Patterns of molecular evolution in caenorhabditis preclude ancient origins of selfing

Genetics

Volumn 178, Issue 4, 2008, Pages 2093-2104

  Cutter, Asher D ^a,d   Wasmuth, James D ^b   Washington, Nicole L ^c  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE;

ARTICLE; BIOLOGICAL MODEL; CAENORHABDITIS; CAENORHABDITIS BRENNERI; CAENORHABDITIS BRIGGSAE; CAENORHABDITIS ELEGANS; CAENORHABDITIS REMANEI; CODON; CONTROLLED STUDY; MATING; MOLECULAR EVOLUTION; NONHUMAN; OUTCROSSING; PRIORITY JOURNAL; SELFING; ANIMAL; CROSS BREEDING; DNA BASE COMPOSITION; FEMALE; GENE; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; INBREEDING; MALE; PHYLOGENY; SEQUENCE HOMOLOGY; TIME;

CAENORHABDITIS; CAENORHABDITIS BRIGGSAE; CAENORHABDITIS ELEGANS;

ANIMALS; BASE COMPOSITION; CAENORHABDITIS; CODON; CROSSES, GENETIC; EVOLUTION, MOLECULAR; FEMALE; GENE EXPRESSION REGULATION; GENES, HELMINTH; INBREEDING; MALE; MODELS, GENETIC; PHYLOGENY; SELECTION (GENETICS); SEQUENCE HOMOLOGY, NUCLEIC ACID; TIME FACTORS; VARIATION (GENETICS);

EID: 44649164281     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.085787     Document Type: Article

References (94)

