Linkage mapping reveals sex-dimorphic map distances in a passerine bird

Proceedings of the Royal Society B: Biological Sciences

Volumn 272, Issue 1578, 2005, Pages 2289-2298

  Hansson, Bengt ^a   Åkesson, Mikael ^b   Slate, Jon ^c   Pemberton, Josephine M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b LUND UNIVERSITY   (Sweden)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Bird; Genetic map; Heterochiasmy; Linkage; Microsatellite; Recombination

Indexed keywords

BIOLOGICAL MARKER;

EVOLUTIONARY THEORY; GENETIC ANALYSIS; PASSERINE; SEXUAL DIMORPHISM;

ARTICLE; BIRD; COMPARATIVE STUDY; FEMALE; GENETIC LINKAGE; GENETIC RECOMBINATION; GENOTYPE; HUMAN; LINKAGE ANALYSIS; MALE; MEDICAL RESEARCH; MICROSATELLITE INSTABILITY; NONHUMAN; PEDIGREE; PRIORITY JOURNAL; SEX CHROMOSOME; SEX DIFFERENCE;

ACROCEPHALUS ARUNDINACEUS; AVES; PASSERIFORMES;

EID: 27244455629     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2005.3228     Document Type: Article

References (84)

1. Archibald, A. L. et al. 1995 The pigmap consortium linkage map of the pig (Sus scrofa). Mamm. Genome 6, 157-175. (doi:10.1007/BF00293008.)
2. Arlt, D., Hansson, B., Bensch, S., von Schantz, T. & Hasselquist, D. 2004 Breeding synchrony does not affect extra-pair paternity in great reed warblers. Behaviour 141, 863-880. (doi:10.1163/1568539042265699.)
3. Badyaev, A. V., Hill, G. E., Beck, M. L., Dervan, A. A., Duckworth, R. A., McGraw, K. J., Nolan, P. M. & Whittingham, L. A. 2002 Sex-biased hatching order and adaptive population divergence in a passerine bird. Science 295, 316-318. (doi:10.1126/science.1066651.)
4. Baverstock, P. R., Adams, M., Polkinghorne, R. W. & Gelder, M. 1982 A sex-linked enzyme in birds-Z-chromosome conservation but no dosage compensation. Nature 296, 763-766. (doi:10.1038/296763a0.)
5. Bensch, S. 1996 Female mating status and reproductive success in the great reed warbler: is there a potential cost of polygyny that requires compensation? J. Anim. Ecol. 65, 283-296.
6. Bensch, S., Hasselquist, D. & von Schantz, T. 1994 Genetic similarity between parents predicts hatching failure: nonincestuous inbreeding in the great reed warbler. Evolution 48, 317-326.
7. Bernstein, H., Hopf, F. & Michod, R. 1988 Is meiotic recombination and adaptation for repairing DNA, producing genetic variability, or both? In The evolution of sex (ed. R. Michod & B. Levin), pp. 139-160. Sunderland, MA: Sinauer.
8. Broman, K. W., Murray, J. C., Sheffield, V. C., White, R. L. & Weber, J. L. 1998 Comprehensive human genetic maps: Individual and sex-specific variation in recombination. Am. J. Hum. Genet. 63, 861-869. (doi:10.1086/302011. )
9. Burns, J. L., Jackson, D. A. & Hassan, A. B. 2001 A view through the clouds of imprinting. FASEB J. 15, 1694-1703. (doi:10.1096/fj.010085rev.)
10. Burt, D. W., Morrice, D. R., Sewalem, A., Smith, J., Paton, I. R., Smith, E. J., Bentley, J. & Hocking, P. M. 2003 Preliminary linkage map of the Turkey (Meleagris gallopavo) based on microsatellite markers. Anim. Genet. 34, 399-409. (doi:10.1046/j.1365-2052.2003.01033.x.)
11. Catchpole, C. K., Leisler, B. & Winkler, H. 1985 Polygyny in the great reed warbler, Acrocephalus arundinaceus: a possible case of deception. Behav. Ecol. Sociobiol. 16, 285-291. (doi:10.1007/BF00310992.)
