Full-genome evolutionary histories of selfing, splitting, and selection in Caenorhabditis

Genome Research

Volumn 125, Issue 5, 2015, Pages 667-678

  Thomas, Cristel G ^a   Wang, Wei ^a   Jovelin, Richard ^a   Ghosh, Rajarshi ^b,c   Lomasko, Tatiana ^d   Trinh, Quang ^d   Kruglyak, Leonid ^b,e,f   Stein, Lincoln D ^d,g,h   Cutter, Asher D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b PRINCETON UNIVERSITY   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF TORONTO   (Canada)

^h Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CAENORHABDITIS; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; GENE FLOW; GENE SEQUENCE; GENETIC LINKAGE; GENETIC POLYMORPHISM; HAPLOTYPE; INBREEDING; MICROBIAL GENOME; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; SELF FERTILIZATION; ANIMAL; CAENORHABDITIS ELEGANS; GENETIC SELECTION; GENETICS; GENOME; MOLECULAR EVOLUTION; MUTATION; PHYSIOLOGY; SPECIES DIFFERENTIATION;

CAENORHABDITIS; CAENORHABDITIS BRIGGSAE; CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; EVOLUTION, MOLECULAR; GENETIC SPECIATION; GENOME, HELMINTH; INBREEDING; MUTATION; SELECTION, GENETIC; SELF-FERTILIZATION;

EID: 84929658226     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.187237.114     Document Type: Article

References (104)

1. The 1000 Genomes Project Consortium. 2012. An integrated map of genetic variation from 1,092 human genomes. Nature 491: 56-65.
2. Alexander DH, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19: 1655-1664.
3. Andersen EC, Gerke JP, Shapiro JA, Crissman JR, Ghosh R, Bloom JS, Félix MA, Kruglyak L. 2012. Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity. Nat Genet 44: 285-290.
4. Baird SE, Stonesifer R. 2012. Reproductive isolation in Caenorhabditis briggsae: dysgenic interactions between maternal-and zygotic-effect loci result in a delayed development phenotype. Worm 1: 189-195.
5. Baird S, Davidson C, Bohrer J. 2005. The genetics of ray pattern variation in Caenorhabditis briggsae. BMC Evol Biol 5: 3.
6. Barrière A, Félix M-A. 2005. High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr Biol 15: 1176-1184.
7. Begun DJ, Holloway AK, Stevens K, Hillier LW,Poh YP, HahnMW, Nista PM, Jones CD, Kern AD, Dewey CN, et al. 2007. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5: e310.
8. Brandvain Y, Slotte T, Hazzouri KM, Wright SI, Coop G. 2013. Genomic identification of founding haplotypes reveals the history of the selfing species Capsella rubella. PLoS Genet 9: e1003754.
9. Brandvain Y, Kenney AM, Flagel L, Coop G, Sweigart AL. 2014. Speciation and introgression between Mimulus nasutus and Mimulus guttatus. PLoS Genet 10: e1004410.
10. Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, Fitz J, Koenig D, Lanz C, Stegle O, Lippert C, et al. 2011. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43: 956-963.
11. Charlesworth B. 1998. Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol 15: 538-543.
12. Charlesworth B, Morgan MT, Charlesworth D. 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289-1303.
13. Charlesworth B, Nordborg M, Charlesworth D. 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.
14. Chen K, Wallis JW, McLellan MD, Larson DE, Kalicki JM, Pohl CS, McGrath SD, Wendl MC, Zhang Q, Locke DP, et al. 2009. BreakDancer: an algorithm for high-resolution mapping of genomic structural variation. Nat Methods 6: 677-681.
15. Chen X, Shen Y, Ellis RE. 2014. Dependence of the sperm/oocyte decision on the nucleosome remodeling factor complex was acquired during recent Caenorhabditis briggsae evolution. Mol Biol Evol 31: 2573-2585.
16. Comeron JM. 2014. Background selection as baseline for nucleotide variation across the Drosophila genome. PLoS Genet 10: e1004434.
