Factors affecting germline mutations in a hypervariable microsatellite: A comparative analysis of six species of swallows (Aves: Hirundinidae)

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 708, Issue 1-2, 2011, Pages 37-43

  Anmarkrud, Jarl A ^a   Kleven, Oddmund ^a   Augustin, Jakob ^b   Bentz, Kristofer H ^a   Blomqvist, Donald ^b   Fernie, Kim J ^c   Magrath, Michael J L ^d   Pärn, Henrik ^a,e   Quinn, James S ^f   Robertson, Raleigh J ^g   Szép, Tibor ^h   Tarof, Scott ⁱ   Wagner, Richard H ^j,k   Lifjeld, Jan T ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c ENVIRONMENT CANADA   (Canada)

^d Department of Wildlife Conservation and Science Zoos Victoria ^*  (Australia)

^e NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^f MCMASTER UNIVERSITY   (Canada)

^g QUEEN S UNIVERSITY   (Canada)

^h Department of Agricultural Sciences and Environmental Management   (Hungary)

ⁱ YORK UNIVERSITY   (Canada)

^j KONRAD LORENZ INSTITUTE FOR ETHOLOGY   (Austria)

^k UNIVERSITY OF VETERINARY MEDICINE   (Austria)

more..

Author keywords

Extrapair paternity; Germline mutations; Hirundinidae; HrU10; Microsatellite evolution; Mutation rates; Sperm competition

Indexed keywords

NUCLEOTIDE;

ALLELE; ANIMAL CELL; ARTICLE; BIRD; BREEDING; CANADA; CONTROLLED STUDY; GAMETOGENESIS; GERMLINE MICRONUCLEUS; HIRUNDINIDAE; MICROSATELLITE MARKER; MUTATIONAL ANALYSIS; NONHUMAN; POPULATION GENETICS; PRIORITY JOURNAL; SEX DIFFERENCE; SPERM COMPETITION; TACHYCINETA BICOLOR;

ANIMALS; EVOLUTION, MOLECULAR; FEMALE; GENETIC MARKERS; GENETICS, POPULATION; GERM-LINE MUTATION; MALE; MICROSATELLITE REPEATS; ONTARIO; RURAL POPULATION; SWALLOWS;

AVES; HIRUNDINIDAE; TACHYCINETA; TACHYCINETA BICOLOR;

EID: 79952449674     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2011.01.006     Document Type: Article

References (83)

