SNP Detection from De Novo Transcriptome Sequencing in the Bivalve Macoma balthica: Marker Development for Evolutionary Studies

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Pante, Eric ^a   Rohfritsch, Audrey ^a   Becquet, Vanessa ^a   Belkhir, Khalid ^b   Bierne, Nicolas ^c   Garcia, Pascale ^a  

^a UNIVERSITÉ DE LA ROCHELLE   (France)

^b INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^c MONTPELLIER BUSINESS SCHOOL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CONTIG; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; TRANSCRIPTOME;

ARTICLE; BIVALVE; CELL NUCLEUS; CELL RESPIRATION; CLIMATE CHANGE; ENERGY METABOLISM; EVOLUTIONARY ADAPTATION; GENETIC MARKER; GENETIC VARIABILITY; HYBRID ZONE; MACOMA BALTHICA; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; POPULATION DIFFERENTIATION; POPULATION GENETICS; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIVALVIA; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENETIC LOCI; GENETIC MARKERS; LINKAGE DISEQUILIBRIUM; MOLECULAR SEQUENCE ANNOTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC;

BIVALVIA; MACOMA BALTHICA;

EID: 84871572679     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052302     Document Type: Article

References (103)

1. Bell G, Collins S, (2008) Adaptation, extinction and global change. Evolutionary Applications 1: 3-16.
2. Parmesan C, Galbraith H (2004) Observed ecological impacts of climate change in North America. Technical report, Pew Center on Global Climate Change, Arlington, VA.
3. Parmesan C, Yohe G, (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37-42.
4. Helmuth B, Mieszkowska N, Moore P, Hawkins SJ, (2006) Living on the edge of two changing worlds: Forecasting the responses of rocky intertidal ecosystems to climate change. Annual Review of Ecology Evolution and Systematics 37: 373-404.
5. Mallet J, (2005) Hybridization as an invasion of the genome. Trends in Ecology & Evolution 20: 229-237.
6. Hilbish TJ, Lima FP, Brannock PM, Fly EK, Rognstad RL, et al. (2012) Change and stasis in marine hybrid zones in response to climate warming. Journal of Biogeography 39: 676-687.
7. Hilbish TJ, Brannock PM, Jones KR, Smith AB, Bullock BN, et al. (2010) Historical changes in the distributions of invasive and endemic marine invertebrates are contrary to global warming predictions: the effects of decadal climate oscillations. Journal of Biogeography 37: 423-431.
8. Barton N, (1979) The dynamics of hybrid zone. Heredity 43: 341-359.
9. Jansen JM, Pronker AE, Bonga SW, Hummel H, (2007) Macoma balthica in Spain, a few decades back in climate history. Journal of Experimental Marine Biology and Ecology 344: 161-169.
10. Hummel H, Bogaards R, Bachelet G, Caron F, Sol J, et al. (2000) The respiratory performance and survival of the bivalve Macoma balthica (L.) at the southern limit of its distribution area: a translocation experiment. Journal of Experimental Marine Biology and Ecology 251: 85-102.
11. Goikoetxea N, Borja A, Fontán A, González M, Valencia V, (2009) Trends and anomalies in sea-surface temperature, observed over the last 60 years, within the southeastern Bay of Biscay. Continental Shelf Research 29: 1060-1069.
12. Edjung G, Bonsdorff E, (1992) Predation on the bivalve Macoma balthica by the isopod Saduria entomon: laboratory and field experiments. Marine Ecology Progress Series 88: 207-214.
13. Piersma T, Beukema J, (1993) Tropic interactions between shorebirds and their invertebrate prey. Netherlands Journal of Sea Research 31: 299-512.
14. Mattila J, Bonsdorff E, (1998) Predation by juvenile flounder (Platichthys flesus L.): a test of prey vulnerability, predator preference, switching behaviour and functional response. Journal of Experimental Marine Biology and Ecology 227: 221-236.
