Molecular population genetics of the male and female mitochondrial DNA molecules of the California Sea Mussel, Mytilus californianus

Genetics

Volumn 177, Issue 2, 2007, Pages 1087-1099

  Ort, Brian S ^a,b   Pogson, Grant H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAN FRANCISCO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; DNA POLYMORPHISM; FEMALE; GENE FREQUENCY; GENE LOCUS; GENE MUTATION; GENE SEQUENCE; GENETIC SELECTION; GENETIC VARIABILITY; GENOME ANALYSIS; MALE; MOLECULAR GENETICS; MUSSEL; MUTATION RATE; NONHUMAN; POPULATION GENETICS; PRIORITY JOURNAL;

ANIMALS; BASE SEQUENCE; CALIFORNIA; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; FEMALE; GENETICS, POPULATION; MALE; MITOCHONDRIAL PROTEINS; MUTATION; MYTILUS; POLYMORPHISM, GENETIC; SELECTION (GENETICS);

MYTILIDAE; MYTILUS CALIFORNIANUS;

EID: 35548958624     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.072934     Document Type: Article

References (73)

1. AVISE, J. C., J. ARNOLD, R. M. BALL, E. BERMINGHAM, T. LAMB et al., 1987 Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Syst. 18: 489-522.
2. BALLARD, J. W. O., and M. C. WHITLOCK, 2004 The incomplete natural history of mitochondria. Mol. Ecol. 13: 729-744.
3. BAZIN, E., S. GLEMIN and N. GALTIER, 2006 Population size does not influence mitochondrial genetic diversity in animals. Science 312: 570-572.
4. BEAGLEY, C. T., K. A. TAYLOR and D. R. WOSTENHOLME, 1997 Gender-associated diverse mitochondrial DNA molecules of the mussel, Mytilus californianus. Curr. Genet. 31: 318-324.
5. BRETON, S., G. BURGER, D. T. STEWART and P. U. BLIER, 2006 Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.). Genetics 172: 1107-1119.
6. BROWN, W. M., M. GEORGE and A. C. WILSON, 1979 Rapid evolution of animal mitochondrial DNA. Proc. Natl. Acad. Sci. USA 76: 1967-1971.
7. BURTON, R. S., 1998 Intraspecific phylogeography across the Point Conception biogeographic boundary. Evolution 52: 734-745.
8. BURZYNSKI, A., M. ZBAWICKA, D. O. F. SKIBINSKI and R. WENNE, 2003 Evidence for recombination of mtDNA in the marine mussel Mytilus trossulus from the Baltic. Mol. Biol. Evol. 20: 388-392.
9. BURZYNSKI, A., M. ZBAWICKA, D. O. F. SKIBINSKI and R. WENNE, 2006 Doubly uniparental inheritance is associated with high polymorphism for rearranged and recombinant control region haplotypes in Baltic Mytilus trossulus. Genetics 174: 1081-1094.
10. CLARK, A. G., and E. M. LYCKEGAARD, 1988 Natural selection with nuclear and cytoplasmic transmission. III. Joint analysis of segregation and mtDNA in Drosophila melanogaster. Genetics 118: 471-481.
11. DENVER, D. R., K. MORRIS, M. LYNCH, L. L. VASSILIEVA and W. K. THOMAS, 2000 High direct estimate of the mutation rate in the mitochondrial genome of Caenorhabditis elegans. Science 289: 2342-2344.
12. ENGEL, J. D., 2004 Population genetic structure of the California sea mussel: influence of the Pleistocene, biogeography, and microevolutionary processes. Ph.D. Thesis, University of California, Santa Cruz, CA.
13. EVERETT, E. M., P. J. WILLIAMS, G. GIBSON and D. T. STEWART, 2004 Mitochondrial DNA polymorphisms and sperm motility in Mytilus edulis (Bivalvia; Mytilidae). J. Exp. Zool. 301: 906-910.
14. EYRE-WALKER, A., 2002 Changing effective population size and the McDonald-Kreitman test. Genetics 162: 2017-2024.