1. Goldstein D.B., Schlötterer C. Microsatellites: Evolution and Applications 1999, Oxford University Press, Oxford.
2. Li Y.C., Korol A.B., Fahima T., Beiles A., Nevo E. Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol. Ecol. 2002, 11:2453-2465.
3. Primmer C.R., Møller A.P., Ellegren H. New microsatellites from the pied flycatcher Ficedula hypoleuca and the swallow Hirundo rustica genomes. Hereditas 1996, 124:281-283.
4. Levinson G., Gutman G.A. Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol. Biol. Evol. 1987, 4. 2032-2021.
5. Strand M., Prolla T.A., Liskay R.M., Petes T.D. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 1993, 365:274-276.
6. Kimura M., Ohta T. Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc. Natl. Acad. Sci. USA 1978, 75:2868-2872.
7. Anderson T.J., Su X.Z., Roddam A., Day K.P. Complex mutations in a high proportion of microsatellite loci from the protozoan parasite Plasmodium falciparum. Mol. Ecol. 2000, 9:1599-1608.
8. Chakraborty R., Kimmel M., Stivers D.N., Davison L.J., Deka R. Relative mutation rates at di-, tri-, and tetranucleotide microsatellite loci. Proc. Natl. Acad. Sci. USA 1997, 94:1041-1046.
9. Schlötterer C., Ritter R., Harr B., Brem G. High mutation rate of a long microsatellite allele in Drosophila melanogaster provides evidence for allele-specific mutation rates. Mol. Biol. Evol. 1998, 15:1269-1274.
10. Eckert K.A., Yan G., Hile S.E. Mutation rate and specificity analysis of tetranucleotide microsatellite DNA alleles in somatic human cells. Mol. Carcinog. 2002, 34:140-150.
11. Boyer J.C., Hawk J.D., Stefanovic L., Farber R.A. Sequence-dependent effect of interruptions on microsatellite mutation rate in mismatch repair-deficient human cells. Mutat. Res. 2008, 640:89-96.
12. Harr B., Todorova J., Schlötterer C. Mismatch repair-driven mutational bias in D. melanogaster. Mol. Cell. 2002, 10:199-205.
13. Hawk J.D., Stefanovic L., Boyer J.C., Petes T.D., Farber R.A. Variation in efficiency of DNA mismatch repair at different sites in the yeast genome. Proc. Natl. Acad. Sci. USA 2005, 102:8639-8643.
14. Pearson C.E., Eichler E.E., Lorenzetti D., Kramer S.F., Zoghbi H.Y., Nelson D.L., Sinden R.R. Interruptions in the triplet repeats of SCA1 and FRAXA reduce the propensity and complexity of slipped strand DNA (S-DNA) formation. Biochemistry 1998, 37:2701-2708.
15. Riley D.E., Jeon J.S., Krieger J.N. Simple repeat evolution includes dramatic primary sequence changes that conserve folding potential. Biochem. Biophys. Res. Commun. 2007, 355:619-625.
16. Ellegren H., Lindgren G., Primmer C.R., Møller A.P. Fitness loss and germline mutations in barn swallows breeding in Chernobyl. Nature 1997, 389:593-596.
17. Beck N.R., Double M.C., Cockburn A. Microsatellite evolution at two hypervariable loci revealed by extensive avian pedigrees. Mol. Biol. Evol. 2003, 20:54-61.
18. Brohede J., Primmer C.R., Møller A.P., Ellegren H. Heterogeneity in the rate and pattern of germline mutation at individual microsatellite loci. Nucleic Acids Res. 2002, 30:1997-2003.
19. Ellegren H. Heterogeneous mutation processes in human microsatellite DNA sequences. Nat. Genet. 2000, 24:400-402.
20. Hoekert W.E., Neufeglise H., Schouten A.D., Menken S.B. Multiple paternity and female-biased mutation at a microsatellite locus in the olive ridley sea turtle (Lepidochelys olivacea). Heredity 2002, 89:107-113.
21. Lai Y., Sun F. The relationship between microsatellite slippage mutation rate and the number of repeat units. Mol. Biol. Evol. 2003, 20:2123-2131.
22. Paun O., Hörandl E. Evolution of hypervariable microsatellites in apomictic polyploid lineages of Ranunculus carpaticola: directional bias at dinucleotide loci. Genetics 2006, 174:387-398.
23. Whittaker J.C., Harbord R.M., Boxall N., Mackay I., Dawson G., Sibly R.M. Likelihood-based estimation of microsatellite mutation rates. Genetics 2003, 164:781-787.
24. Primmer C.R., Saino N., Møller A.P., Ellegren H. Unraveling the processes of microsatellite evolution through analysis of germ line mutations in barn swallows. Mol. Biol. Evol. 1998, 15:1047-1054.
25. Bohossian H.B., Skaletsky H., Page D.C. Unexpectedly similar rates of nucleotide substitution found in male and female hominids. Nature 2000, 406:622-625.
26. Makova K.D., Li W.-H. Strong male-driven evolution of DNA sequences in humans and apes. Nature 2002, 416:624-626.
27. Ellegren H. Characteristics, causes and evolutionary consequences of male-biased mutation. Proc. R. Soc. B 2007, 274:1-10.