15. Philippart C, Van Aken H, Beukema J, Bos O, Cadee G, et al. (2003) Climate-related changes in recruitment of the bivalve Macoma balthica. Limnology and Oceanography 48: 2171-2185.
16. Becquet V, Simon-Bouhet B, Pante E, Hummel H, Garcia P, (2012) Glacial refugium versus range limit: conservation genetics of Macoma balthica, a key species in the Bay of Biscay (France). Journal of Experimental Marine Biology and Ecology 432-433: 73-82.
17. Jolly MT, Viard F, Gentil F, Thiébaut E, Jollivet D, (2006) Comparative phylogeography of two coastal polychaete tubeworms in the Northeast Atlantic supports shared history and vicariant events. Molecular Ecology 15: 1841-1855.
18. Jolly MT, Jollivet D, Gentil F, Thiébaut E, Viard F, (2005) Sharp genetic break between Atlantic and English Channel populations of the polychaete Pectinaria koreni, along the North coast of France. Heredity 94: 23-32.
19. Gilad Y, Pritchard JK, Thornton K, (2009) Characterizing natural variation using next-generation sequencing technologies. Trends in Genetics 25: 463-471.
20. Wolf JBW, Lindell J, Backström N, (2010) Speciation genetics: current status and evolving approaches. Philosophical transactions of the Royal Society of London Series B, Biological sciences 365: 1717-1733.
21. Ekblom R, Galindo J, (2011) Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity 107: 1-15.
22. Barbazuk W, Emrich S, Chen H, Li L, Schnable P, (2007) SNP discovery via 454 transcriptome sequencing. The Plant Journal 51: 910-918.
23. Vera JC, Wheat CW, Fescemyer HW, Frilander MJ, Crawford DL, et al. (2008) Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Molecular Ecology 17: 1636-1647.
24. Meyer E, Aglyamova GV, Wang S, Buchanan-Carter J, Abrego D, et al. (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. BMC Genomics 10: 219.
25. Cahais V, Gayral P, Tsagkogeorga G, Melo-Ferreira J, Ballenghien M, et al. (2012) Reference-free transcriptome assembly in non-model animals from next-generation sequencing data. Molecular Ecology Resources 12: 834-845.
26. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-80.
27. Luttikhuizen PC, Drent J, van Delden W, Piersma T, (2003) Spatially structured genetic variation in a broadcast spawning bivalve: quantitative vs. molecular traits. Journal of Evolutionary Biology 16: 260-272.
28. Luttikhuizen PC, Drent J, Baker AJ, (2003) Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal. Molecular Ecology 12: 2215-2229.
29. Nikula R, Strelkov P, Väinölä R, (2007) Diversity and trans-arctic invasion history of mitochondrial lineages in the North Atlantic Macoma balthica complex (Bivalvia: Tellinidae). Evolution 61: 928-941.
30. Excoffier L, Hofer T, Foll M, (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103: 285-298.
31. Bultelle F, Panchout M, Leboulenger F, Danger JM, (2002) Identification of differentially expressed genes in Dreissena polymorpha exposed to contaminants. Marine Environmental Research 54: 385-389.
32. Boutet I, Tanguy A, Moraga D, (2004) Response of the Pacific oyster Crassostrea gigas to hydrocarbon contamination under experimental conditions. Gene 329: 147-157.
33. Huvet A, Herpin A, Dégremont L, Labreuche Y, Samain JF, et al. (2004) The identification of genes from the oyster Crassostrea gigas that are differentially expressed in progeny exhibiting opposed susceptibility to summer mortality. Gene 343: 211-220.
34. Putnam NH, Butts T, Ferrier DEK, Furlong RF, Hellsten U, et al. (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453: 1064-1071.
35. Khachane AN, Harrison PM, (2009) Assessing the genomic evidence for conserved transcribed pseudogenes under selection. BMC Genomics 10: 435.
