Speciation in the deep sea: Multi-locus analysis of divergence and gene flow between two hybridizing species of hydrothermal vent mussels

PLoS ONE

Volumn 4, Issue 8, 2009, Pages

  Faure, Baptiste ^a,b,c,d   Jollivet, Didier ^a,b   Tanguy, Arnaud ^a,b   Bonhomme, François ^c,d   Bierne, Nicolas ^c,d  

^a STATION BIOLOGIQUE   (France)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

^c UNIV MONTPELLIER   (France)

^d INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL PROTEIN; NUCLEAR PROTEIN; DNA; PRIMER DNA;

ALLELE; ALLOPATRY; ANIMAL TISSUE; ARTICLE; BATHYMODIOLUS AZORICUS; BATHYMODIOLUS PUTEOSERPENTIS; BATHYMODIOLUS THERMOPHILUS; CONTROLLED STUDY; DEEP SEA SPECIES; DNA FOOTPRINTING; DNA SEQUENCE; GENE FLOW; GENE FREQUENCY; GENE LOCUS; GENETIC ANALYSIS; GENETIC MODEL; GENETIC VARIABILITY; GEOGRAPHICAL VARIATION (SPECIES); HYDROTHERMAL VENT SPECIES; INTROGRESSION; MOLECULAR EVOLUTION; MUSSEL; MUTATION RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; POPULATION GENETICS; POPULATION SIZE; RECOMBINANT GENE; SPECIES COMPARISON; SPECIES DIFFERENTIATION; UNINDEXED SEQUENCE; ANIMAL; BIOLOGICAL MODEL; BIVALVE; GENETICS; HYBRIDIZATION; POPULATION MIGRATION; SPECIES DIFFERENCE;

BATHYMODIOLUS; BATHYMODIOLUS AZORICUS; BATHYMODIOLUS PUTEOSERPENTIS;

ANIMAL MIGRATION; ANIMALS; BASE SEQUENCE; BIVALVIA; DNA; DNA PRIMERS; GENE FLOW; GENETIC VARIATION; HYBRIDIZATION, GENETIC; MODELS, GENETIC; SPECIES SPECIFICITY;

EID: 68149128530     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006485     Document Type: Article

References (75)