12. Christians, E., Boiani, M., Garagna, S., Dessy, C., Redi, C. A., Renard, J. P. & Zuccotti, M. 1999 Gene expression and chromatin organization during mouse oocyte growth. Dev. Biol. 207, 76-85. (doi:10.1006/dbio.1998.9157.)
13. Dawson, D. A., Burke, T., Hansson, B., Pandhal, J., Hale, M. C., Hinten, G. H. & Slate, J. 2006 A predicted microsatellite map of the passerine genome based on chicken-passerine sequence similarity. Mol. Ecol. (In press.)
14. Degnan, S. M., Robertson, B. C., Clegg, S. B. & Moritz, C. C. 1999 Microsatellite primers for studies of gene flow and mating systems in white-eyes (Zosterops). Mol. Ecol. 8, 159-160. (doi:10.1046/j.1365-294X.1999.00799.x.)
15. Derjusheva, S., Kurganova, A., Habermann, F. & Gaginskaya, E. 2004 High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosome Res. 12, 715-723. (doi:10.1023/B:CHRO.0000045779.50641.00.)
16. Dietrich, W. F. et al. 1996 A comprehensive genetic map of the mouse genome. Nature 380, 149-152. (doi:10.1038/380149a0.)
17. Double, M. C., Dawson, D., Burke, T. & Cockburn, A. 1997 Finding the fathers in the least faithful bird: a microsatellite-based genotyping system for the superb fairywren Malurus cyaneus. Mol. Ecol. 6, 691-693. (doi:10. 1046/j.1365-294X.1997.00228.x.)
18. Ellegren, H. 2005 The avian genome uncovered. Trends Ecol. Evol. 20, 180-186. (doi:10.1016/j.tree.2005.01.015.)
19. Flint, J. & Mott, R. 2001 Finding the molecular basis of quantitative traits: successes and pitfalls. Nat. Rev. Genet. 2, 437-445. (doi:10.1038/35076585.)
20. Frentiu, F. D., Lange, C. L., Burke, T. & Owens, I. P. F. 2003 Isolation of microsatellite loci in the Capricorn silvereye, Zosterops lateralis chlorocephalus (Aves: Zosteropidae). Mol. Ecol Notes 3, 462-464. (doi:10.1046/j.1471-8286.2003. 00484.x.)
21. Gibbs, H. L., Tabak, L. M. & Hobson, K. 1999 Characterization of microsatellite DNA loci for a neotropical migrant songbird, the Swainson's thrush (Catharus ustulatus). Mol. Ecol. 8, 1551-1552. (doi:10.1046/j.1365-294x. 1999.00673.x.)
22. Griffith, S. C., Stewart, I. R. K., Dawson, D. A., Owens, I. P. F. & Burke, T. 1999 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. 68, 303-316. (doi:10.1006/bijl.1999.0343.)
23. Groenen, M. A. M. et al. 2000 A consensus linkage map of the chicken genome. Genome Res. 10, 137-147.
24. Gustafsson, L. & Sutherland, W. J. 1988 The cost of reproduction in the collared flycatcher Ficedula albicollis. Nature 335, 813-815. (doi:10.1038/335813a0.)
25. Haldane, J. B. S. 1922 Sex ratio and unisexual sterility in hybrid animals. J. Genet. 12, 101-109.
26. Hanotte, O., Zanon, C., Greig, C., Dixon, A. & Burke, T. 1994 Isolation and characterization of microsatellite loci in a passerine bird: the reed bunting Emberiza schoeniclus. Mol. Ecol. 3, 529-530.
27. Hansson, B. & Kawabe, A. 2005 A simple method to score single nucleotide polymorphisms based on allele-specific PCR and primer-induced fragment-length variation. Mol. Ecol. Notes 5, 692-696. (doi:10.1111/j.1471- 8286.2005. 01033.x.)
28. Hansson, B., Bensch, S. & Hasselquist, D. 2000a Patterns of nest predation contribute to polygyny in the great reed warbler. Ecology 81, 319-328.
29. Hansson, B., Bensch, S., Hasselquist, D., Lillandt, B.-G., Wennerberg, L. & von Schantz, T. 2000b Increase of genetic variation over time in a recently founded population of great reed warblers (Acrocephalus arundinaceus) revealed by microsatellites and DNA fingerprinting. Mol. Ecol. 9, 1529-1538. (doi:10.1046/j.1365-294x.2000.01028.x.)
