Mate choice for genetic compatibility in the house mouse
Article first published online: 20 MAR 2013
© 2013 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Ecology and Evolution
Volume 3, Issue 5, pages 1231–1247, May 2013
Total views since publication: 394
How to Cite
Ecology and Evolution 2013; 3(5):1231–1247.
- Issue published online: 10 MAY 2013
- Article first published online: 20 MAR 2013
- Manuscript Accepted: 20 FEB 2013
- Manuscript Revised: 14 FEB 2013
- Manuscript Received: 24 AUG 2012
- University of Zurich
- Swiss National Science Foundation. Grant Number: 3100A0 – 120444
- 2003. Co-duplication of olfactory receptor and MHC class I genes in the mouse major histocompatibility complex. Hum. Mol. Genet. 12:3025–3040. , , , , , , et al.
- 2006. Sexual selection and mate choice. Trends Ecol. Evol. 21:296–302. , and .
- 1997. The nature of selection on the major histocompatibility complex [Review]. Crit. Rev. Immunol. 17:179–224. , , , , and .
- 1996. Recent evolution of mouse t haplotypes at polymorphic microsatellites associated with the t complex responder (Tcr) locus. Genet. Res. 67:1–10. , and .
- 1984. Gene mapping within the T/t complex of the mouse III: t-lethal genes are arranged in three clusters on chromosome 17. Cell 39:565–572. .
- 2008. Mendelian inheritance of t haplotypes in house mouse (Mus musculus domesticus) field populations. Genet. Res. 90:331–339.
- 1960. Selective fertilization at the T-locus of the mouse. Genet. Res. 1:226–238.
- 2011. lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-39. Available at http://CRAN.R-project.org/package=lme4 (accessed December 3, 2011). , , and .
- 2005. The t-complex-encoded GTPase-activating protein Tagap1 acts as a transmission ratio distorter in mice. Nat. Genet. 37:969–973. , , , and .
- 2007. The t-complex-encoded guanine nucleotide exchange factor Fgd2 reveals that two opposing signaling pathways promote transmission ratio distortion in the mouse. Genes Dev. 21:143–147. , , , and .
- 2007. The dynamic of the t-haplotype in wild populations of the house mouse Mus musculus domesticus in Israel. Mamm. Genome 18:164–172. , , , , and .
- 2008. Genus Mus. Pp. 141–149 in S. Harris and D. W. Yalden, eds. Mammals of the British Isles Handbook. 4th ed. The Mammal Society, Southampton, U.K. , , and .
- 2002. Postcopulatory sexual selection. Nat. Rev. Genet. 3:262–273. , and .
- 2006. MHC peptides and the sensory evaluation of genotype. Trends Neurosci. 29:100–107. , and .
- 1993. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33–39. , , , , , , et al.
- 2008. Group atmotMGD. The Mouse Genome Database (MGD): mouse biology and model systems. Nucleic Acids Res. 36:D724–D728. , , , , and .
- 2002. Discrimination of MHC-derived odors by untrained mice is consistent with divergence in peptide-binding region residues. Proc. Natl. Acad. Sci. USA 99:2187–2192. , , and .
- 2004. Fitness effects of a selfish gene (the Mus t complex) are revealed in an ecological context. Evolution 58:1318–1328. , , , , and .
- 1994. The evolution of lethals in the t-haplotype system of the mouse. Proc. Biol. Sci. 258:101–107.
- 2007. The genetic basis of individual-recognition signals in the mouse. Curr. Biol. 17:1771–1777. , , , , , and .
- 1983. Characterization of an antigen present on testicular cells and pre-implantation embryos whose expression is modified by the t12 haplotype. Int. J. Immunogenet. 10:465–485. , , , , and .
- 1936. The inheritance of taillessness (anury) in the house mouse. Genetics 21:525–536. , and .
- 1992. Female preferences based on male quality in house mice – interaction between male-dominance rank and T-Complex genotype. Ethology 90:1–16. , and .
- 1976. The selfish gene. Oxford Univ. Press, Oxford, U.K.
- 2006. The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol. Ecol. 15:4141–4151. , , and .
- 1987. T-locus effects on the male urinary chemosignal that accelerates puberty in female mice. Anim. Behav. 35:1581–1583. , and .