1. Hey J, Machado CA (2003) The study of structured populations - New hope for a difficult and divided science. Nature Reviews Genetics 4: 535-543.
2. Hey J (2006) Recent advances in assessing gene flow between diverging populations and species. Current Opinion in Genetics & Development 16: 592-596.
3. Won YJ, Hey J (2005) Divergence population genetics of chimpanzees. Molecular Biology and Evolution 22: 297-307.
4. Niemiller ML, Fitzpatrick BM, Miller BT (2008) Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies. Molecular Ecology 17: 2258-2275.
5. Nosil P (2008) Speciation with gene flow could be common. Molecular Ecology 17: 2103-2106.
6. Machado CA, Hey J (2003) The causes of phylogenetic conflict in a classic Drosophila species group. Proceedings of the Royal Society of London Series B-Biological Sciences 270: 1193-1202.
7. Harrison RG (1990) Hybrid zones: windows on evolutionary processes. Oxf Surv Evol Biol 7: 69-128.
8. Bougault H, Charlou JL, Fouquet Y, Needham HD, Vaslet N, et al. (1993) Fast and Slow-Spreading Ridges: Structure and Hydrothermal Activity, Ultramafic Topographic Highs, and Ch4 Output. Journal of Geophysical Research-Solid Earth 98: 9643-9651.
9. Charlou JL, Donval JP, Fouquet Y, Jean-Baptiste P, Holm N (2002) Geochemistry of high H-2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36 degrees 14 ′ N, MAR). Chemical Geology 191: 345-359.
10. Tunnicliffe V (1991) The biology of hydrothermal vents: ecology and evolution. Oceanography and Marine Biology Annual Review 29: 319-407.
11. Van Dover CL, German CR, Speer KG, Parson LM, Vrijenhoek RC (2002) Marine biology - Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295: 1253-1257.
12. Matabos M, Thiebaut E, Le Guen D, Sadosky F, Jollivet D, et al. (2008) Geographic clines and stepping-stone patterns detected along the East Pacific Rise in the vetigastropod Lepetodrilus elevatus reflect species crypticism. Marine Biology 153: 545-563.
13. Genio L, Johnson SB, Vrijenhoek RC, Cunha MR, Tyler PA, et al. (2008) New record of "Bathymodiolus" mauritanicus Cosel 2002 from the Gulf of Cadiz (NE Atlantic) mud volcanoes. Journal of Shellfish Research 27: 53-61.
14. Kenk VC, Wilson BR (1985) A new mussel (Bivalvia, Mytilidae) from hydrothermal vents in the Galapagos Rift zone. Malacologia 26: 253-271.
15. Palumbi SR (1992) Marine Speciation on a Small Planet. Trends in Ecology & Evolution 7: 114-118.
16. Jones WJ, Won YJ, Maas PAY, Smith PJ, Lutz RA, et al. (2006) Evolution of habitat use by deep-sea mussels. Marine Biology 148: 841-851.
17. Olu-Le Roy K, Von Cosel R, Hourdez S, Carney SL, Jollivet D (2007) Amphi-Atlantic cold-seep Bathymodiolus species complexes across the equatorial belt. Deep-Sea Research I 54: 1890-1911.
18. Jollivet D, Comtet T, Chevaldonne P, Hourdez S, Desbruyeres D, et al. (1998) Unexpected relationship between dispersal strategies and speciation within the association Bathymodiolus (Bivalvia) - Branchipolynoe (Polychaeta) inferred from the rDNA neutral ITS2 marker. Cahiers De Biologie Marine 39: 359-362.
19. O'Mullan GD, Maas PAY, Lutz RA, Vrijenhoek RC (2001) A hybrid zone between hydrothermal vent mussels (Bivalvia: Mytilidae) from the Mid-Atlantic Ridge. Molecular Ecology 10: 2819-2831.
20. Won Y, Hallam SJ, O'Mullan GD, Vrijenhoek RC (2003) Cytonuclear disequilibrium in a hybrid zone involving deep-sea hydrothermal vent mussels of the genus Bathymodiolus. Molecular Ecology 12: 3185-3190.
21. Macdonald KC, Castillo DA, Miller SP, Fox PJ, Kastens KA, et al. (1986) Deep-Tow Studies of the Vema Fracture-Zone.1. Tectonics of a Major Slow Slipping Transform-Fault and Its Intersection with the Mid-Atlantic Ridge. Journal of Geophysical Research-Solid Earth and Planets 91: 3334-&.
22. Cannat M, Mevel C, Maia M, Deplus C, Durand C, et al. (1995) Thin Crust, Ultramafic Exposures, and Rugged Faulting Patterns at Mid-Atlantic Ridge (22-Degrees 24-Degrees-N). Geology 23: 49-52.
23. Hey J, Nielsen R (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.
24. Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press.
