Condition-dependent mate choice and a reproductive disadvantage for MHC-divergent male tiger salamanders

Molecular Ecology

Volumn 18, Issue 15, 2009, Pages 3307-3315

  Bos, David H ^a   Williams, Rod N ^a   Gopurenko, David ^a   Bulut, Zafer ^a   Dewoody, J Andrew ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Ambystoma tigrinum; Heterosis; Mate choice; Reproductive success; Sexual selection; Sperm storage

Indexed keywords

MICROSATELLITE DNA;

AMBYSTOMA; ANIMAL; ARTICLE; DNA SEQUENCE; FEMALE; GENETIC VARIABILITY; GENETICS; GENOTYPE; HISTOLOGY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MATE CHOICE; REPRODUCTION;

AMBYSTOMA; ANIMALS; FEMALE; GENETIC VARIATION; GENOTYPE; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MATING PREFERENCE, ANIMAL; MICROSATELLITE REPEATS; REPRODUCTION; SEQUENCE ANALYSIS, DNA;

AMBYSTOMA; AMBYSTOMA TIGRINUM; ANIMALIA; SALAMANDROIDEA;

EID: 68149142294     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04242.x     Document Type: Article

References (55)

1. Arnold SJ (1976) Sexual behavior, sexual interference, and sexual defense in the salamanders Ambystoma maculatum, Ambystoma tigrinum and Plethodon jordani. Zeitschrift für Tierpsychologie, 42, 247 300.
2. Boehm T, Zufall F (2006) MHC peptides and the sensory evaluation of genotype. Trends in Neurosciences, 29, 100 107.
3. Bonneaud C, Chastel O, Federici P, Westerdahl H, Sorci G (2006) Complex Mhc-based mate choice in a wild passerine. Proceedings of the Royal Society B: Biological Sciences, 273, 1111 1116.
4. Bos DH, DeWoody JA (2005) Molecular characterization of major histocompatibility complex class II alleles in wild tiger salamanders (Ambystoma tigrinum). Immunogenetics, 57, 775 781.
5. Bos DH, Turner SM, DeWoody JA (2007) Haplotype inference from diploid sequence data: evaluating performance using non-neutral MHC sequences. Hereditas, 144, 228 234.
6. Bos DH, Gopurenko D, Williams RN, DeWoody JA (2008) Inferring population history and demography using microsatellites, mitochondrial DNA, and major histocompatibility complex (MHC) genes. Evolution, 62, 1458 1468.
7. Bulut Z, McCormick CR, Gopurenko D, Williams RN, Bos DH, DeWoody JA (2009) Microsatellite mutation rates in the eastern tiger salamander (Ambystoma tigrinum tigrinum) differ 10-fold across loci. Genetica, 136, 501 504.
8. Candolin U (2003) The use of multiple cues in mate choice. Biological Reviews, 78, 575 595.
9. Chandler CH, Zamudio KR (2008) Reproductive success by large, closely related males facilitated by sperm storage in an aggregate breeding amphibian. Molecular Ecology, 17, 1564 1576.
10. Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Current Biology, 16, R755 R765.
11. Donnelly MA, Guyer C, Juterbock JE, Alford RA (1994) Techniques for marking amphibians. In : Measuring and Monitoring Biological Diversity. Standard Methods for Amphibians (eds Heyer WR, Donnelly MA, McDiarmid RW, Hayek L-AC, Foster MS pp. 277 284. Smithsonian Institution Press, Washington D. C.
12. Ekblom R, Saether SA, Grahn M et al 2004) Major histocompatibility complex variation and mate choice in a lekking bird, the great snipe (Gallinago media). Molecular Ecology, 13, 3821 3828.
13. Forsburg LA, Dannetoitz J, Petersson E, Grahn M (2007) Influence of genetic dissimilarity in the reproductive success and mate choice of brown trout-females fishing for optimal MHC dissimilarity. Journal of Evolutionary Biology, 20, 1859 1869.
14. Gopurenko D, Williams RN, McCormick CR, DeWoody JA (2006) Insights into the mating habits of the tiger salamander (Ambystoma tigrinum tigrinum) as revealed by genetic parentage analyses. Molecular Ecology, 15, 1917 1928.
15. Grantham R (1974) Amino acid difference formula to help explain protein evolution. Science, 185, 862 864.
16. Hedrick PW, Black FL (1997) HLA and mate selection: no evidence in South Amerindians. American Journal of Human Genetics, 61, 505 511.
17. Hood GM (2006) Poptools. Commonwealth Scientific and Research Organization, Canberra, Australia.
18. Howard RD, Moorman RS, Whiteman HH (1997) Differential effects of mate competition and mate choice on eastern tiger salamanders. Animal Behavior, 53, 1345 1356.
19. Ilmonen P, Penn DJ, Damjanovich K et al 2007) Major histocompatibility complex heterozygosity reduces fitness in experimentally infected mice. Genetics, 176, 2501 2508.
20. Jacob S, McClintock MK, Zelano B, Ober C (2002) Paternally inherited HLA alleles are associated with women's choice of male odor. Nature Genetics, 30, 175 179.
21. Jones AG (2005) Gerud 2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parents. Molecular Ecology Notes, 5, 708 711.
22. Kauer JS (2002) On the scents of smell in the salamander. Nature, 417, 336 342.
23. Kaufman J (1999) Co-evolving genes in MHC haplotypes: the 'rule' for nonmammalian vertebrates? Immunogenetics, 50, 228 236.
24. Kaufman J, Volk H, Wallny H-J (1995) A 'minimal essential Mhc' and an 'unrecognized Mhc': two extremes in selection for polymorphism. Immunological Reviews, 143, 63 88.
25. Kumpf KM (1934) The courtship of Ambystoma tigrinum. Copeia, 1, 7 10.