1. AKASHI, H., 1995 Inferring weak selection from patterns of polymorphism and divergence at silent sites in Drosophila DNA. Genetics 139: 1067-1076.
2. BAER, C. F., F. SHAW, C. STEDING, M. BAUMGARTNER, A. HAWKINS et al., 2005 Comparative evolutionary genetics of spontaneous mutations affecting fitness in rhabditid nematodes. Proc. Natl. Acad. Sci. USA 102: 5785-5790.
3. BARRIÈRE, A., and M. A. FÉLIX, 2005 High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr. Biol. 15: 1176-1184.
4. BARRIÈRE, A., and M. A. FÉLIX, 2007 Temporal dynamics and linkage disequilibrium in natural Caenorhabditis elegans populations. Genetics 176: 999-1011.
5. BETANCOURT, A. J., and D. C. PRESGRAVES, 2002 Linkage limits the power of natural selection in Drosophila. Proc. Natl. Acad. Sci. USA 99: 13616-13620.
6. BIERNE, N., and A. EYRE-WALKER, 2006 Variation in synonymous codon use and DNA polymorphism within the Drosophila genome. J. Evol. Biol. 19: 1-11.
7. BULMER, M., 1991 The selection-mutation-drift theory of synonymous codon usage. Genetics 129: 897-907.
8. C. ELEGANS SEQUENCING CONSORTIUM, 1998 Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282: 2012-2018.
9. CHARLESWORTH, B., 1992 Evolutionary rates in partially self-fertilizing species. Am. Nat. 140: 126-148.
10. CHARLESWORTH, B., M. T. MORGAN and D. CHARLESWORTH, 1993 The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289-1303.
11. CHARLESWORTH, B., M. NORDBORG and D. CHARLESWORTH, 1997 The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet. Res. 70: 155-174.
12. CHARLESWORTH, D., 2003 Effects of inbreeding on the genetic diversity of populations. Phil. Trans. R. Soc. Lond. B Biol. Sci. 358: 1051-1070.
13. CHARLESWORTH, D., and S. I. WRIGHT, 2001 Breeding systems and genome evolution. Curr. Opin. Genet. Dev. 11: 685-690.
14. CHASNOV, J. R., and K. L. CHOW, 2002 Why are there males in the hermaphroditic species Caenorhabditis elegans? Genetics 160: 983-994.
15. CHASNOV, J. R., W. K. SO, C. M. CHAN and K. L. CHOW, 2007 The species, sex, and stage specificity of a Caenorhabditis sex pheromone. Proc. Natl. Acad. Sci. USA 104: 6730-6735.
16. COGHLAN, A., and K. H. WOLFE, 2002 Fourfold faster rate of genome rearrangement in nematodes than in Drosophila. Genome Res. 12: 857-867.
17. COMERON, J. M., and T. B. GUTHRIE, 2005 Intragenic Hill-Robertson interference influences selection intensity on synonymous mutations in Drosophila. Mol. Biol. Evol. 22: 2519-2530.
18. CUTTER, A. D., 2004 Sperm-limited fecundity in nematodes: How many sperm are enough? Evolution 58: 651-655.
19. CUTTER, A. D., 2006 Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans. Genetics 172: 171-184.
20. CUTTER, A. D., 2008a Divergence times in Caenorhabditis and Drosophila inferred from direct estimates of the neutral mutation rate. Mol. Biol. Evol. 25: 778-786.
21. CUTTER, A. D., 2008b Multilocus patterns of polymorphism and selection across the X-chromosome of Caenorhabditis remanei. Genetics 178: 1659-1670.
22. CUTTER, A. D., and B. CHARLESWORTH, 2006 Selection intensity on preferred codons correlates with overall codon usage bias in Caenorhabditis remanei. Curr. Biol. 16: 2053-2057.
23. CUTTER, A. D., and B. A. PAYSEUR, 2003 Rates of deleterious mutation and the evolution of sex in Caenorhabditis. J. Evol. Biol. 16: 812-822.
24. CUTTER, A. D., and S. WARD, 2005 Sexual and temporal dynamics of molecular evolution in C. elegans development. Mol. Biol. Evol. 22: 178-188.
25. CUTTER, A. D., L. AVILÉS and S. WARD, 2003 The proximate determinants of sex ratio in C. elegans populations. Genet. Res. 81: 91-102.
26. CUTTER, A. D., S. E. BAIRD and D. CHARLESWORTH, 2006a High nucleotide polymorphism and rapid decay of linkage disequilibrium in wild populations of Caenorhabditis remanei. Genetics 174: 901-913.
27. CUTTER, A. D., M. A. FELIX, A. BARRIERE and D. CHARLESWORTH, 2006b Patterns of nucleotide polymorphism distinguish temperate and tropical wild isolates of Caenorhabditis briggsae. Genetics 173: 2021-2031.
28. CUTTER, A. D., J. WASMUTH and M. L. BLAXTER, 2006c The evolution of biased codon and amino acid usage in nematode genomes. Mol. Biol. Evol. 23: 2303-2315.
29. DENVER, D. R., K. MORRIS, M. LYNCH and W. K. THOMAS, 2004 High mutation rate and predominance of insertions in the Caenorhabditis elegans nuclear genome. Nature 430: 679-682.
30. DURET, L., 2000 tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes. Trends Genet. 16: 287-289.
31. DURET, L., and D. MOUCHIROUD, 1999 Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc. Natl. Acad. Sci. USA 96: 4482-4487.
32. GARCIA, L. R., B. LEBOEUF and P. KOO, 2007 Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes. Genetics 175: 1761-1771.