30. Hansson, B., Bensch, S., Hasselquist, D. & Nielsen, B. 2002 Restricted dispersal in a long-distance migrant bird with patchy distribution, the great reed warbler. Oecologia 130, 536-542. (doi:10.1007/s00442-001-0831-2.)
31. Hansson, B., Gavrilov, E. & Gavrilov, A. 2003 Hybridisation between great reed warblers Acrocephalus arundinaceus and clamorous reed warblers A. stentoreus: morphological and molecular evidence. Avian Sci. 3, 145-151.
32. Hansson, B., Bensch, S. & Hasselquist, D. 2004a Do female great reed warblers seek extra-pair fertilizations to avoid inbreeding? Proc. R. Soc. B 271(Suppl. 5), S290-S292. (doi:10.1098/rsbl.2004.0164.)
33. Hansson, B., Bensch, S. & Hasselquist, D. 2004b Lifetime fitness of short- and long-distance dispersing great reed warblers. Evolution 58, 2546-2557.
34. Hansson, B., Westerdahl, H., Bensch, S., Hasselquist, D. & Akesson, M. 2004c Does linkage disequilibrium generate heterozygosity-fitness correlations in great reed warblers? Evolution 58, 870-879.
35. Hasselquist, D. 1998 Polygyny in the great reed warbler: a long-term study of factors contributing to male fitness. Ecology 79, 2376-2390.
36. Hasselquist, D., Bensch, S. & von Schantz, T. 1996 Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381, 229-232. (doi:10.1038/381229a0.)
37. Helbig, A. J. & Seibold, I. 1999 Molecular phylogeny of the Palearctic-African Acrocephalus and Hippolais warblers (Aves: Sylviidae). Mol. Phylogenet. Evol. 11, 246-260. (doi:10.1006/mpev.1998.0571.)
38. Hulten, M. 1974 Chiasma distribution at diakinesis in normal human male. Hereditas 76, 55-78.
39. Hurst, L. D., Pal, C. & Lercher, M. J. 2004 The evolutionary dynamics of eukaryotic gene order. Nat. Rev. Genet. 5, 299-310. (doi:10.1038/nrg1319.)
40. Huxley, J. S. 1928 Sexual differences of linkage in Gammarus chevreuxi. J. Genet. 20, 145-156.
41. International Chicken Genome Sequencing Consortium 2004 Sequencing and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432, 695-716. (doi:10.1038/nature03154.)
42. Irwin, D. E., Bensch, S. & Price, T. D. 2001 Speciation in a ring. Nature 409, 333-337. (doi:10.1038/35053059.)
43. Ishibashi, Y., Mikami, O. & Abe, S. 2000 Isolation and characterization of microsatellite loci in the Japanese marsh warbler Locustella pryeri. Mol. Ecol. 9, 373-375. (doi:10.1046/j.1365-294x.2000.00874-5.x.)
44. Kayang, B. B., Vignal, A., Inoue-Murayama, M., Miwa, M., Monvoisin, J. L., Ito, S. & Minvielle, F. 2004 A first-generation microsatellite linkage map of the Japanese quail. Anim. Genet. 35, 195-200. (doi:10.1111/j.1365-2052. 2004.01135.x.)
45. Keller, L. F., Arcese, P., Smith, J. N. M., Hochachka, W. M. & Stearns, S. C. 1994 Selection against inbred song sparrows during a natural population bottleneck. Nature 372, 356-357. (doi:10.1038/372356a0.)
46. Komdeur, J. 1992 Importance of habitat saturation and territory quality for the evolution of cooperative breeding in the Seychelles warbler. Nature 358, 493-495. (doi:10. 1038/358493a0.)
47. Kong, A. et al. 2002 A high-resolution recombination map of the human genome. Nat. Genet. 31, 241-247.
48. Kuroda, Y., Arai, N., Arita, M., Teranishi, M., Hori, T., Harata, M. & Mizuno, S. 2001 Absence of Z-chromosome inactivation for five genes in male chickens. Chromosome Res. 9, 457-468. (doi:10.1023/A:1011672227256.)
49. Lander, E. S. & Green, P. 1987 Construction of multilocus genetic-linkage maps in humans. Proc. Natl Acad. Sci. USA 84, 2363-2367.