- 1937. A third lethal in the T (Brachy) series in the house mouse. Proc. Natl. Acad. Sci. USA 23:474–477.
- 1957. Evidence of evolutionary forces leading to the spread of lethal genes in wild populations house mice. Proc. Natl. Acad. Sci. USA 43:158–163.
- 1971. Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol. Reprod. 4:195–215. , and .
- 2009. Effects of brood size on multiple-paternity rates: a case for ‘paternity share’ as an offspring-based estimate. Anim. Behav. 78:563–571. , and .
- 1985. Responses of male mice to odors of females: effects of T- and H-2-locus genotype. Behav. Genet. 15:287–295. , and .
- 1970. Probable haploid expression of HL-A antigens on human spermatozoon. Nature 225:191–193. , and .
- 1985. Evolution of mouse major histocompatibility complex genes borne by t chromosomes. Proc. Natl. Acad. Sci. USA 82:2819–2823. , , , and .
- 2008a. The frequency of multiple paternity predicts variation in testes size among island populations of house mice. J. Evol. Biol. 21:1524–1533. , and .
- 2008b. Polyandry facilitates postcopulatory inbreeding avoidance in house mice. Evolution 62:603–611. , and .
- 1997. Applied regression analysis, linear models and related methods. Sage, Thousand Oaks, CA.
- 2004. Functional characterization of a mouse testicular olfactory receptor and its role in chemosensing and in regulation of sperm motility. J. Cell Sci. 117:5835–5845. , , , and .
- 1979. Assay for antibody mediated cytotoxicity of mouse spermatozoa by Rb-86 release. Tissue Antigens 13:177–185. , , , and .
- 1979. Analysis of anti-sperm sera for T/t locus-specific antibody. J. Reprod. Immunol. 1:11–21. , , , and .
- 1995. Multiple mating, sperm competition and meiotic drive. J. Evol. Biol. 8:265–282. , and .
- 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. 41:95–98.
- 1989. Evolution of mouse chromosome 17 and the origin of inversions associated with t haplotypes. Proc. Natl. Acad. Sci. USA 86:3261–3265. , , and .
- 1999. A protein kinase encoded by the t complex responder gene causes non-mendelian inheritance. Nature 402:141–146. , , , , and .
- 1994. Sharing of human-leukocyte antigens in couples with unexplained infertility affects the success of in-vitro fertilization and tubal embryo-transfer. Am. J. Obstet. Gynecol. 170:63–71. , , , , , , et al.
- 2001. Frequency and distribution of t-haplotypes in the Southeast Asian house mouse (Mus musculus castaneus) in Taiwan. Mol. Ecol. 10:2349–2354. , , and .
- 2007. Major histocompatibility complex heterozygosity reduces fitness in experimentally infected mice. Genetics 176:2501–2508. , , , , , and .
- 1991. The t complex of the mouse: chemical characterization by urinary volatile profiles. J. Chem. Ecol. 17:353–367. , , , , and .
- 1995. Sperm from mice carrying one or two t haplotypes are deficient in investment and oocyte penetration. Dev. Biol. 168:138–149. , , , and .
- 1998. New perspectives on mate choice and the MHC. Heredity 81:127–133.Direct Link:, and .
- 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16:1099–1106. , , and .
- 2005. Genes, odours and the recognition of parasitized individuals by rodents. Trends Ecol. Evol. 21:423–429. , , and .
- 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17:230–241. , and .
- 1984. Polymorphism of t-complex genes in European wild mice. Genet. Res. 44:39–46. , , .
- 2012. The complex social environment of female house mice (Mus domesticus). Pp. 114–134 in M. Malochán, S. J. E. Baird, P. Munclinger, and J. Piálek, eds. Evolution of the house mouse. Cambridge Univ. Press, Cambridge, U.K. , and .
- 1990. Sex-specific embryonic mortality during concurrent pregnancy and lactation in house mice. J. Exp. Zool. 256:106–112.
- 1992. Sex ratio manipulation in wild house mice: the effect of fetal resorption in relation to the mode of reproduction. Biol. Reprod. 47:541–548.
- 2009. Major histocompatibility complex-regulated odortypes: peptide-free urinary volatile signals. Physiol. Behav. 96:184–188. , , , , , and .