17. Cruickshank TE, HahnMW. 2014. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol 23: 3133-3157.
18. Cutter AD. 2006. Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans. Genetics 172: 171-184.
19. Cutter AD. 2013. Integrating phylogenetics, phylogeography and population genetics through genomes and evolutionary theory. Mol Phylogenet Evol 69: 1172-1185.
20. Cutter AD, Choi JY. 2010. Natural selection shapes nucleotide polymorphism across the genome of the nematode Caenorhabditis briggsae. Genome Res 20: 1103-1111.
21. Cutter AD, Payseur BA. 2003. Selection at linked sites in the partial selfer Caenorhabditis elegans. Mol Biol Evol 20: 665-673.
22. Cutter AD, Payseur BA. 2013. Genomic signatures of selection at linked sites: unifying the disparity among species. Nat Rev Genet 14: 262-274.
23. Cutter AD, Félix MA, Barrière A, Charlesworth D. 2006. Patterns of nucleotide polymorphism distinguish temperate and tropical wild isolates of Caenorhabditis briggsae. Genetics 173: 2021-2031.
24. Cutter AD, Dey A, Murray RL. 2009. Evolution of the Caenorhabditis elegans genome. Mol Biol Evol 26: 1199-1234.
25. Cutter AD, Yan W, Tsvetkov N, Sunil S, Félix MA. 2010. Molecular population genetics and phenotypic sensitivity to ethanol for a globally diverse sample of the nematode Caenorhabditis briggsae. Mol Ecol 19: 798-809.
26. Cutter AD, Jovelin R, Dey A. 2013. Molecular hyperdiversity and evolution in very large populations. Mol Ecol 22: 2074-2095.
27. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, et al. 2011. The variant call format and VCFtools. Bioinformatics 27: 2156-2158.
28. Delattre M, Félix MA. 2001. Polymorphism and evolution of vulval precursor cell lineages within two nematode genera, Caenorhabditis and Oscheius. Curr Biol 11: 631-643.
29. Denver DR, Dolan PC, Wilhelm LJ, Sung W, Lucas-Lledo JI, Howe DK, Lewis SC, Okamoto K, Thomas WK, Lynch M, et al. 2009. A genome-wide view of Caenorhabditis elegans base-substitution mutation processes. Proc Natl Acad Sci 106: 16310-16324.
30. Denver DR, Wilhelm LJ, Howe DK, Gafner K, Dolan PC, Baer CF. 2012. Variation in base-substitution mutation in experimental and natural lineages of Caenorhabditis nematodes. Genome Biol Evol 4: 513-522.
31. Dey A, Chan CKW, Thomas CG, Cutter AD. 2013. Nucleotide hyperdiversity defines populations of Caenorhabditis brenneri. Proc Natl Acad Sci 110: 11056-11060.
32. Dolgin ES, Félix MA, Cutter AD. 2008. Hakuna nematoda: genetic and phenotypic diversity in African isolates of Caenorhabditis elegans and C. briggsae. Heredity 100: 304-315.
33. Ellis RE, Lin SY. 2014. The evolutionary origins and consequences of selffertility in nematodes. F1000Prime Rep 6: 62.
34. Elyashiv E, Sattath S, Hu TT, Strustovsky A, McVicker G, Andolfatto P, Sella G. 2014. A genomic map of the effects of linked selection in Drosophila. arXiv: 1408.5461.
35. Fay JC, Wu CI. 2000. Hitchhiking under positive Darwinian selection. Genetics 155: 1405-1413.
36. Félix MA, Jovelin R, Ferrari C, Han S, Cho YR, Andersen EC, Cutter AD, Braendle C. 2013. Species richness, distribution and genetic diversity of Caenorhabditis nematodes in a remote tropical rainforest. BMC Evol Biol 13: 10.
37. Félix MA, Braendle C, Cutter AD. 2014. A streamlined system for species diagnosis in Caenorhabditis (Nematoda: Rhabditidae) with name designations for 15 distinct biological species. PLoS One 9: e94723.