33. GELDZILER, B., I. CHATTERJEE, P. KADANDALE, E. PUTIRI, R. PATEL et al., 2006 A comparative study of sperm morphology, cytology and activation in Caenorhabditis elegans, Caenorhabditis remanei and Caenorhabditis briggsae. Dev. Genes Evol. 216: 198-208.
34. GRAUSTEIN, A., J. M. GASPAR, J. R. WALTERS and M. F. PALOPOLI, 2002 Levels of DNA polymorphism vary with mating system in the nematode genus Caenorhabditis. Genetics 161: 99-107.
35. HABER, M., M. SCHUNGEL, A. PUTZ, S. MULLER, B. HASERT et al., 2005 Evolutionary history of Caenorhabditis elegans inferred from microsatellites: evidence for spatial and temporal genetic differentiation and the occurrence of outbreeding. Mol. Biol. Evol. 22: 160-173.
36. HILL, R. C., C. EGYDIO DE CARVALHO, J. SALOGIANNIS, B. SCHLAGER, D. PILGRIM et al., 2006 Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. Dev. Cell 10: 531-538.
37. HILLIER, L. W., R. D. MILLER, S. E. BAIRD, A. CHINWALLA, L. A. FULTON et al., 2007 Comparison of C. elegans and C. briggsae genome sequences reveals extensive conservation of chromosome organization and synteny. PLoS Biol. 5: e167.
38. HODGKIN, J., and T. DONIACH, 1997 Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146: 149-164.
39. IKEMURA, T., 1985 Codon usage and transfer-RNA content in unicellular and multicellular organisms. Mol. Biol. Evol. 2: 13-34.
40. JOVELIN, R., B. C. AJIE and P. C. PHILLIPS, 2003 Molecular evolution and quantitative variation for chemosensory behaviour in the nematode genus Caenorhabditis. Mol. Ecol. 12: 1325-1337.
41. KANAYA, S., Y. YAMADA, M. KINOUCHI, Y. KUDO and T. IKEMURA, 2001 Codon usage and tRNA genes in eukaryotes: correlation of codon usage diversity with translation efficiency and with CG-dinucleotide usage as assessed by multivariate analysis. J. Mol. Evol. 53: 290-298.
42. KIM, S. K., J. LUND, M. KIRALY, K. DUKE, M. JIANG et al., 2001 A gene expression map for Caenorhabditis elegans. Science 293: 2087-2092.
43. KIMURA, M., 1968 Evolutionary rate at molecular level. Nature 217: 624-626.
44. KIONTKE, K., and D. H. A. FITCH, 2005 The phylogenetic relationships of Caenorhabditis and other rhabditids, in WormBook, edited by THE C. ELEGANS RESEARCH COMMUNITY. WormBook, http:// www.wormbook.org.
45. KIONTKE, K., and W. SUDHAUS, 2006 Ecology of Caenorhabditis species, in WormBook, edited by D. H. A. FITCH and THE C. ELEGANS RESEARCH COMMUNITY. WormBook, http://www.wormbook.org.
46. KIONTKE, K., N. P. GAVIN, Y. RAYNES, C. ROEHRIG, F. PIANO et al., 2004 Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc. Natl. Acad. Sci. USA 101: 9003-9008.
47. KIONTKE, K., A. BARRIÈRE, I. KOLOTUEV, B. PODBILEWICZ, R. SOMMER et al., 2007 Trends, stasis, and drift in the evolution of nematode vulva development. Curr. Biol. 17: 1925-1937.
48. KLEEMANN, G. A., and A. L. BASOLO, 2007 Facultative decrease in mating resistance in hermaphroditic Caenorhabditis elegans with self-sperm depletion. Anim. Behav. 74: 1339-1347.
49. KOCH, R., H. G. A. M. VAN LUENEN, M. VAN DER HORST, K. L. THIJSSEN and R. H. A. PLASTERK, 2000 Single nucleotide polymorphisms in wild isolates of Caenorhabditis elegans. Genome Res. 10: 1690-1696.
50. KREITMAN, M., and M. ANTEZANA, 1999 The population and evolutionary genetics of codon bias, pp. 82-101 in Evolutionary Genetics: From Molecules to Morphology, edited by R. S. SINGH and C. B. KRIMBAS. Cambridge University Press, New York.
51. LI, L., C. J. STOECKERT, JR. and D. S. ROOS, 2003 OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13: 2178-2189.
52. LI, W. H., 1987 Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. J. Mol. Evol. 24: 337-345.
53. LINTS, R., and S. W. EMMONS, 2002 Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family. Genes Dev. 16: 2390-2402.
54. LIPTON, J., G. KLEEMANN, R. GHOSH, R. LINTS and S. W. EMMONS, 2004 Mate searching in Caenorhabditis elegans: a genetic model for sex drive in a simple invertebrate. J. Neurosci. 24: 7427-7434.
55. LOEWE, L., and B. CHARLESWORTH, 2006 Inferring the distribution of mutational effects on fitness in Drosophila. Biol. Lett. 2: 426-430.
56. LOEWE, L., and B. CHARLESWORTH, 2007 Background selection in single genes may explain patterns of codon bias. Genetics 175: 1381-1393.
57. LOEWE, L., B. CHARLESWORTH, C. BARTOLOME and V. NOEL, 2006 Estimating selection on nonsynonymous mutations. Genetics 172: 1079-1092.
58. LYNCH, M., and J. S. CONERY, 2003 The origins of genome complexity. Science 302: 1401-1404.
59. LYNCH, M., and W. GABRIEL, 1990 Mutation load and the survival of small populations. Evolution 44: 1725-1737.
60. MARAIS, G., B. CHARLESWORTH and S. I. WRIGHT, 2004a Recombination and base composition: the case of the highly self-fertilizing plant Arabidopsis thaliana. Genome Biol. 5: R45.
61. MARAIS, G., T. DOMAZET-LOSO, D. TAUTZ and B. CHARLESWORTH, 2004b Correlated evolution of synonymous and nonsynonymous sites in Drosophila. J. Mol. Evol. 59: 771-779.
