BMC Evolutionary Biology | |
Females tend to prefer genetically similar mates in an island population of house sparrows | |
Gabriele Sorci2  Stéphane Garnier2  Arnaud Grégoire1  Marie Belvalette2  Elise Cellier-Holzem2  Luc Dunoyer2  Yoshan Moodley3  Dustin J Penn3  Coraline Bichet2  | |
[1] CEFE, UMR-CNRS 5175, Université de Montpellier 2, 1919 route de Mende, 34293 Montpellier, France;Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France;Konrad Lorenz Institute of Ethology, Department of Integrative Biology and Evolution, University of Veterinary Medicine, Savoyenstr 1a, Vienna A-1160, Vienna, Austria | |
关键词: Extra-pair paternity; Microsatellites; Major Histocompatibility Complex (MHC); Passer domesticus; Mate choice; Sexual selection; | |
Others : 857779 DOI : 10.1186/1471-2148-14-47 |
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received in 2013-04-30, accepted in 2014-03-04, 发布年份 2014 | |
【 摘 要 】
Background
It is often proposed that females should select genetically dissimilar mates to maximize offspring genetic diversity and avoid inbreeding. Several recent studies have provided mixed evidence, however, and in some instances females seem to prefer genetically similar males. A preference for genetically similar mates can be adaptive if outbreeding depression is more harmful than inbreeding depression or if females gain inclusive fitness benefits by mating with close kin. Here, we investigated genetic compatibility and mating patterns in an insular population of house sparrow (Passer domesticus), over a three-year period, using 12 microsatellite markers and one major histocompability complex (MHC) class I gene. Given the small population size and the distance from the mainland, we expected a reduced gene flow in this insular population and we predicted that females would show mating preferences for genetically dissimilar mates.
Results
Contrary to our expectation, we found that offspring were less genetically diverse (multi-locus heterozygosity) than expected under a random mating, suggesting that females tended to mate with genetically similar males. We found high levels of extra-pair paternity, and offspring sired by extra-pair males had a better fledging success than those sired by the social male. Again, unexpectedly, females tended to be more closely related to extra-pair mates than to their social mates. Our results did not depend on the type of genetic marker used, since microsatellites and MHC genes provided similar results, and we found only little evidence for MHC-dependent mating patterns.
Conclusions
These results are in agreement with the idea that mating with genetically similar mates can either avoid the disruption of co-adapted genes or confer a benefit in terms of kin selection.
【 授权许可】
2014 Bichet et al.; licensee BioMed Central Ltd.
【 预 览 】
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20140723084443920.pdf | 298KB | download | |
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【 图 表 】
【 参考文献 】
- [1]Andersson MB: Sexual Selection. New Jersey: Princeton University Press; 1994.
- [2]Clutton-Brock T: Sexual selection in males and females. Science 2007, 318:1882-1885.
- [3]Kempenaers B: Mate choice and genetic quality: a review of the heterozygosity theory. In Advances in the Study of Behavior, Vol 37. San Diego: Elsevier Academic Press Inc; 2007:189-278. Advances in the Study of Behavior
- [4]Neff BD, Pitcher TE: Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 2005, 14:19-38.
- [5]Mays HL, Albrecht T, Liu M, Hill GE: Female choice for genetic complementarity in birds: a review. Genetica 2008, 134:147-158.
- [6]Mays HL, Hill GE: Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 2004, 19:554-559.
- [7]Tregenza T, Wedell N: Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 2000, 9:1013-1027.
- [8]Ferretti V, Massoni V, Bulit F, Winkler DW, Lovette IJ: Heterozygosity and fitness benefits of extrapair mate choice in White-rumped Swallows (Tachycineta leucorrhoa). Behav Ecol 2011, 22:1178-1186.
- [9]Richardson DS, Komdeur J, Burke T, von Schantz T: MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc Royal Soc B-Biolog Sci 2005, 272:759-767.
- [10]Charlesworth D, Willis JH: Fundamental concepts in genetics. The genetics of inbreeding depression. Nat Rev Genet 2009, 10:783-796.
- [11]Cohen LB, Dearborn DC: Great frigatebirds, Fregata minor, choose mates that are genetically similar. Anim Behav 2004, 68:1229-1236.
- [12]Krokene C, Lifjeld JT: Variation in the frequency of extra-pair paternity in birds: a comparison of an island and a mainland population of blue tits. Behaviour 2000, 137:1317-1330.
- [13]Wang C, Lu X: Female ground tits prefer relatives as extra-pair partners: driven by kin-selection? Mol Ecol 2011, 20:2851-2863.
- [14]Shields WM: The natural and unnatural history of inbreeding and outbreeding. In The Natural and Unnatural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives. Edited by Thornhill NW. Chicago: Chicago University Press; 1993:143-169.