50. Lenormand, T. 2003 The evolution of sex dimorphism in recombination. Genetics 163, 811-822.
51. Lynn, A., Kashuk, C., Petersen, M. B., Bailey, J. A., Cox, D. R., Antonarakis, S. E. & Chakravarti, A. 2000 Patterns of meiotic recombination on the long arm of human chromosome 21. Genome Res. 10, 1319-1332. (doi:10. 1101/gr.138100.)
52. McQueen, H. A., McBride, D., Miele, G., Bird, A. P. & Clinton, M. 2001 Dosage compensation in birds. Curr. Biol. 11, 253-257. (doi:10.1016/S0960- 9822(01)00070-7.)
53. McRae, S. B. & Amos, W. 1999 Characterization of hypervariable microsatellites in the cooperatively breeding white-browed sparrow weaver Plocepasser mahali. Mol. Ecol. 8, 903-904.
54. Martinez, J. G., Soler, J. J., Soler, M., Møller, A. P. & Burke, T. 1999 Comparative population structure and gene flow of a brood parasite, the great spotted cuckoo (Clamator glandarius), and its primary host, the magpie (Pica pica). Evolution 53, 269-278.
55. Masabanda, J. S. et al. 2004 Molecular cytogenetic definition of the chicken genome: the first complete avian karyotype. Genetics 166, 1367-1373. (doi:10.1534/genetics.166.3. 1367.)
56. Mellersh, C. S. et al. 1997 A linkage map of the canine genome. Genomics 46, 326-336. (doi:10.1006/geno.1997. 5098.)
57. Merilä, J., Kruuk, L. E. B. & Sheldon, B. C. 2001 Cryptic evolution in a wild bird population. Nature 412, 76-79.
58. Neff, M. W., Broman, K. W., Mellersh, C. S., Ray, K., Acland, G. M., Aguirre, G. D., Ziegle, J. S., Ostrander, E. A. & Rine, J. 1999 A second-generation genetic linkage map of the domestic dog, Canis familiaris. Genetics 151, 803-820.
59. Neumann, K. & Wetton, J. H. 1996 Highly polymorphic microsatellites in the house sparrow Passer domesticus. Mol. Ecol. 5, 307-309. (doi:10.1046/j.1365-294X.1996. 00095.x.)
60. Nishiumi, I., Yamagishi, S., Maekawa, H. & Shimoda, C. 1996 Paternal expenditure is related to brood sex ratio in polygynous great reed warblers. Behav. Ecol. Sociobiol. 39, 211-217. (doi:10.1007/s002650050283.)
61. Norris, K. 1993 Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature 362, 537-539. (doi:10.1038/362537a0.)
62. O'Connell, J. R. & Weeks, D. E. 1998 PedCheck: a program for identification of genotype incompatibilities in linkage analysis. Am. J. Hum. Genet. 63, 259-266. (doi:10.1086/301904.)
63. Otsuka, R., Nishiumi, I. & Wada, M. 2003 Characterisation of 12 polymorphic microsatellite loci in the Japanese bush warbler Cettia diphone. Mol. Ecol. Notes 3, 44-46. (doi:10. 1046/j.1471-8286.2003.00345.x.)
64. Otter, K., Ratclifle, L., Michaud, D. & Boag, P. T. 1998 Do female black-capped chickadees prefer high-ranking males as extra-pair partners? Behav. Ecol. Sociobiol. 43, 25-36. (doi:10.1007/s002650050463.)
65. Otto, S. P. & Lenormand, T. 2002 Resolving the paradox of sex and recombination. Nat. Rev. Genet. 3, 252-261. (doi:10.1038/nrg761.)
66. Petren, K. 1998 Microsatellite primers from Geospiza fortis and cross-species amplification in Darwin's finches. Mol. Ecol. 7, 1782-1784.
67. Piertney, S. B., Marquiss, M. & Summers, R. 1998 Characterization of tetranucleotide microsatellite markers in the Scottish crossbill (Loxia scotica). Mol. Ecol. 7, 1261-1263. (doi:10.1046/j.1365-294x.1998.00493.x.)
68. Plomion, C. & O'Malley, D. M. 1996 Recombination rate differences for pollen parents and seed parents in Pinus pinaster. Heredity 77, 341-350.