36. Gagliardi D, Stepien PP, Temperley RJ, Lightowlers RN, Chrzanowska-Lightowlers ZMA, (2004) Messenger RNA stability in mitochondria: different means to an end. Trends in Genetics 20: 260-267.
37. Mohanty BK, Kushner SR, (2011) Bacterial/archaeal/organellar polyadenylation. Wiley Interdisciplinary Reviews: RNA 2: 256-276.
38. Butow RA, Zhu H, Perlman P, Conrad-Webb H, (1989) The role of a conserved dodecamer sequence in yeast mitochondrial gene expression. Genome 31: 757-760.
39. Gagliardi D, Leaver CJ, (1999) Polyadenylation accelerates the degradation of the mitochondrial mRNA associated with cytoplasmic male sterility in sunflower. The EMBO journal 18: 3757-3766.
40. Bensasson D, Zang DX, Hartl DL, Hewitt GM, (2001) Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology & Evolution 16: 314-321.
41. Boore JL, (2006) The complete sequence of the mitochondrial genome of Nautilus macromphalus (Mollusca: Cephalopoda). BMC Genomics 7: 182.
42. DeJong RJ, Emery AM, Adema CM, (2004) The mitochondrial genome of Biomphalaria glabrata (Gastropoda: Basommatophora), intermediate host of Schistosoma mansoni. The Journal of Parasitology 90: 991-997.
43. Faure E, Delaye L, Tribolo S, Levasseur A, Seligmann H, et al. (2011) Probable presence of an ubiquitous cryptic mitochondrial gene on the antisense strand of the cytochrome oxidase I gene. Biology Direct 6: 56.
44. Galindo J, Grahame JW, Butlin RK, (2010) An EST-based genome scan using 454 sequencing in the marine snail Littorina saxatilis- Corrigendum. Journal of Evolutionary Biology 23: 2768-2769.
45. Galindo J, Grahame JW, Butlin RK, (2010) An EST-based genome scan using 454 sequencing in the marine snail Littorina saxatilis. Journal of Evolutionary Biology 23: 2004-2016.
46. Futschik A, Schlötterer C, (2010) The next generation of molecular markers from massively parallel sequencing of pooled DNA samples. Genetics 186: 207-218.
47. Kolaczkowski B, Kern AD, Holloway AK, Begun DJ, (2011) Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster. Genetics 187: 245-260.
48. Sauvage C, Bierne N, Lapegue S, Boudry P, (2007) Single Nucleotide polymorphisms and their relationship to codon usage bias in the Pacific oyster Crassostrea gigas. Gene 406: 13-22.
49. Cutter AD, Baird SE, Charlesworth D, (2006) High nucleotide polymorphism and rapid decay of linkage disequilibrium in wild populations of Caenorhabditis remanei. Genetics 174: 901-913.
50. Small K, Brudno M, Hill M, Sidow A, (2007) Extreme genomic variation in a natural population. Proceedings of the National Academy of Sciences of the United States of America 104: 5698-5703.
51. Shapiro JA, Huang W, Zhang C, Hubisz MJ, Lu J, et al. (2007) Adaptive genic evolution in the Drosophila genomes. Proceedings of the National Academy of Sciences of the United States of America 104: 2271-2276.
52. Dégremont L, Ernande B, Bedier E, Boudry P, (2007) Summer mortality of hatchery-produced Pacific oyster spat (Crassostrea gigas). I. estimation of genetic parameters for survival and growth. Aquaculture 262: 41-53.
53. Bazin E, Glemin S, Galtier N, (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312: 570-572.
54. Nosil P, Funk DJ, Ortiz-Barrientos D, (2009) Divergent selection and heterogeneous genomic divergence. Molecular Ecology 18: 375-402.
55. Beaumont M, Nichols R, (1996) Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society B-Biological Sciences 263: 1619-1626.