38. Foxe JP, Slotte T, Stahl EA, Neuffer B, Hurka H, Wright SI. 2009. Recent speciation associated with the evolution of selfing in Capsella. Proc Natl Acad Sci 106: 5241-5245.
39. Frøkjaer-Jensen C. 2013. Exciting prospects for precise engineering of Caenorhabditis elegans genomes with CRISPR/Cas9. Genetics 195: 635-642.
40. Geraldes A, Basset P, Smith KL, NachmanMW. 2011. Higher differentiation among subspecies of the house mouse (Mus musculus) in genomic regions with low recombination. Mol Ecol 20: 4722-4736.
41. Gillespie JH, Langley CH. 1979. Are evolutionary rates really variable? J Mol Evol 13: 27-34.
42. Guo Y, Lang S, Ellis RE. 2009. Independent recruitment of F box genes to regulate hermaphrodite development during nematode evolution. Curr Biol 19: 1853-1860.
43. Haag ES, Liu QW. 2013. Using Caenorhabditis to explore the evolution of the germ line. In Germ cell development in C. elegans (ed. Schedl T), pp. 405-425. Springer Science, NY.
44. Hellmann I, Ebersberger I, Ptak SE, Pääbo S, Przeworski M. 2003. A neutral explanation for the correlation of diversity with recombination rates in humans. Am J Hum Genet 72: 1527-1535.
45. Hershberg R, Petrov DA. 2008. Selection on codon bias. Annu Rev Genet 42: 287-299.
46. Hill RC, Egydio de Carvalho C, Salogiannis J, Schlager B, Pilgrim D, Haag ES. 2006. Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. Dev Cell 10: 531-538.
47. Hillier LW, Miller RD, Baird SE, Chinwalla A, Fulton LA, Koboldt DC, Waterston RH. 2007. Comparison of C. elegans and C. briggsae genome sequences reveals extensive conservation of chromosome organization and synteny. PLoS Biol 5: e167.
48. Hoehn K, McGaugh S, Noor MF. 2012. Effects of premature termination codon polymorphisms in the Drosophila pseudoobscura subclade. J Mol Evol 75: 141-150.
49. Hudson RR, Slatkin M, Maddison WP. 1992. Estimation of levels of gene flow from DNA-sequence data. Genetics 132: 583-589.
50. Hufford MB, Xu X, van Heerwaarden J, Pyhäjärvi T, Chia JM, Cartwright RA, Elshire RJ, Glaubitz JC, Guill KE, Kaeppler SM, et al. 2012. Comparative population genomics of maize domestication and improvement. Nat Genet 44: 808-811.
51. Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
52. Jukes TH, Cantor CR. 1969. Evolution of protein molecules. In Mammalian protein metabolism (ed. Munro HN), pp. 21-132. Academic Press, New York.
53. Kaiser VB, Charlesworth B. 2009. The effects of deleterious mutations on evolution in nonrecombining genomes. Trends Genet 25: 9-12.
54. Keinan A, Reich D. 2010. Human population differentiation is strongly correlated with local recombination rate. PLoS Genet 6: e1000886.
55. Kiontke K, Félix MA, Ailion M, Rockman M, Braendle C, Penigault JB, Fitch D. 2011. A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evol Biol 11: 339.
56. Koboldt DC, Staisch J, Thillainathan B, Haines K, Baird SE, Chamberlin HM, Haag ES, Miller RD, Gupta BP. 2010. A toolkit for rapid gene mapping in the nematode Caenorhabditis briggsae. BMC Genomics 11: 236.
57. Kozlowska JL, Ahmad AR, Jahesh E, Cutter AD. 2012. Genetic variation for post-zygotic reproductive isolation between Caenorhabditis briggsae and Caenorhabditis sp. 9. Evolution 66: 1180-1195.