25. Tanguy A, Bierne N, Saavedra C, Pina B, Bachere E, et al. (2008) Increasing genomic information in bivalves through new EST collections in four species: Development of new genetic markers for environmental studies and genome evolution. Gene 408: 27-36.
26. Faure B, Bierne N, Tanguy A, Bonhomme F, Jollivet D (2007) Evidence for a slightly deleterious effect of intron polymorphisms at the EF1 alpha gene in the deep-sea hydrothermal vent bivalve Bathymodiolus. Gene 406: 99-107.
27. Bierne N, Tanguy A, Faure M, Faure B, David E, et al. (2007) Mark-recapture cloning: a straightforward and cost-effective cloning method for population genetics of single-copy nuclear DNA sequences in diploids. Molecular Ecology Notes 7: 562-566.
28. Faure M, David P, Bonhomme F, Bierne N (2008) Genetic hitchhiking in a subdivided population of Mytilus edulis. BMC Evolutionary Biology 8: 164.
29. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673-4680.
30. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
31. Bryant D, Moulton V (2004) Neighbor-Net: An agglomerative method for the construction of phylogenetic networks. Molecular Biology and Evolution 21: 255-265.
32. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23: 254-267.
33. Bahlo M, Griffiths RC (2000) Inference from gene trees in a subdivided population. Theoretical Population Biology 57: 79-95.
34. Lyngso RB, Song YS, Hein J (2005) Minimum recombination histories by branch and bound. Algorithms in Bioinformatics, Proceedings. Berlin: Springer-Verlag Berlin. pp 239-250.
35. Watterson GA (1975) Number of Segregating Sites in Genetic Models without Recombination. Theoretical Population Biology 7: 256-276.
36. Nei M (1987) Molecular Evolutionary Genetics. New York: Columbia Univ. Press.
37. Tajima F (1989a) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
38. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19: 2092-2100.
39. Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA-sequences. Genetics 111: 147-164.
40. Rozas J, Sànchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
41. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online. pp 47-50.
42. Hudson RR, Kreitman M, Aguadé M (1987) A test of neutral molecular evolution based on nuclotide data. Genetics 116: 153-159.
43. Ramirez-Soriano A, Ramos-Onsins SE, Rozas J, Calafell F, Navarro A (2008) Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics 179: 555-567.
44. Galtier N, Depaulis F, Barton NH (2000) Detecting Bottlenecks and Selective Sweeps From DNA Sequence Polymorphism. Genetics Society of America 155: 981-987.
45. Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proceedings of the National Academy of Sciences of the United States of America 104: 2785-2790.
46. Nielsen R, Wakeley J (2001) Distinguishing Migration From Isolation: A Markov Chain Monte Carlo Approach. Genetics 158: 885-896.
47. Geyer CJ (1992) Practical Markov Chain Monte Carlo. Statistical Science 7: 473-511.
48. Hasegawa M, Kishino H, Yano TA (1985) Dating of the Human Ape Splitting by a Molecular Clock of Mitochondrial-DNA. Journal of Molecular Evolution 22: 160-174.
49. Naar DF, Hey RN (1991) Tectonic evolution of the Easter Microplate. Journal of Geophysical Research-Solid Earth and Planets 96: 7961-7993.
50. Chevaldonne P, Jollivet D, Desbruyeres D, Lutz RA, Vrijenhoek RC (2002) Sister-species of eastern Pacific hydrothermal vent worms (Ampharetidae, Alvinellidae, Vestimentifera) provide new mitochondrial COI clock calibration. Cahiers De Biologie Marine 43: 367-370.
51. Johnson SB, Young CR, Jones WJ, Waren A, Vrijenhoek RC (2006) Migration, isolation, and speciation of hydrothermal vent limpets (Gastropoda; Lepetodrilidae) across the Blanco Transform Fault. Biological Bulletin 210: 140-157.
52. Rhoads DC, Lutz RA, Revelas EC, Cerrato RM (1981) Growth of Bivalves at Deep-Sea Hydrothermal Vents Along the Galapagos Rift. Science 214: 911-913.