56. Gompert Z, Buerkle CA, (2009) A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Molecular Ecology 18: 1207-1224.
57. Luttikhuizen PC, Drent J, Peijnenburg KTCA, Van der Veer HW, Johannesson K, (2012) Genetic architecture in a marine hybrid zone: comparing outlier detection and genomic clines analysis in the bivalve Macoma balthica. Molecular Ecology 21: 30-48-3061.
58. Harr B, (2006) Genomic islands of differentiation between house mouse subspecies. Genome Research 16: 730-737.
59. Freamo H, O'Reilly P, Berg PR, Lien S, Boulding EG, (2011) Outlier SNPs show more genetic structure between two Bay of Fundy metapopulations of Atlantic salmon than do neutral SNPs. Molecular Ecology Resources 11Suppl 1: 254-267.
60. Orsini L, Jansen M, Souche EL, Geldof S, De Meester L, (2011) Single nucleotide polymorphism discovery from expressed sequence tags in the waterflea Daphnia magna. BMC Genomics 12: 309.
61. Bierne N, Welch J, Loire E, Bonhomme F, David P, (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology 20: 2044-2072.
62. Turner TL, Bourne EC, Von Wettberg EJ, Hu TT, Nuzhdin SV, (2010) Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nature Genetics 42: 260-263.
63. Ellison CK, Burton RS, (2006) Disruption of mitochondrial function in interpopulation hybrids of Tigriopus californicus. Evolution 60: 1382-1391.
64. Asmussen MA, Arnold J, Avise JC, (1987) Definition and properties of disequilibrium statistics for associations between nuclear and cytoplasmic genotypes. Genetics 115: 755-768.
65. Arnorld M, (1993) Cytonuclear disequilibria in hybrid zones. Annual Review of Ecology and Systematics 24: 521-554.
66. Breewer J, Werren J, (1995) Hybrid breakdown between two haplodiploid species: The role of nuclear and cytoplasmic genes. Evolution 49: 705-717.
67. Burton RS, Ellison CK, Harrison JS, (2006) The sorry state of F2 hybrids: consequences of rapid mitochondrial DNA evolution in allopatric populations. American Naturalist 168Suppl 6: S14-24.
68. Oliveira DCSG, Raychoudhury R, Lavrov DV, Werren JH, (2008) Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Molecular Biology and Evolution 25: 2167-2180.
69. Gagnaire PA, Normandeau E, Bernatchez L, (2012) Comparative genomics reveals adaptive protein evolution and a possible cytonuclear incompatibility between European and American eels. Molecular Biology and Evolution 29: 2909-2919.
70. Burton RS, Barreto FS, (2012) A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Molecular Ecology 21: 4942-57.
71. Väinölä R, (2003) Repeated trans-Arctic invasions in littoral bivalves: molecular zoogeography of the Macoma balthica complex. Marine Biology 143: 935-946.
72. Nikula R, Strelkov P, Väinölä R, (2008) A broad transition zone between an inner Baltic hybrid swarm and a pure North Sea subspecies of Macoma balthica (Mollusca, Bivalvia). Molecular Ecology 17: 1505-1522.
73. Strelkov P, Nikula R, Väinölä R, (2007) Macoma balthica in the White and Barents Seas: properties of a widespread marine hybrid swarm (Mollusca: Bivalvia). Molecular Ecology 16: 4110-4127.
74. Latta RG, Linhart YB, Mitton JB, (2001) Cytonuclear disequilibrium and genetic drift in a natural population of Ponderosa pine. Genetics 158: 843-850.
75. Riginos C, Cunningham CW, (2007) Hybridization in postglacial marine habitats. Molecular Ecology 16: 3971-3972.
76. Becquet V, Lanneluc I, Simon-Bouhet B, Garcia P, (2009) Microsatellite markers for the Baltic clam, Macoma balthica (Linné, 1758), a key species concerned by changing southern limit, in exploited littoral ecosystems. Conservation Genetics Resources 1: 265-267.