15. FISHER, C., and D. O. F. SKIBINSKI, 1990 Sex-biased mitochondrial heteroplasmy in the marine mussel Mytilus. Proc. R. Soc. Lond. B Biol. Sci. 242: 149-156.
16. GRANT, W. S., I. B. SPIES and M. F. CANINO, 2006 Biogeographic evidence for selection on mitochondrial DNA in the north Pacific walleye pollock Theragra chalcogramma. J. Hered. 97: 571-580.
17. GRANTHAM, R., 1974 Amino acid difference formula to help explain protein evolution. Science 185: 862-864.
18. HAAG-LIAUTARD, C., M. DORRIS, X. MASIDE, S. MACASKILL, D. L. HALLIGAN et al., 2007 Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature 445: 82-85.
19. HEY, J, and R. NIELSEN, 2004 Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167: 747-760.
20. HO, S. Y. W., M. J. PHILLIPS, A. COOPER and A. J. DRUMMOND, 2005 Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol. Biol. Evol. 22: 1561-1568.
21. HOEH, W. R., D. T. STEWART, B. W. SUTHERLAND and E. ZOUROS, 1996 Multiple origins of gender-associated mitochondrial DNA lineages in bivalves (Mollusca: Bivalvia). Evolution 50: 2276-2286.
22. HOEH, W. R., D. T. STEWART and S. I. GUTTMAN, 2002 High fidelity of mitochondrial genome transmission under the doubly uniparental mode of inheritance in freshwater mussels (Bivalvia: Unionidae). Evolution 56: 2252-2261.
23. HOFFMAN, R. J., J. L. BOORE and W. M. BROWN, 1992 A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131: 397-412.
24. HOWELL, N., C. B. SMEJKAL, D. A. MACKEY, P. F. CHINNERY, D. M. TURNBULL et al., 2003 The pedigree rate of sequence divergence in the human mitochondrial genome: there is a difference between phylogenetic and pedigree rates. Am. J. Hum. Genet. 75: 659-670.
25. HUDSON, R. R., and N. L. KAPLAN, 1985 Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111: 147-164.
26. JAMES, A. C., and J. W. O. BALLARD, 2003 Mitochondrial genotype affects fitness in Drosophila simulans. Genetics 164: 187-194.
27. KUMAR, S., K. TAMURA and M. NEI, 2004 MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief. Bioinform. 5: 150-163.
28. LADOUKAKIS, E. D., and E. ZOUROS, 2001 Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol. Biol. Evol. 18: 1168-1175.
29. LEVINTON, J. S., and R. K. KOEHN, 1976 Population genetics of mussels, pp. 357-384 in Marine Mussels: Their Ecology and Physiology, edited by B. L. BAYNE. Cambridge University Press, Cambridge, UK.
30. LEVINTON, J. S., and T. H. SUCHANEK, 1978 Geographic variation, niche breadth and genetic differentiation at different geographic scales in the mussels Mytilus californianus and M. edulis. Mar. Biol. 49: 363-375.
31. LI, H., and W. STEPHAN, 2006 Inferring the demographic history and rate of adaptive substitution in Drosophila. PLoS Genet. 2: 1580-1589.
32. LI, W.-H., C.-I. WU and C.-C. LUO, 1985 A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol. Biol. Evol. 2: 150-174.
33. LIU, H. P., J. B. MITTON and S. K. WU, 1996 Paternal mitochondrial DNA differentiation far exceeds maternal mitochondrial DNA and allozyme differentiation in the freshwater mussel, Anodonta grandis grandis. Evolution 50: 952-957.
34. MCDONALD, J. H., and M. KREITMAN, 1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652-654.