69. Primmer, C. R., Møller, A. P. & Ellegren, H. 1995 Resolving genetic relationship with microsatellite markers: a parentage testing system for the swallow Hirundo rustica. Mol. Ecol. 4, 493-498.
70. Primmer, C. R., Raudsepp, T., Chowdhary, B. P., Moller, A. P. & Ellegren, H. 1997 Low frequency of microsatellites in the avian genome. Genome Res. 7, 471-482.
71. Rice, W. R. 2002 Experimental tests of the adaptive significance of sexual recombination. Nat. Rev. Genet. 3, 241-251. (doi:10.1038/nrg760.)
72. Richardson, D. S., Jury, F. L., Dawson, D. A., Salgueiro, P., Komdeur, J. & Burke, T. 2000 Fifty Seychelles warbler (Acrocephalus sechellensis) microsatellite loci polymorphic in Sylviidae species and their cross-species amplification in other passerine birds. Mol. Ecol. 9, 2226-2231. (doi:10. 1046/j.1365-294X.2000.105338.x.)
73. Richman, A. D. & Price, T. 1992 Evolution of ecological differences in the Old World leaf Warblers. Nature 355, 817-821. (doi:10.1038/355817a0.)
74. Saetre, G. P., Borge, T., Lindroos, K., Haavie, J., Sheldon, B. C., Primmer, C. & Syvanen, A. C. 2003 Sex chromosome evolution and speciation in Ficedula flycatchers. Proc. R. Soc. B 270, 53-59. (doi:10.1098/rspb.2002. 2204.)
75. Sakamoto, T. et al. 2000 A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155, 1331-1345.
76. Saladin, V., Bonfils, D., Binz, T. & Richner, H. 2003 Isolation and characterization of 16 microsatellite loci in the Great Tit Parus major. Mol. Ecol. Notes 3, 520-522. (doi:10. 1046/j.1471-8286.2003.00498.x.)
77. Samollow, P. B., Kammerer, C. M., Mahaney, S. M., Schneider, J. L., Westenberger, S. J., VandeBerg, J. L. & Robinson, E. S. 2004 First-generation linkage map of the gray, short-tailed opossum, Monodelphis domestica, reveals genome-wide reduction in female recombination rates. Genetics 166, 307-329. (doi:10.1534/genetics.166.1.307.)
78. Slate, J., Visscher, P. M., MacGregor, S., Stevens, D., Tate, M. L. & Pemberton, J. M. 2002 A genome scan for quantitative trait loci in a wild population of red deer (Cervus elaphus). Genetics 162, 1863-1873.
79. Stauss, M., Tomiuk, J., Segelbacher, G., Driesel, S., Fietz, J., Bachmann, L. & Kompf, J. 2003 Sex-specific recombination rates in Parus major and P. caeruleus, an exception to Huxley's rule. Hereditas 139, 199-205. (doi:10.1111/j. 1601-5223.2003.01698.x.)
80. Trivers, R. 1988 Sex differences in rates of recombination and sexual selection. In The evolution of sex (ed. R. Michod & B. Levin), pp. 270-286. Sunderland, MA: Sinauer.
81. Veen, T., Borge, T., Griffith, S. C., Sætre, G. P., Bures, S., Gustafsson, L. & Sheldon, B. C. 2001 Hybridization and adaptive mate choice in flycatchers. Nature 411, 45-50. (doi:10.1038/35075000.)
82. Westerdahl, H., Bensch, S., Hansson, B., Hasselquist, D. & von Schantz, T. 2000 Brood sex ratios, female harem status and resources for nestling provisioning in the great reed warbler. Behav. Ecol. Sociobiol. 47, 312-318. (doi:10. 1007/s002650050671.)
83. Westerdahl, H., Hansson, B., Bensch, S. & Hasselquist, D. 2004 Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? J. Evol. Biol. 17, 485-492. (doi:10.1111/j.1420-9101.2004. 00711.x.)
84. Xu, H. L., Swoboda, I., Bhalla, P. L. & Singh, M. B. 1999 Male gametic cell-specific gene expression in flowering plants. Proc. Natl Acad. Sci. USA 96, 2554-2558. (doi:10. 1073/pnas.96.5.2554.)