77. Väinölä R, Varvio SL (1989) Biosystematics of Macoma balthica in northwestern Europe. In: Ryland J, Tyler P, editors, Reproduction, genetics and distributions of marine organisms. Fredensborg: Olsen and Olsen, 23rd Eur Mar Biol Symp, 309-316.
78. Beaumont MA, (2005) Adaptation and speciation: what can F(st) tell us? Trends in Ecology & Evolution 20: 435-440.
79. Van Tassell C, Smith T, Matukumalli L, Taylor J, Schnabel R, et al. (2008) SNP discovery and allele frequency estimation by deep sequencing of reduced representation libraries. Nature Methods 5: 247-252.
80. Pérez-Enciso M, Ferretti L, (2010) Massive parallel sequencing in animal genetics: wherefroms and wheretos. Animal Genetics 41: 561-569.
81. SeqClean (2012) DFCI Gene Indices Software Tools. URL http://compbio.dfci.harvard.edu/tgi/software/.
82. NCBI (2012) Sequence Read Archive (SRA). Available: http://www.ncbi.nlm.nih.gov/sra. Accessed 25 Nov 2012.
83. Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Müller WEG, et al. (2004) Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Research 14: 1147-1159.
84. Li W, Godzik A, (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
85. Götz S, Arnold R, Sebastián-León P, Martn-Rodríguez S, Tischler P, et al. (2011) B2G-FAR, a species-centered GO annotation repository. Bioinformatics 27: 919-924.
86. Götz S, Garciá-Gómez JM, Terol J, Williams TD, Nagaraj SH, et al. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Research 36: 3420-3435.
87. Conesa A, Götz S (2008) Blast2go: A comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics Article ID 619832: 12 pages.
88. Conesa A, Götz S, Garca-Gómez JM, Terol J, Talón M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
89. Tatusov T, Tatusov R (2012) ORF Finder (Open Reading Frame Finder). Available: http://www.ncbi.nlm.nih.gov/projects/gorf/. Accessed 25 Nov 2012.
90. Stapley J, Reger J, Feulner PGD, Smadja C, Galindo J, et al. (2010) Adaptation genomics: the next generation. Trends in Ecology & Evolution 25: 705-712.
91. Ponstingl H (2012) Smalt. Available: http://www.sanger.ac.uk/resources/software/smalt/. Accessed 25 Nov 2012.
92. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, et al. (2005) Galaxy: a platform for interactive large-scale genome analysis. Genome Research 15: 1451-1455.
93. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, et al. (2010) Galaxy: a web-based genome analysis tool for experimentalists. In: Current Protocols in Molecular Biology. 1-21.
94. Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, et al. (2010) Manipulation of FASTQ data with Galaxy. Bioinformatics 26: 1783-1785.
95. Goecks J, Nekrutenko A, Taylor J, (2010) Galaxy Team (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11: R86.
96. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The sequence alignment/map format and samtools. Bioinformatics 25: 2078-2079.
97. Kofler R, Orozco-terWengel P, De Maio N, Pandey RV, Nolte V, et al. (2011) PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS ONE 6: e15925.
98. R Development Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available: http://www.R-project.org. Accessed 25 Nov 2012. ISBN 3-900051-07-0.
99. Paradis E, Claude J, Strimmer K, (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290.
100. Charif D, Lobry J (2007) SeqinR 1.0-2: a contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. In: U Bastolla HR M Porto, Vendruscolo M, editors, Structural approaches to sequence evolution: Molecules, networks, populations, New York: Springer Verlag, Biological and Medical Physics, Biomedical Engineering. 207-232.
101. Foll M, Gaggiotti O, (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a bayesian perspective. Genetics 180: 977-993.
102. Narum SR, Hess JE, (2011) Comparison of F(ST) outlier tests for SNP loci under selection. Molecular Ecology Resources 11Suppl 1: 184-194.
103. Jeffreys H (1961) The Theory of Probability. Oxford, 3rd edition, 432 pp.