- [15]Waller NM: The statics and dynamics of mating system evolution. In The Natural and Unnatural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives. Edited by Thornhill NW. Chicago: Chicago University Press; 1993:97-117.
- [16]Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB: Predicting the probability of outbreeding depression. Conserv Biol 2011, 25:465-475.
- [17]Puurtinen M: Mate choice for optimal (K) inbreeding. Evolution 2011, 65:1501-1505.
- [18]Bateson P: Sexual imprinting and optimal outbreeding. Nature 1978, 273:659-660.
- [19]Bateson P: Optimal outbreeding. In Mate Choice. Edited by Bateson P. Cambridge: Cambridge University Press; 1983:257-277.
- [20]Dolgin ES, Charlesworth B, Baird SE, Cutter AD: Inbreeding and outbreeding depression in Caenorhabditis nematodes. Evolution 2007, 61:1339-1352.
- [21]Ryder TB, Tori WP, Blake JG, Loiselle BA, Parker PG: Mate choice for genetic quality: a test of the heterozygosity and compatibility hypotheses in a lek-breeding bird. Behav Ecol 2010, 21:203-210.
- [22]Sherman CDH, Wapstra E, Uller T, Olsson M: Males with high genetic similarity to females sire more offspring in sperm competition in Peron’s tree frog Litoria peronii. Proc Royal Soc B-Biolog Sci 2008, 275:971-978.
- [23]Kokko H, Ots I: When not to avoid inbreeding. Evolution 2006, 60:467-475.
- [24]Oh KP: Inclusive fitness of ‘kissing cousins’: new evidence of a role for kin selection in the evolution of extra-pair mating in birds. Mol Ecol 2011, 20:2657-2659.
- [25]Waser PM, Austad SN, Keane B: When should animals tolerate inbreeding. Am Nat 1986, 128:529-537.
- [26]Lehmann L, Perrin N: Inbreeding avoidance through kin recognition: choosy females boost male dispersal. Am Nat 2003, 162:638-652.
- [27]Parker GA: Sexual conflict over mating and fertilization: an overview. Philos Transac Royal Soc B-Biolog Sci 2006, 361:235-259.
- [28]Thunken T, Bakker TCM, Baldauf SA, Kullmann H: Active inbreeding in a cichlid fish and its adaptive significance. Curr Biol 2007, 17:225-229.
- [29]Cockburn A: Prevalence of different modes of parental care in birds. Proc Royal Soc B-Biolog Sci 2006, 273:1375-1383.
- [30]Lack D: Ecological Adaptations for Breeding in Birds. London: Methuen; 1968.
- [31]Griffith SC, Owens IPF, Thuman KA: Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 2002, 11:2195-2212.
- [32]Moller AP, Ninni P: Sperm competition and sexual selection: a meta-analysis of paternity studies of birds. Behav Ecol Sociobiol 1998, 43:345-358.
- [33]Kleven O, Jacobsen F, Robertson RJ, Lifjeld JT: Extrapair mating between relatives in the barn swallow: a role for kin selection? Biol Lett 2005, 1:389-392.
- [34]Apanius V, Penn D, Slev PR, Ruff LR, Potts WK: The nature of selection on the major histocompatibility complex. Crit Rev Immunol 1997, 17:179-224.
- [35]Penn DJ, Potts WK: The evolution of mating preferences and major histocompatibility complex genes. Am Nat 1999, 153:145-164.
- [36]Milinski M: The major histocompatibility complex, sexual selection, and mate choice. In Annual Review of Ecology Evolution and Systematics. Volume 37. Palo Alto: Annual Reviews; 2006:159-186. Annual Review of Ecology Evolution and Systematics
- [37]Piertney SB, Oliver MK: The evolutionary ecology of the major histocompatibility complex. Heredity 2006, 96:7-21.
- [38]Landry C, Garant D, Duchesne P, Bernatchez L: ‘Good genes as heterozygosity’: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc Royal Soc B-Biolog Sci 2001, 268:1279-1285.
- [39]Reusch TBH, Haberli MA, Aeschlimann PB, Milinski M: Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 2001, 414:300-302.
- [40]Penn DJ: The scent of genetic compatibility: Sexual selection and the major histocompatibility complex. Ethology 2002, 108:1-21.
- [41]Penn DJ, Damjanovich K, Potts WK: MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc Natl Acad Sci USA 2002, 99:11260-11264.
- [42]Bonneaud C, Chastel O, Federici P, Westerdahl H, Sorci G: Complex Mhc-based mate choice in a wild passerine. Proc Royal Soc B-Biolog Sci 2006, 273:1111-1116.
- [43]Griggio MGM, Biard C, Penn DJ, Hoi H: Female house sparrows “count on” male genes: experimental evidence for MHC-dependent mate preference in birds. Bmc Evol Biol 2011, 11:44. BioMed Central Full Text
- [44]Wagner WE: Measuring female mating preferences. Anim Behav 1998, 55:1029-1042.