- 2010. In search of the chemical basis for MHC odourtypes. Proc. Biol. Sci. 277:2417–2425. , , , , and .
- 2004. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306:1033–1037. , , , , , , et al.
- 1991. The t complex: a story of genes, behavior, and populations. Adv. Study Behav. 20:51–86.
- 1992. Genetic basis of mating preferences in wild house mice. Am. Zool. 32:40–47. , and .
- 1985. Female discrimination of male odors correlated with male genotype at the T locus: a response to T-locus or H-2-locus variability? Behav. Genet. 15:53–67. , and .
- 1988. Analysis of a genetic recognition system in wild house mice. Behav. Genet. 18:549–564. , , and .
- 1994. Female preference and variability among t-haplotypes in wild house mice. Am. Nat. 143:766–784. , , and .
- 2003. Transmission ratio distortion in mice. Annu. Rev. Genet. 37:393–408.
- 2011. Polyandry and the decrease of a selfish genetic element in a wild house mouse population. Evolution 65:2435–2447. , , , and .
- 1999. Cyclic expression of HLA class I and II molecules on the surface of purified human spermatozoa and their control by serum inhibin B levels. Biol. Reprod. 61:1381–1386. , , and .
- 2004. Choosing mates: good genes versus genes that are a good fit. Trends Ecol. Evol. 19:554–559. , and .
- 1997. A microsatellite-based MHC genotyping system for house mice (Mus domesticus). Hereditas. 127:75–82. , and .
- 2000. Male-male competition magnifies inbreeding depression in wild house mice. Proc. Natl. Acad. Sci. USA 97:3324–3329. , , and .
- 2006. The major histocompatibility complex, sexual selection, and mate choice. Annu. Rev. Ecol. Evol. Syst. 37:159–186.
- 2001. The Y chromosomes of Drosophila simulans are highly polymorphic for their ability to suppress sex-ratio drive. Evolution 55:728–737. , , and .
- 1989. An efficient salt-chloroform extraction of DNA from blood and tissues. Trends Genet. 5:391. , , .
- 2005. Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol. Ecol. 14:19–38. , and .
- 1974. An effect of the female genotype on sperm transport in mice. J. Reprod. Fertil. 39:421–424. , and .
- 1992. Decreased fecundability in Hutterite couples sharing HLA-DR. Am. J. Hum. Genet. 50:6–14. , , , and .
- 1978. Rate of egg penetration in vitro accelerated by T/t locus in the mouse. J. Exp. Zool. 206:323–331. , and .
- 2009. Major histocompatibility complex (MHC) heterozygote superiority to natural multi-parasite infections in the water vole (Arvicola terrestris). Proc. Biol. Sci. 276:1119–1128. , , and .
- 1998. Sperm competition and the evolution of ejaculates: towards a theory base. Pp. 3–53 in T. R. Birkhead and A. P. Møller, eds. Sperm competition and sexual selection. Academic Press, San Diego, CA.
- 2002. The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21.
- 2012. The evolution of MHC diversity in house mice. Pp. 221–252 in M. Macholán, S. J. E. Baird, P. Munclinger, and J. Piálek, eds. Evolution of the house mouse. Cambridge Univ. Press, Cambridge, U.K. , and .
- 2002. MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc. Natl. Acad. Sci. USA 99:11260–11264. , , and .
- 1967. Studies of natural populations of Mus. II. Polymorphism at the T locus. Evolution 21:466–478.
- 2001. Dominant rams lose out by sperm depletion – a waning success in siring counters a ram's high score in competition for ewes. Nature 409:681–682. , , , and .
- 2008. Selfish genetic elements and sexual selection: their impact on male fertility. Genetica 134:99–111. , and .
- 2010. Polyandry prevents extinction. Curr. Biol. 20:1–5. , , and .
- 2012. No evidence of mate discrimination against males carrying a sex ratio distorter in Drosophila pseudoobscura. Behav. Ecol. Sociobiol. 66:561–568. , , , , and .
- 2005. Genetic compatibility and sexual selection. Trends Ecol. Evol. 20:157–158. , , and .
- 2009. The good-genes and compatible-genes benefits of mate choice. Am. Nat. 174:741–752. , , and .
- R Development Core Team. 2011. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
- 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86:248–249. , and .