53. Comtet T (1998) Structure des populations, reproduction, croissance et phyloge'ographie des Mytilidae des champs hydrothermaux Lucky Strike et Menez Gwen (37°17′9N et 37°50′N sur la dorsale médio-atlantique) [Thèse de doctorat]: Université Bretagne Occidentale, Brest. 244 p.
54. Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155: 1405-1413.
55. Segonzac M (1992) The Hydrothermal Vent Communities of Snake Pit Area (Mid-Atlantic Ridge, 23-Degrees-N, 3,480 M) - Megafaunal Composition and Microdistribution. Comptes Rendus De L Academie Des Sciences Serie Iii-Sciences De La Vie-Life Sciences 314: 593-600.
56. Van Dover CL, Desbruyères D, Segonzac M, Comtet T, Saldanha L, et al. (1996) Biology of the Lucky Strike hydrothermal field. Deep-Sea Research I 43: 1509-1529.
57. Von Cosel R, Metivier B, Hashimoto J (1994) Three new species of Bathymodiolus (Bivalvia, Mytilidae) from hydrothermal vents in the Lau Basin and the North Fiji Basin, Western Pacific, and the Snake Pit Area, Mid-Atlantic Ridge. Veliger 37: 374-392.
58. Barton NH, Hewitt GM (1985) Analysis of Hybrid Zones. Annual Review of Ecology and Systematics 16: 113-148.
59. Endler JA (1977) Geographic variation, speciation and gene flow. Princeton, NJ: Princeton Univ. Press.
60. Comtet T, Desbruyères D (1998) Population structure and recruitment in mytilid bivalves from the Lucky Strike and Menez Gwen hydrothermal vent fields (37°17′ N and 37°509 N on the Mid-Atlantic Ridge). Marine Ecology Progress Series 163: 165-177.
61. Gebruk AV, Chevaldonne P, Shank T, Lutz RA, Vrijenhoek RC (2000) Deep-sea hydrothermal vent communities of the Logatchev area (14 degrees 45 ′ N, Mid-Atlantic Ridge): diverse biotopes and high biomass. Journal of the Marine Biological Association of the United Kingdom 80: 383-393.
62. Barton NH (1986) The effects of linkage and density-dependent regulation on gene flow. Heredity 57: 415-426.
63. Buggs RJA (2007) Empirical study of hybrid zone movement. Heredity 99: 301-312.
64. Amos AF, Gordon AL, Schneider ED (1971) Water masses and circulation patterns in the region of the Blake-Bahama Outer Ridge. Deep-Sea Research 18: 145-165.
65. Stephens JC, Marshall DP (2000) Dynamical pathways of Antarctic Bottom Water in the Atlantic. Journal of Physical Oceanography 30: 622-640.
66. Machado CA, Kliman RM, Markert JA, Hey J (2002) Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila obscura and close relatives. Mol Biol Evol 19(4): 472-488.
67. Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312: 570-572.
68. Orr HA, Masly JP, Presgraves DC (2004) Speciation genes. Current Opinion in Genetics & Development 14: 675-679.
69. Distel DL, Lee HKW, Cavanaugh CM (1995) Intracellular coexistence of methano- and thioautotrophic bacteria in a hydrothermal vent mussel. Proceedings of the National Academy of Sciences of the USA 92: 9598-9602.
70. Fiala-Medioni A, McKiness ZP, Dando P, Boulegue J, Mariotti A, et al. (2002) Ultrastructural, biochemical, and immunological characterization of two populations of the mytilid mussel Bathymodiolus azoricus from the Mid-Atlantic Ridge: evidence for a dual symbiosis. Marine Biology 141: 1035-1043.
71. Kadar E, Bettencourt R, Costa V, Santos RS, Lobo-Da-Cunha A, et al. (2005) Experimentally induced endosymbiont loss and re-acquirement in the hydrothermal vent bivalve Bathymodiolus azoricus. Journal of Experimental Marine Biology and Ecology 318: 99-110.
72. Won YJ, Hallam SJ, O'Mullan GD, Pan IL, Buck KR, et al. (2003) Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Applied and Environmental Microbiology 69: 6785-6792.
73. Schierup MH, Hein J (2000) Consequences of recombination on traditional phylogenetic analysis. Genetics 156: 879-891.
74. Hilton H, Kliman RM, Hey J (1994) Using Hitchhiking Genes to Study Adaptation and Divergence During Speciation within the Drosophila-Melanogaster Species Complex. Evolution 48: 1900-1913.
75. Stephan W, Xing L, Kirby DA, Braverman JM (1998) A test of the background selection hypothesis based on nucleotide data from Drosophila ananassae. Proceedings of the National Academy of Sciences of the United States of America 95: 5649-5654.