26. Landry C, Garant D, Duchesne P, Bernatchez L (2001) 'Good genes as heterozygosity': the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proceedings of the Royal Society B: Biological Sciences, 268, 1279 1285.
27. Leinders-Zufall T, Brennan P, Widmayer P et al 2004) MHC class I peptides as chemosensory signals in the vomeronasal organ. Science, 306, 1033 1037.
28. McClelland EE, Penn DJ, Potts WK (2003) Major histocompatibility complex heterozygote superiority during coinfection. Infection and Immunity, 71, 2079 2086.
29. Neff BD (2004) Stabilizing selection on genomic divergence in a wild fish population. Proceedings of the National Academy of Science, 101, 2381 2385.
30. Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: and integrated framework for good genes and compatible genes. Molecular Ecology, 14, 19 38.
31. Olsson M, Madsen T, Nordby J et al 2003) Major histocompatibility complex and mate choice in sand lizards. Proceedings of the Royal Society B: Biological Sciences, 270 (Supplement S254 S256.
32. Park D, McGuire JM, Majchrzak AL, Ziobro JM, Eisthen HL (2004) Discrimination of conspecific sex and reproductive condition using chemical cues in axolotls (Ambystoma mexicanum). Journal of Comparative Physiology A - Neuroethology Sensory Neural and Behavioral Physiology, 190, 415 427.
33. Peakall R, Smouse PE (2006) GenAlEx6: genetic analysis in Excel. Population genetics software for teaching and research. Molecular Ecology Notes, 6, 288 295.
34. Penn DJ, Potts WK (1998a) MHC-dissortative mating preferences reversed by cross-fostering. Proceedings of the Royal Society B: Biological Sciences, 265, 1299 1306.
35. Penn DJ, Potts WK (1998b) Untrained mice discriminate MHC-determined odors. Physiology and Behavior, 63, 235 243.
36. Penn DJ, Damjanovich K, Potts WK (2002) MHC heterozygosity confers a selective advantage against multiple-strain infections. Proceedings of the National Academy of Sciences, USA, 99, 11260 11264.
37. Potts WK, Manning CJ, Wakeland EK (1991) Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature, 352, 619 621.
38. Potts WK, Manning CJ, Wakeland EK (1994) The role of infectious disease, inbreeding and mating preferences in maintaining MHC diversity: an experimental test. Philosophical Transactions of the Royal Society B: Biological Sciences, 346, 369 378.
39. Puurtinen M, Ketola T, Katiaho JS (2005) Genetic compatibility and sexual selection. Trends in Ecology & Evolution, 20, 157 158.
40. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution, 43, 258 275.
41. Richardson DS, Komdeur J, Burke T, von Schantz T (2005) MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proceedings of the Royal Society Series B - Biological Sciences, 272, 759 767.
42. Roberts SC, Gosling LM (2003) Genetic similarity and quality interact in mate choice decisions by female mice. Nature Genetics, 35, 103 106.
43. Rollmann SM, Houck LD, Feldhoff RC (1999) Proteinaceous pheromone affecting female receptivity in a terrestrial salamander. Science, 285, 1907 1909.
44. Rose FL, Armentrout D (1976) Adaptive strategies of Ambystoma tigrinum Green inhabiting the Llano Estacado of west Texas. Journal of Animal Ecology, 45, 713 729.
45. Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Press, Cold Spring Harbor, New York.
46. Sever DM (1995) Spermathecae of Ambystoma tigrinum (Amphibia: Caudata): development and a role for the secretions. Journal of Herpetology, 29, 243 255.
47. Sherborne AL, Thom MD, Paterson S et al 2007) The genetic basis of inbreeding avoidance in house mice. Current Biology, 17, 2061 2066.
48. Sherman CDH, Wapstra E, Uller T, Olsson M (2009) Males with high genetic similarity to females sire more offspring in sperm competition in Peron's tree frog Litoria peronii. Proceedings of the Royal Society Series B - Biological Sciences, 275, 917 978.
49. Sommer S (2005) Major histocompatibility complex and mate choice in a monogamous rodent. Behavioral Ecology and Sociobiology, 58, 181 189.
50. Tennessen JA, Zamudio KR (2003) Early male reproductive advantage, multiple paternity and sperm storage in an amphibian aggregate breeder. Molecular Ecology, 12, 1567 1576.
51. Williams RN, DeWoody JA (2009) Reproductive success and sexual selection in wild tiger salamanders (Ambystoma tigrinum). Evolutionary Biology, 36, 201 213.
52. Williams RN, Gopurenko D, Kemp KR, Williams BC, DeWoody JA (2009) Breeding chronology, sexual dimorphism, and genetic diversity of congeneric Ambystomatid Salamanders under different sexual selection regimes. Journal of Herpetology, in press.
53. Yamazaki K, Boyse EA, Miké V et al 1976) Control of mating preferences in mice by genes in the major histocompatibility complex. Journal of Experimental Medicine, 144, 1324 1335.
54. 2 segregants of crosses between MHC-congenic mouse strains. Immunogenetics, 6, 253 259.
55. Zinkernagel RM, Doherty P (1974) Restriction of in vitro T-cell mediated cytotoxicity in lymphocytic chorio-meningitis within a syngenic or semiallogeneic system. Nature, 248, 701 702.