- 2003. Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J. Mol. Biol. 331:623–641. , and .
- 2000. Genes in the first and fourth inversions of the mouse t complex synergistically mediate sperm capacitation and interactions with the oocyte. Dev. Biol. 226:267–280. , , , , and .
- 2009. Complexity and context of MHC-correlated mating preferences in wild populations. Mol. Ecol. 18:3121–3123.
- 2006. Correlations between heterozygosity and measures of genetic similarity: implications for understanding mate choice. J. Evol. Biol. 19:558–569. , , and .
- 2003. Free female choice in house mice: leaving best for last. Behaviour 140:1371–1388. , , and .
- 2008. genepop ‘007: a complete reimplementation of the Genepop software for Windows and Linus. Mol. Ecol. Resour. 8:103–106.
- 1998. MHC-genotype of progeny influenced by parental infection. Proc. Biol. Sci. 265:711–716. , , , , and .
- 2004. MHC variability of a small lemur in the littoral forest fragments of southeastern Madagascar. Conserv. Genet. 5:299–309. , , and .
- 1990. Rapid identification of mouse t haplotypes by PCR polymorphism (PCRP). Mouse Genome 87:108. , and .
- 2007. The genetic basis of inbreeding avoidance in house mice. Curr. Biol. 17:2061–2066. , , , , , , et al.
- 1993. The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends Genet. 9:250–254.
- 1987. The selection-arena hypothesis. Pp. 337–349 in S. C. Stearns, ed. The evolution of sex and its consequences. Birkhäuser Verlag, Basel.
- 1997. No evidence of sperm selection by female common shrews. Proc. Biol. Sci. 264:1497–1500. .
- 2008. Identification of selective sweeps in closely related populations of the house mouse based on microsatellite scans. Genetics 180:1537–1545. , , , and .
- 1981. Male genotype influences sperm transport in female mice. Biol. Reprod. 24:806–813. , and .
- 1989. The house mouse atlas of embryonic development. Springer-Verlag, New York.
- 2011. Major histocompatibility complex heterozygosity enhances reproductive success. Mol. Ecol. 20:1546–1557. , , , and .
- 2000. Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9:1013–1027. , and .
- 2002. Modern applied statistics with S. Springer, New York. , and .
- 2009. Retention of gene products in syncytial spermatids promotes non-Mendelian inheritance as revealed by the t complex responder. Genes Dev. 23:2705–2710. , , , , , and .
- 1982. The regulation of infanticide and parental behaviour: implications for reproductive success in male mice. Science 215:1270–1272. , and .
- 1996. Non-random fertilization in mice correlates with the MHC and something else. Heredity 77:400–409. , , , and .
- 2013. The dynamic relationship between polyandry and selfish genetic elements. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368:20120049. .
- 1993. Factors modulating preferences of female house mice for males differing in t-complex genotype: role of t-complex genotype, genetic background, and estrous condition of females. Behav. Genet. 23:51–58. , and .
- 2006. Individual odortypes: interaction of MHC and background genes. Immunogenetics 58:967–982. , , , , , and .
- 2007. Genetic basis for MHC-dependent mate choice. Adv. Genet. 59:129–145. , and .
- 1979. Recognition among mice: evidence from the use of a Y-maze differentially scented by congenic mice of different major histocompatibility types. J. Exp. Med. 150:755–760. , , , , , and .
- 1990. Single MHC gene mutations alter urine odour constitution in mice. Pp. 255–259 in D. W. Macdonald, D. Müller-Schwarze, and S. E. N, eds. Chemical signals in vertebrates. Oxford Univ. Press, Oxford, U.K. , , , and .
- 1974. Serological identification of sperm antigens specified by lethal t-alleles in the mouse. Immunogenetics 1:57–67. , , , , and .
- 1997. The evolution of polyandry II: post-copulatory defences against genetic compatibility. Proc. Biol. Sci. 264:69–75. , and .
- 2002. Possible roles for products of polymorphic MHC and linked olfactory receptor genes during selection processes in reproduction. Am. J. Reprod. Immunol. 48:34–42. , , and .
- 2005. Female choice and the MHC. Trends Immunol. 26:496–502. , , and .
- 2010. Self/Nonself perception, reproduction and the extended MHC. Landes Biosci. 1:176–191. , , , and .