62. MAYNARD SMITH, J., and J. HAIGH, 1974 Hitch-hiking effect of a favorable gene. Genet. Res. 23: 23-35.
63. MIRA, A., H. OCHMAN and N. A. MORAN, 2001 Deletional bias and the evolution of bacterial genomes. Trends Genet. 17: 589-596.
64. MORGAN, M. T., 2001 Transposable element number in mixed mating populations. Genet. Res. 77: 261-275.
65. NORDBORG, M., 2000 Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154: 923-929.
66. NUZHDIN, S. V., 1999 Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica 107: 129-137.
67. PANNELL, J. R., 2003 Coalescence in a metapopulation with recurrent local extinction and recolonization. Evolution 57: 949-961.
68. PANNELL, J. R., and B. CHARLESWORTH, 1999 Neutral genetic diversity in a metapopulation with recurrent local extinction and recolonization. Evolution 53: 664-676.
69. PARKINSON, J., A. ANTHONY, J. WASMUTH, R. SCHMID, A. HEDLEY et al., 2004a PartiGene - constructing partial genomes. Bioinformatics 20: 1398-1404.
70. PARKINSON, J., C. WHITTON, R. SCHMID, M. THOMSON and M. BLAXTER, 2004b NEMBASE: a resource for parasitic nematode ESTs. Nucleic Acids Res. 32: D427-D430.
71. PETROV, D. A., Y. T. AMINETZACH, J. C. DAVIS, D. BENSASSON and A. E. HIRSH, 2003 Size matters: non-LTR retrotransposable elements and ectopic recombination in Drosophila. Mol. Biol. Evol. 20: 880-892.
72. PIGANEAU, G., and A. EYRE-WALKER, 2003 Estimating the distribution of fitness effects from DNA sequence data: implications for the molecular clock. Proc. Natl. Acad. Sci. USA 100: 10335-10340.
73. POLLAK, E., 1987 On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics 117: 353-360.
74. POPADIN, K., L. V. POLISHCHUK, L. MAMIROVA, D. KNORRE and K. GUNBIN, 2007 Accumulation of slightly deleterious mutations in mitochondrial protein-coding genes of large versus small mammals. Proc. Natl. Acad. Sci. USA 104: 13390-13395.
75. REINKE, V., I. S. GIL, S. WARD and K. KAZMER, 2004 Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131: 311-323.
76. SHARP, P. M., and W. H. LI, 1987 The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol. Biol. Evol. 4: 222-230.
77. SHIMIZU, K. K., J. M. CORK, A. L. CAICEDO, C. A. MAYS, R. C. MOORE et al., 2004 Darwinian selection on a selfing locus. Science 306: 2081-2084.
78. SIJEN, T., and R. H. PLASTERK, 2003 Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 426: 310-314.
79. SIVASUNDAR, A., and J. HEY, 2003 Population genetics of Caenorhabditis elegans: the paradox of low polymorphism in a widespread species. Genetics 163: 147-157.
80. STEIN, L. D., Z. BAO, D. BLASIAR, T. BLUMENTHAL, M. R. BRENT et al., 2003 The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol. 1: 166-192.
81. STENICO, M., A. T. LLOYD and P. M. SHARP, 1994 Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases. Nucleic Acids Res. 22: 2437-2446.
82. STEWART, M. R., N. L. CLARK, G. MERRIHEW, E. M. GALLOWAY and J. H. THOMAS, 2005 High genetic diversity in the chemoreceptor superfamily of Caenorhabditis elegans. Genetics 169: 1985-1996.
83. SUEOKA, N., 1962 On the genetic basis of variation and heterogeneity of DNA base composition. Proc. Natl. Acad. Sci. USA 48: 582-592.
84. SUPEK, F., and K. VLAHOVICEK, 2004 INCA: synonymous codon usage analysis and clustering by means of self-organizing map. Bioinformatics 20: 2329-2330.
85. TANG, C., C. TOOMAJIAN, S. SHERMAN- BROYLES, V. PLAGNOL, Y. L. GUO et al., 2007 The evolution of selfing in Arabidopsis thaliana. Science 317: 1070-1072.
86. TEOTONIO, H., D. MANOEL and P. C. PHILLIPS, 2006 Genetic variation for outcrossing among Caenorhabditis elegans isolates. Evolution 60: 1300-1305.
87. THOMAS, J. H., J. L. KELLEY, H. M. ROBERTSON, K. LY and W. J. SWANSON, 2005 Adaptive evolution in the SRZ chemoreceptor families of Caenorhabditis elegans and Caenorhabditis briggsae. Proc. Natl. Acad. Sci. USA 102: 4476-4481.
88. THOMPSON, J. D., D. G. HIGGINS and T. J. GIBSON, 1994 Clustal-W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
89. WASMUTH, J., and M. BLAXTER, 2004 prot4EST: translating expressed sequence tags from neglected genomes. BMC Bioinformatics 5: 187.
90. WRIGHT, F., 1990 The effective number of codons used in a gene. Gene 87: 23-29.
91. WRIGHT, S. I., B. LAUGA and D. CHARLESWORTH, 2002 Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol. Biol. Evol. 19: 1407-1420.
92. WRIGHT, S. I., B. LAUGA and D. CHARLESWORTH, 2003 Subdivision and haplotype structure in natural populations of Arabidopsis lyrata. Mol. Ecol. 12: 1247-1263.
93. YANG, Z. H., 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13: 555-556.
94. YANG, Z., N. GOLDMAN and A. FRIDAY, 1994 Comparison of models for nucleotide substitution used in maximum-likelihood phylogenetic estimation. Mol. Biol. Evol. 11: 316-324.