35. MCVEAN, G., P. AWADALLA and P. FEARNHEAD, 2002 A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160: 1231-1241.
36. NACHMAN, M. W., 1998 Deleterious mutations in animal mitochondrial DNA. Genetica 103: 61-69.
37. NACHMAN, M. W., W. M. BROWN, M. STONEKING and C. F. AQUADRO, 1996 Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics 142: 953-963.
38. NIELSEN, R., and J. WAKELEY, 2001 Distinguishing isolation from migration: a Markov chain Monte Carlo approach. Genetics 158: 885-896.
39. PASSAMONTI, M., and V. SCALI, 2001 Gender-associated mitochondrial DNA heteroplasmy in the venerid clam Tapes philippinarum (Mollusca: Bivalvia). Curr. Genet. 39: 117-124.
40. PASSAMONTI, M., J. L. BOORE and V. SCALI, 2003 Molecular evolution and recombination in gender-associated mitochondrial DNAs of the Manila clam Tapes philippinarum. Genetics 164: 603-611.
41. POGSON, G., H., K. A. MESA and R. G. BOUTILIER, 1995 Genetic population structure and gene flow in the Atlantic cod Gadus morhua: a comparison of allozyme and nuclear RFLP loci. Genetics 139: 375-385.
42. POSADA, D., and K. CRANDALL, 1998 MODELTEST: testing themodel of DNA substitution. Bioinformatics 14: 817-818.
43. QUESADA, H., R. WENNE and D. O. F. SKIBINSKI, 1995 Differential introgression of mitochondrial DNA across species boundaries within the marine mussel genus Mytilus. Proc. R. Soc. Lond. B Biol. Sci. 262: 51-56.
44. QUESADA, H., C. GALLAGHER, D. A. G. SKIBINSKI and D. O. F. SKIBINSKI 1998a Patterns of polymorphism and gene flow of gender-associated mitochondrial DNA lineages in European mussel populations. Mol. Ecol. 7: 1041-1051.
45. QUESADA, H., M. WARREN and D. O. F. SKIBINSKI, 1998b Nonneutral evolution and differential mutation rate of gender-associated mitochondrial DNA lineages in the marine mussel Mytilus. Genetics 149: 1511-1526.
46. QUESADA, H., R. WENNE and D. O. F. SKIBINSKI, 1999 Interspecies transfer of female mitochondrial DNA is coupled with role-reversals and departure from neutrality in the mussel Mytilus trossulus. Mol. Biol. Evol. 16: 655-665.
47. RAMBAUT, A., and A. DRUMMOND, 2005 TRACER, version 1.3. (http://evolve.zoo.ox.ac.uk).
48. RAND, D. M., 2001 The units of selection on mitochondrial DNA. Annu. Rev. Ecol. Syst. 32: 415-448.
49. RAND, D. M., and L. M. KANN, 1996 Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol. Biol. Evol. 13: 735-748.
50. RAND, D. M., and L. M. KANN, 1998 Mutation and selection at silent and replacement sites in the evolution of animal mitochondrial DNA. Genetica 103: 393-407.
51. RAWSON, P. D., 2005 Nonhomologous recombination between the large unassigned region of the male and female mitochondrial genomes in the mussel, Mytilus trossulus. J. Mol. Evol. 61: 717-732.
52. RAWSON, P. D., and T. J. HILBISH, 1995 Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex. Mol. Biol. Evol. 12: 893-901.
53. RAWSON, P. D., and T. J. HILBISH, 1998 Asymmetric introgression of mitochondrial DNA among European populations of blue mussels (Mytilus spp.). Evolution 52: 100-108.
54. RAWSON, P. D., C. L. SECOR and T. J. HILBISH, 1996 The effects of natural hybridization on the regulation of doubly uniparental mtDNA inheritance in blue mussels (Mytilus spp.). Genetics 144: 241-248.