- [45]Seutin G, White BN, Boag PT: Preservation of avian blood and tissue samples for DNA analyses. Canad J Zool-Revue Canadienne De Zoologie 1991, 69:82-90.
- [46]White GC, Burnham KP: Program MARK: survival estimation from populations of marked animals. Bird Study 1999, 46:120-139.
- [47]Choquet R, Lebreton JD, Gimenez O, Reboulet AM, Pradel R: U-CARE: Utilities for performing goodness of fit tests and manipulating CApture-REcapture data. Ecography 2009, 32:1071-1074.
- [48]Garnier S, Durand P, Arnathau C, Risterucci AM, Esparza-Salas R, Cellier-Holzem E, Sorci G: New polymorphic microsatellite loci in the house sparrow, Passer domesticus. Mol Ecol Resour 2009, 9:1063-1065.
- [49]Li SH, Huang YJ, Brown JL: Isolation of tetranucleotide microsatellites from the Mexican jay Aphelocoma ultramarina. Mol Ecol 1997, 6:499-501.
- [50]Richardson DS, Jury FL, Dawson DA, Salgueiro P, Komdeur J, Burke T: Fifty Seychelles warbler (Acrocephalus sechellensis) microsatellite loci polymorphic in Sylviidae species and their cross-species amplification in other passerine birds. Mol Ecol 2000, 9:2226-2231.
- [51]Griffith SC, Stewart IRK, Dawson DA, Owens IPF, Burke T: Contrasting levels of extra-pair paternity in mainland and island populations of the house sparrow (Passer domesticus): is there an ‘island effect’? Biol J Linn Soc 1999, 68:303-316.
- [52]Neumann K, Wetton JH: Highly polymorphic microsatellites in the house sparrow Passer domesticus. Mol Ecol 1996, 5:307-309.
- [53]Griffith SC, Dawson DA, Jensen H, Ockendon N, Greig C, Neumann K, Burke T: Fourteen polymorphic microsatellite loci characterized in the house sparrow Passer domesticus (Passeridae, Aves). Mol Ecol Notes 2007, 7:333-336.
- [54]Dawson DA, Horsburgh GJ, Kupper C, Stewart IRK, Ball AD, Durrant KL, Hansson B, Bacon I, Bird S, Klein A, Krupa AP, Lee J-W, Martin-Galvez D, Simeoni M, Smith G, Spurgin LG, Burke T: New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility - as demonstrated for birds. Mol Ecol Resour 2010, 10:475-494.
- [55]Bonneaud C, Sorci G, Morin V, Westerdahl H, Zoorob R, Wittzell H: Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus). Immunogenetics 2004, 55:855-865.
- [56]Loiseau C, Richard M, Garnier S, Chastel O, Julliard R, Zoorob R, Sorci G: Diversifying selection on MHC class I in the house sparrow (Passer domesticus). Mol Ecol 2009, 18:1331-1340.
- [57]Loiseau C, Zoorob R, Robert A, Chastel O, Julliard R, Sorci G: Plasmodium relictum infection and MHC diversity in the house sparrow (Passer domesticus). Proc Biol Sci 2011, 278:1264-1272.
- [58]Balakrishnan CN, Ekblom R, Volker M, Westerdahl H, Godinez R, Kotkiewicz H, Burt DW, Graves T, Griffin DK, Warren WC, Edwards SV: Gene duplication and fragmentation in the zebra finch major histocompatibility complex. Bmc Biology 2010, 8:29. BioMed Central Full Text
- [59]DeWoody JA, Schupp J, Kenefic L, Busch J, Murfitt L, Keim P: Universal method for producing ROX-labeled size standards suitable for automated genotyping. Biotechniques 2004, 37:348.
- [60]Amos W, Wilmer JW, Fullard K, Burg TM, Croxall JP, Bloch D, Coulson T: The influence of parental relatedness on reproductive success. Proc Roy Soc Lond B Biol Sci 2001, 268:2021-2027.
- [61]Li CC, Weeks DE, Chakravarti A: Similarity of DNA fingerprints due to chance and relatedness. Hum Hered 1993, 43:45-52.
- [62]Lynch M, Ritland K: Estimation of pairwise relatedness with molecular markers. Genetics 1999, 152:1753-1766.
- [63]Van de Casteele T, Galbusera P, Matthysen E: A comparison of microsatellite-based pairwise relatedness estimators. Mol Ecol 2001, 10:1539-1549.
- [64]Wetton JH, Carter RE, Parkin DT, Walters D: Demographic-study of a wild house sparrow population by DNA fingerprinting. Nature 1987, 327:147-149.
- [65]Kalinowski ST, Taper ML, Marshall TC: Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 2007, 16:1099-1106.
