44. Only females in poor condition display a clear preference and prefer males with an average badge. M Griggio H Hoi, BMC Evol Biol 2010 10 261 20799928
45. The underestimated role of olfaction in avian reproduction? J Balthazart M Taziaux, Behav Brain Res 2009 200 248 259 10.1016/j.bbr.2008.08.036 18804490
46. A tangerine-scented social odour in a monogamous seabird. JC Hagelin IL Jones LEL Rasmussen, Proc R Soc Lond B 2003 270 1323 1329 10.1098/rspb.2003.2379 (Pubitemid 36831293)
47. Atypical homing or self-odour avoidance? Blue petrels (Halobaena caerulea) are attracted to their mate's odour but avoid their own. J Mardon F Bonadonna, Behav Ecol Sociobiol 2009 63 537 542 10.1007/s00265-008-0688-z
48. Songbird chemosignals: volatile compounds in preen gland secretions vary among individuals, sexes, and populations. DJ Whittaker HA Soini JW Atwell C Hollars MV Novotny ED Ketterson, Behav Ecol 2010 21 608 614 10.1093/beheco/ arq033
49. Mate choice and genetic quality: a review of the heterozygosity theory. B Kempenaers, Adv Study Behav 2007 37 189 277 full-text
50. Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus). C Bonneaud G Sorci V Morin H Westerdahl R Zoorob H Wittzell, Immunogenetics 2004 55 855 865 10.1007/s00251-004-0648-3 14963619 (Pubitemid 38650991)
51. Antagonistic effects of a Mhc class I allele on malaria-infected house sparrows. C Loiseau R Zoorob S Garnier J Birard P Federici J Julliard G Sorci, Ecol Lett 2008 11 258 265 10.1111/j.1461-0248.2007.01141.x 18070099 (Pubitemid 351172047)
52. Polymorphism and signature of selection in the MHC class I genes of the three-spined stickleback Gasterosteus aculeatus. H Schaschl KM Wegner, J Fish Biol 2006 69 Suppl. B 177 188 10.1111/j.1095-8649.2006.01223.x (Pubitemid 44924214)
53. Polymorphic MHC loci in an asexual fish, the amazon molly (Poecilia formosa; Poeciliidae). H Schaschl M Tobler M Plath DJ Penn I Schlupp, Mol Ecol 2008 17 5220 5230 10.1111/j.1365-294X.2008.03997.x 19120996
54. Universal method for producing ROX-labeled size standards suitable for automated genotyping. JA DeWoody J Schupp L Kenefic J Busch L Murfitt P Keim, Biotechniques 2004 37 348 352 15470886 (Pubitemid 39180905)
55. Fourteen polymorphic microsatellite loci characterized in the house sparrow Passer domesticus (Passeridae, Aves). SC Griffith DA Dawson H Jensen N Ockendon C Greig K Neumann T Burke, Mol Ecol Notes 2007 7 333 336 10.1111/j.1471-8286.2006.01598.x (Pubitemid 46339159)
56. Major histocompatibility alleles associated with local resistance to malaria in a passerine. C Bonneaud J Perez-Tris P Federici O Chastel G Sorci, Evolution 2006 60 383 389 16610328 (Pubitemid 44804560)
57. Female ornamentation and directional male mate preference in the rock sparrow. M Griggio A Devigili H Hoi A Pilastro, Behav Ecol 2009 20 1072 1078 10.1093/beheco/arp099
58. Dual utility of a melanin-based ornament in bearded tits. H Hoi M Griggio, Ethology 2008 114 1094 1100 10.1111/j.1439-0310.2008.01566.x
59. Armaments and ornaments in the rock sparrow: a possible dual utility of a carotenoid-based feather signal. M Griggio L Serra D Licheri A Monti A Pilastro, Behav Ecol Sociobiol 2007 61 423 433 10.1007/s00265-006-0270-5 (Pubitemid 44953015)
60. Plumage maintenance affects ultraviolet colour and female preference in the budgerigar. M Griggio H Hoi A Pilastro, Behav Process 2010 84 739 744 10.1016/j.beproc.2010.05.003
61. White tail markings are an indicator of quality and affect mate preference in rock sparrows. M Griggio F Valera A Casas-Crivillé H Hoi A Barbosa, Behav Ecol Sociobiol