58. Kumar S, Koutsovoulos G, Kaur G, Blaxter M. 2012. Toward 959 nematode genomes. Worm 1: 42-50.
59. Langley CH, Stevens K, Cardeno C, Lee YCG, Schrider DR, Pool JE, Langley SA, Suarez C, Corbett-Detig RB, Kolaczkowski B, et al. 2012. Genomic variation in natural populations of Drosophila melanogaster. Genetics 192: 533-598.
60. Lawson DJ, Hellenthal G, Myers S, Falush D. 2012. Inference of population structure using dense haplotype data. PLoS Genet 8: e1002453.
61. Lee YCG, Reinhardt JA. 2012. Widespread polymorphism in the positions of stop codons in Drosophila melanogaster. Genome Biol Evol 4: 533-549.
62. Lercher MJ, Hurst LD. 2002. Human SNP variability and mutation rate are higher in regions of high recombination. Trends Genet 18: 337-340.
63. Levin M, Hashimshony T, Wagner F, Yanai I. 2012. Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev Cell 22: 1101-1108.
64. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
65. Li H, Durbin R. 2011. Inference of human population history from individual whole-genome sequences. Nature 475: 493-496.
66. Lunter G, Goodson M. 2011. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 21: 936-939.
67. Marri S, Gupta BP. 2009. Dissection of lin-11 enhancer regions in Caenorhabditis elegans and other nematodes. Dev Biol 325: 402-411.
68. Maynard Smith J, Haigh J. 1974. Hitch-hiking effect of a favorable gene. Genet Res 23: 23-35.
69. McVean G, Awadalla P, Fearnhead P. 2002. A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160: 1231-1241.
70. Nachman MW, Payseur BA. 2012. Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice. Philos Trans R Soc Lond B Biol Sci 367: 409-421.
71. Nei M, Li WH. 1979. Mathematical-model for studying genetic-variation in terms of restriction endonucleases. Proc Natl Acad Sci 76: 5269-5273.
72. Nielsen R. 2005. Molecular signatures of natural selection. Annu Rev Genet 39: 197-218.
73. Noor MAF, Bennett SM. 2009. Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 103: 439-444.
74. Pease JB, HahnMW. 2013. More accurate phylogenies inferred from low-recombination regions in the presence of incomplete lineage sorting. Evolution 67: 2376-2384.
75. Pickrell JK, Pritchard JK. 2012. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet 8: e1002967.
76. Plotkin JB, Kudla G. 2011. Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12: 32-42.
77. Prasad A, Croydon-Sugarman M, Murray RL, Cutter AD. 2011. Temperaturedependent fecundity associates with latitude in Caenorhabditis briggsae. Evolution 65: 52-63.
78. Raboin MJ, Timko AF, Howe DK, Félix MA, Denver DR. 2010. Evolution of Caenorhabditis mitochondrial genome pseudogenes and C. briggsae natural isolates. Mol Biol Evol 27: 1087-1096.
79. Reich D, Thangaraj K, Patterson N, Price AL, Singh L. 2009. Reconstructing Indian population history. Nature 461: 489-494.
80. Renaut S, Grassa CJ, Yeaman S, Moyers BT, Lai Z, Kane NC, Bowers JE, Burke JM, Rieseberg LH. 2013. Genomic islands of divergence are not affected by geography of speciation in sunflowers. Nat Commun 4: 1827.
81. Riche S, Zouak M, Argoul F, Arneodo A, Pecreaux J, Delattre M. 2013. Evolutionary comparisons reveal a positional switch for spindle pole oscillations in Caenorhabditis embryos. J Cell Biol 201: 653-662.
82. Rockman MV, Skrovanek SS, Kruglyak L. 2010. Selection at linked sites shapes heritable phenotypic variation in C. elegans. Science 330: 372-376.
83. Rödelsperger C, Neher RA, Weller AM, Eberhardt G, Witte H, Mayer WE, Dieterich C, Sommer RJ. 2014. Characterization of genetic diversity in the nematode Pristionchus pacificus from population-scale resequencing data. Genetics 196: 1153-1165.