- [66]Frasier TR: STORM: software for testing hypotheses of relatedness and mating patterns. Mol Ecol Resour 2008, 8:1263-1266.
- [67]Bates D, Maechler M, Bolker B: lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42. 2011. http://CRAN.R-project.org/package=lme4 webcite
- [68]Burnham KP, Anderson DR: Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. 2nd edition. New York: Springer; 2002.
- [69]Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS: Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 2009, 24:127-135.
- [70]Barton K: MuMIn: Multi-model inference. R Package Version 1.7.2. edition 2012. http://CRAN.R-project.org/package=MuMIn webcite
- [71]Symonds MRE, Moussalli A: A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 2011, 65:13-21.
- [72]Frankham R: Do island populations have less genetic variation than mainland populations? Heredity 1997, 78:311-327.
- [73]Petrie M, Krupa A, Burke T: Peacocks lek with relatives even in the absence of social and environmental cues. Nature 1999, 401:155-157.
- [74]Stewart IRK, Hanschu RD, Burke T, Westneat DF: Tests of ecological, phenotypic, and genetic correlates of extra-pair paternity in the House Sparrow. Condor 2006, 108:399-413.
- [75]Veiga JP, Boto L: Low frequency of extra-pair fertilisations in House Sparrows breeding at high density. J Avian Biol 2000, 31:237-244.
- [76]Cordero PJ, Wetton JH, Parkin DT: Extra-pair paternity and male badge size in the House Sparrow. J Avian Biol 1999, 30:97-102.
- [77]Whitekiller RR, Westneat DF, Schwagmeyer PL, Mock DW: Badge size and extra-pair fertilizations in the House Sparrow. Condor 2000, 102:342-348.
- [78]Griffith SC: High fidelity on islands: a comparative study of extrapair paternity in passerine birds. Behav Ecol 2000, 11:265-273.
- [79]Charmantier A, Blondel J: A contrast in extra-pair paternity levels on mainland and island populations of mediterranean blue tits. Ethology 2003, 109:351-363.
- [80]Conrad KF, Johnston PV, Crossman C, Kempenaers B, Robertson RJ, Wheelwright NT, Boag T: High levels of extra-pair paternity in an isolated, low-density, island population of tree swallows (Tachycineta bicolor). Mol Ecol 2001, 10:1301-1308.
- [81]Fridolfsson AK, Gyllensten UB, Jakobsson S: Microsatellite markers for paternity testing in the willow warbler Phylloscopus trochilus: high frequency of extra-pair young in an island population. Hereditas 1997, 126:127-132.
- [82]Potts WK, Manning CJ, Wakeland EK: Matting patterns in seminatural populations of mice influenced by MHC genotype. Nature 1991, 352:619-621.
- [83]Egid K, Brown JL: The major histocompatibility complex and female mating preferences in mice. Anim Behav 1989, 38:548-550.
- [84]Olsson M, Madsen T, Nordby J, Wapstra E, Ujvari B, Wittsell H: Major histocompatibility complex and mate choice in sand lizards. Proc Roy Soc Lond B Biol Sci 2003, 270:S254-S256.
- [85]Ekblom R, Saether SA, Grahn M, Fiske P, Kalas JA, Hoglund J: Major histocompatibility complex variation and mate choice in a lekking bird, the great snipe (Gallinago media). Mol Ecol 2004, 13:3821-3828.
- [86]von Schantz T, Wittzell H, Goransson G, Grahn M: Mate choice, male condition-dependent ornamentation and MHC in the pheasant. Hereditas 1997, 127:133-140.
- [87]Freeman-Gallant CR, Meguerdichian M, Wheelwright NT, Sollecito SV: Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. Mol Ecol 2003, 12:3077-3083.
- [88]Westerdahl H: No evidence of an MHC-based female mating preference in great reed warblers. Mol Ecol 2004, 13:2465-2470.
- [89]Maitland K, Kyes S, Williams TN, Newbold CI: Genetic restriction of Plasmodium falciparum in an area of stable transmission: an example of island evolution? Parasitology 2000, 120:335-343.
- [90]Moro D, Lawson MA, Hobbs RP, Thompson RCA: Pathogens of house mice on arid Boullanger Island and subantarctic Macquarie Island, Australia. J Wildl Dis 2003, 39:762-771.
- [91]Lenaghan S, Boback S, Sundermann C, Crim A, Hester L, Hill B, Tedin K: Comparison of parasitic infections of Boa constrictor from mainland Belize and the surrounding islands. In ICOPA XI: Proceedings of the 11th International Congress of Parasitology. Bologna: Medimond S R L; 2006:471-474.
- [92]Nieberding C, Morand S, Libois R, Michaux JR: Parasites and the island syndrome: the colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). J Biogeogr 2006, 33:1212-1222.