28. Hurst L.D., Ellegren H. Sex biases in the mutation rate. Trends Genet. 1998, 14:446-452.
29. Li W.-H., Yi S., Makova K. Male-driven evolution. Curr. Opin. Genet. Dev. 2002, 12:650-656.
30. Anmarkrud J.A., Kleven O., Bachmann L., Lifjeld J.T. Microsatellite evolution: Mutations, sequence variation, and homoplasy in the hypervariable avian microsatellite locus HrU10. BMC Evol. Biol. 2008, 8:138.
31. Petrie M., Roberts G. Sexual selection and the evolution of evolvability. Heredity 2006, 98:198-205.
32. Cotton S., Wedekind C. Male mutation bias and possible long-term effects of human activities. Conserv. Biol. 2010, 24:1190-1197.
33. Kirkpatrick M., Ryan M.J. The evolution of mating preferences and the paradox of the lek. Nature 1991, 350:33-38.
34. Bartosch-Harlid A., Berlin S., Smith N.G., Møller A.P., Ellegren H. Life history and the male mutation bias. Evolution 2003, 57:2398-2406.
35. Møller A.P., Cuervo J.J. Sexual selection, germline mutation rate and sperm competition. BMC Evol. Biol. 2003, 3:6.
36. Petrie M., Doums C., Møller A.P. The degree of extra-pair paternity increases with genetic variability. Proc. Natl. Acad. Sci. USA 1998, 95:9390-9395.
37. Møller A.P., Cuervo J.J. Minisatellite mutation rates increase with extra-pair paternity among birds. BMC Evol. Biol. 2009, 9:100.
38. Amos W. Sexual selection does not influence minisatellite mutation rate. BMC Evol. Biol. 2009, 9.
39. Griffith S.C., Owens I.P.F., Thuman K.A. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 2002, 11:2195-2212.
40. Primmer C.R., Møller A.P., Ellegren H. A wide-range survey of cross-species microsatellite amplification in birds. Mol. Ecol. 1996, 5:365-378.
41. Delmore K.E., Kleven O., Laskemoen T., Crowe S.A., Lifjeld J.T., Robertson R.J. Sex allocation and parental quality in tree swallows. Behav. Ecol. 2008, 19:1243-1249.
42. Kleven O., Jacobsen F., Robertson R.J., Lifjeld J.T. Extrapair mating between relatives in the barn swallow: a role for kin selection?. Biol. Lett. 2005, 1:389-392.
43. Møller A.P., Brohede J., Cuervo J.J., de Lope F., Primmer C.R. Extrapair paternity in relation to sexual ornamentation, arrival date, and condition in a migratory bird. Behav. Ecol. 2003, 14:707-712.
44. Neuman C.R., Safran R.J., Lovette I.J. Male tail streamer length does not predict apparent or genetic reproductive success in North American barn swallows Hirundo rustica erythrogaster. J. Avian Biol. 2007, 38:28-36.
45. O'Brien E.L., Dawson R.D. Context-dependent genetic benefits of extra-pair mate choice in a socially monogamous passerine. Behav. Ecol. Sociobiol. 2007, 61:775-782.
46. Whittingham L.A., Dunn P.O. Survival of extrapair and within-pair young in tree swallows. Behav. Ecol. 2001, 12:496-500.
47. Dawson D.A., Burke T., Hansson B., Pandhal J., Hale M.C., Hinten G.N., Slate J. A predicted microsatellite map of the passerine genome based on chicken-passerine sequence similarity. Mol. Ecol. 2006, 15:1299-1320.
48. Yauk C.L., Quinn J.S. Multilocus DNA fingerprinting reveals high rate of heritable genetic mutation in herring gulls nesting in an industrialized urban site. Proc. Natl. Acad. Sci. USA 1996, 93. 12337-12141.
49. Somers C.M., Yauk C.L., White P.A., Parfett C.L.J., Quinn J.S. Air pollution induces heritable DNA mutations. Proc. Natl. Acad. Sci. USA 2002, 99:15904-15907.
50. Sheldon F.H., Whittingham L.A., Moyle R.G., Slikas B., Winkler D.W. Phylogeny of swallows (Aves: Hirundinidae) estimated from nuclear and mitochondrial DNA sequences. Mol. Phylogenet. Evol. 2005, 35:254-270.
51. Stutchbury B.J.M., Hill J.R., Kramer P.M., Rush S.A., Tarof S.A. Sex and age-specific annual survival in a Neotropical migratory songbird, the purple martin (Progne subis). Auk 2009, 126:278-287.
52. Bentz K.H. Germline mutation rate of the microsatellite HrU10 in tree swallows, Tachycineta bicolor, in an area with high PAH pollution. The Natural History Museum 2009, University of Oslo, Oslo, pp. 23.
53. Whittingham L.A., Lifjeld J.T. Extra-pair fertilizations increase the opportunity for sexual selection in the monogamous house martin (Delichon urbica). J. Avian Biol. 1995, 26:283-288.
54. Augustin J., Blomqvist D., Szép T., Szabó Z., Wagner R. No evidence of genetic benefits from extra-pair fertilisations in female sand martins (Riparia riparia). J. Ornithol. 2007, 148:189-198.