84. Ross JA, Koboldt DC, Staisch JE, Chamberlin HM, Gupta BP, Miller RD, Baird SE, Haag ES. 2011. Caenorhabditis briggsae recombinant inbred line genotypes reveal inter-strain incompatibility and the evolution of recombination. PLoS Genet 7: e1002174.
85. Schaeffer SW. 2002. Molecular population genetics of sequence length diversity in the Adh region of Drosophila pseudoobscura. Genet Res 80: 163-175.
86. Sella G, Petrov DA, Przeworski M, Andolfatto P. 2009. Pervasive natural selection in the Drosophila genome? PLoS Genet 5: e1000495.
87. Sivasundar A, Hey J. 2003. Population genetics of Caenorhabditis elegans: the paradox of low polymorphism in a widespread species. Genetics 163: 147-157.
88. Stegeman GW, de Mesquita MB, Ryu WS, Cutter AD. 2013. Temperaturedependent behaviours are genetically variable in the nematode Caenorhabditis briggsae. J Exp Biol 216: 850-858.
89. Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, Chen N, Chinwalla A, Clarke L, Clee C, Coghlan A, et al. 2003. The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 1: 166-192.
90. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
91. Thomas CG, Li RH, Smith HE, Woodruff GC, Oliver B, Haag ES. 2012. Simplification and desexualization of gene expression in self-fertile nematodes. Curr Biol 22: 2167-2172.
92. Thompson O, Edgley M, Strasbourger P, Flibotte S, Ewing B, Adair R, Au V, Chaudry I, Fernando L, Hutter H, et al. 2013. The million mutation project: a new approach to genetics in Caenorhabditis elegans. Genome Res 23: 1749-1762.
93. Van der Auwera GA, Carneiro MO, Hartl C, Poplin R, del Angel G, Levy-Moonshine A, Jordan T, Shakir K, Roazen D, Thibault J, et al. 2013. From FastQ data to high-confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr Protoc Bioinformatics 43: 11.10.11-11.10.33.
94. Verster AJ, Ramani AK, McKay SJ, Fraser AG. 2014. Comparative RNAi screens in C. elegans and C. briggsae reveal the impact of developmental system drift on gene function. PLoS Genet 10: e1004077.
95. Wakeley J. 2009. Coalescent theory: an introduction. Roberts and Company Publishers, Greenwood Village
96. CO. Wang X, Chamberlin HM. 2004. Evolutionary innovation of the excretory system in Caenorhabditis elegans. Nat Genet 36: 231-232.
97. Weir BS, Hill WG. 1980. Effect of mating structure on variation in linkage disequilibrium. Genetics 95: 477-488.
98. Woodruff GC, Eke O, Baird SE, Félix MA, Haag ES. 2010. Insights into species divergence and the evolution of hermaphroditism from fertile interspecies hybrids of Caenorhabditis nematodes. Genetics 186: 997-1012.
99. Wright SI, Kalisz S, Slotte T. 2013. Evolutionary consequences of self-fertilization in plants. Proc Biol Sci 280: 20130133.
100. Yahara K, Furuta Y, Oshima K, Yoshida M, Azuma T, Hattori M, Uchiyama I, Kobayashi I. 2013. Chromosome painting in silico in a bacterial species reveals fine population structure. Mol Biol Evol 30: 1454-1464.
101. Yan C, Bi Y, Yin D, Zhao Z. 2012. A method for rapid and simultaneous mapping of genetic loci and introgression sizes in nematode species. PLoS One 7: e43770.
102. Ye K, Schulz MH, Long Q, Apweiler R, Ning Z. 2009. Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics 25: 2865-2871.
103. Zeng K, Fu YX, Shi S, Wu CI. 2006. Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174: 1431-1439.
104. Zhao Z, Boyle TJ, Bao Z, Murray JI, Mericle B, Waterston RH. 2008. Comparative analysis of embryonic cell lineage between Caenorhabditis briggsae and Caenorhabditis elegans. Dev Biol 314: 93-99.