55. RIGINOS, C., M. J. HICKERSON, C. M. HENZER and C. W. CUNNINGHAM, 2004 Differential patterns of male and female mtDNA exchange across the Atlantic Ocean in the blue mussel, Mytilus edulis. Evolution 58: 2438-2451.
56. RONQUIST, F., and J. P. HUELSENBECK, 2003 MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
57. ROZAS, J., J. C. SANCHEZ-DELBARRIO, X. MESSEGUER and R. ROZAS, 2003 DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
58. RUIZ-PESINI, E., D. MISHMAR, M. BRANDON, V. PROCACCIO and D. C. WALLACE, 2004 Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303: 223-226.
59. SAAVEDRA, C., D. T. STEWART, R. R. STANWOOD and E. ZOUROS, 1996 Species-specific segregation of gender-associated mitochondrial DNA types in an area where two mussel species (Mytilus edulis and M. trossulus) hybridize. Genetics 143: 1359-1367.
60. SCHMIDT, T. R., W. WU, M. GOODMAN and L. I. GROSSMAN, 2001 Evolution of nuclear- and mitochondrial-encoded subunit interaction in cytochrome c oxidase. Mol. Biol. Evol. 18: 563-569.
61. SCHNEIDER, S., D. ROESSLI and L. EXCOFFIER, 2000 Arlequin (Version 2.000): A Software for Population Genetic Analyses. Genetics and Biometry Laboratory, University of Geneva, Geneva.
62. SKIBINSKI, D. O. F., C. GALLAGHER and C. M. BEYNON, 1994 Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics 138: 801-809.
63. SKIBINSKI, D. O. F., C. GALLAGHER and H. QUESADA, 1999 On the roles of selection, mutation and drift in the evolution of mitochondrial DNA diversity in British Mytilus edulis (Mytilidae; Mollusca) populations. Biol. J. Linn. Soc. Lond. 68: 195-213.
64. SMIETANKA, B., M. ZBAWICKA, M. WOLOWICZ and R. WENNE, 2004 Mitochondrial DNA lineages in the European populations of mussels (Mytilus spp.). Mar. Biol. 146: 79-92.
65. STEWART, D. T., C. SAAVEDRA, R. R. STANWOOD, A. O. BALL and E. ZOUROS, 1995 Male and female mitochondrial DNA lineages in the blue mussel (Mytilus edulis) species group. Mol. Biol. Evol. 12: 735-747.
66. STEWART, D. T., E. R. KENCHINGTON, R. K. SINGH and E. ZOUROS, 1996 Degree of selective constraint as an explanation of the different rates of evolution of gender-specific mitochondrial DNA lineages in the mussel Mytilus. Genetics 143: 1349-1357.
67. TAJIMA, F., 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
68. WARES, J. P., and C. W. CUNNINGHAM, 2001 Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55: 2455-2469.
69. WENNE, R., and D. O. F. SKIBINSKI, 1995 Mitochondrial DNA heteroplasmy in European populations of the mussel Mytilus trossulus. Mar. Biol. 122: 619-624.
70. WILLETT, C. S., and R. S. BURTON, 2004 Evolution of interacting proteins in the mitochondrial electron transport system in a marine copepod. Mol. Biol. Evol. 21: 443-453.
71. WILLIAMSON, S. H., R. HERNANDEZ, A. FLEDEL-ALON, L. ZHU, R. NIELSEN et al., 2005 Simultaneous inference of selection and population growth from patterns of variation in the human genome. Proc. Natl. Acad. Sci. USA 102: 7882-7887.
72. WOOD, A. R., G. TURNER, D. O. F. SKIBINSKI and A. R. BEAUMONT, 2003 Disruption of doubly uniparental inheritance of mitochondrial DNA in hybrid mussels (Mytilus edulis X M. galloprovincialis). Heredity 91: 354-360.
73. ZOUROS, E., A. O. BALL, C. SAAVEDRA and K. R. FREEMAN, 1994 An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc. Natl. Acad. Sci. USA 91: 7463-7467.