55. Magrath M., Santema P., Bouwman K., Brinkhuizen D., Griffith S., Langmore N. Seasonal decline in reproductive performance varies with colony size in the fairy martin, Petrochelidon ariel. Behav. Ecol. Sociobiol. 2009, 63:661-672.
56. Magrath M.J.L., Elgar M.A. Paternal care declines with increased opportunity for extra-pair matings in fairy martins. Proc. R. Soc. Lond. B 1997, 264:1731-1736.
57. Ellegren H. Microsatellite mutations in the germline: Implications for evolutionary inference. Trends Genet. 2000, 16:551-558.
58. Freckleton R.P., Harvey P.H., Pagel M. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 2002, 160:712-726.
59. Pagel M. Inferring the historical patterns of biological evolution. Nature 1999, 401:877-884.
60. R Development Core Team (2010). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL: http://www.r-project.org/.
61. Paradis E., Claude J., Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 2004, 20:289-290.
62. Woodruff R.C., Thompson J.N. Have premeiotic clusters of mutation been overlooked in evolutionary theory?. J. Evol. Biol. 1992, 5:457-464.
63. Somers C.M., McCarry B.E., Malek F., Quinn J.S. Reduction of particulate air pollution lowers the risk of heritable mutations in mice. Science 2004, 304:1008-1010.
64. Huang Q.Y., Xu F.H., Shen H., Deng H.Y., Liu Y.J., Liu Y.Z., Li J.L., Recker R.R., Deng H.W. Mutation patterns at dinucleotide microsatellite loci in humans. Am. J. Hum. Genet. 2002, 70:625-634.
65. Jeffreys A.J., Tamaki K., MacLeod A., Monckton D.G., Neil D.L., Armour J.A.L. Complex gene conversion events in germline mutation at human minisatellites. Nat. Genet. 1994, 6:136-145.
66. Marvin C.H., Allan L., McCarry B.E., Bryant D.W. Chemico/biological investigation of contaminated sediment from the hamilton harbour area of Western Lake Ontario. Environ. Mol. Mutagen. 1993, 22:61-70.
67. Yauk C.L., Fox G.A., McCarry B.E., Quinn J.S. Induced minisatellite germline mutations in herring gulls (Larus argentatus) living near steel mills. Mutat. Res. 2000, 452:211-218.
68. Lofts B., Murton R.K. Reproduction in birds. Avian Biology 1973, 1-107. Academic Press, London. D.S. Farner, J.R. King, K.C. Parkes (Eds.).
69. Møller A.P., Mousseau T.A., Lynnn C., Ostermiller S., Rudolfsen G. Impaired swimming behaviour and morphology of sperm from barn swallows Hirundo rustica in Chernobyl. Mutat. Res. 2008, 650:210-216.
70. Crow J.F. The origins, patterns and implications of human spontaneous mutation. Nat. Rev. Genet. 2000, 1:40-47.
71. Brinkmann B., Klintschar M., Neuhuber F., Huhne J., Rolf B. Mutation rate in human microsatellites: influence of the structure and length of the tandem repeat. Am. J. Hum. Genet. 1998, 62:1408-1415.
72. Weber J.L., Wong C. Mutation of human short tandem repeats. Hum. Mol. Genet. 1993, 2:1123-1128.
73. Ellegren H., Fridolfsson A.-K. Male-driven evolution of DNA sequences in birds. Nat. Genet. 1997, 17:182-184.
74. Berlin S., Brandström M., Backström N., Axelsson E., Smith N., Ellegren H. Substitution rate heterogeneity and the male mutation bias. J. Mol. Evol. 2006, 62:226-233.
75. Ortego J., Aparicio J.M., Cordero P.J., Calabuig G. Characteristics of loci and individuals are associated with germline microsatellite mutation rates in lesser kestrels (Falco naumanni). Mutat. Res. 2008, 648:82-86.
76. Crozier R.H., Kaufmann B., Carew M.E., Crozier Y.C. Mutability of microsatellites developed for the ant Camponotus consobrinus. Mol. Ecol. 1999, 8:271-276.
77. Primmer C.R., Møller A.P., Ellegren H. Resolving genetic relationships with microsatellite markers: a parentage testing system for the swallow Hirundo rustica. Mol. Ecol. 1995, 4:493-498.
78. Double M.C., Dawson D., Burke T., Cockburn A. Finding the fathers in the least faithful bird: a microsatellite-based genotyping system for the superb fairy-wren Malurus cyaneus. Mol. Ecol. 1997, 6:691-693.
79. Hunt P.A., Hassold T.J. Sex matters in meiosis. Science 2002, 296:2181-2183.
80. Eward K.L., Obermann E.C., Shreeram S., Loddo M., Fanshawe T., Williams C., Jung H.-I., Prevost A.T., Blow J.J., Stoeber K., Williams G.H. DNA replication licensing in somatic and germ cells. J. Cell. Sci. 2004, 117:5875-5886.
81. Bell S.P., Dutta A. DNA replication in eukaryotic cells. Annu. Rev. Biochem. 2002, 71:333-374.
82. Labib K., Diffley J.F.X. Is the MCM2-7 complex the eukaryotic DNA replication fork helicase?. Curr. Opin. Genet. Dev. 2001, 11:64-70.
83. Lei M., Tye B. Initiating DNA synthesis: from recruiting to activating the MCM complex. J. Cell. Sci. 2001, 114:1447-1454.