Multiple gene genealogies reveal asymmetrical hybridization and introgression among strongylocentrotid sea urchins

Molecular Ecology

Volumn 18, Issue 6, 2009, Pages 1239-1251

  Addison, Jason A ^a,b   Pogson, Grant H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF NEW BRUNSWICK   (Canada)

Author keywords

Gamete compatibility; Gene genealogies; Hybridization; Introgression; Speciation; Strongylocentrotus

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; DNA SEQUENCE; FERTILIZATION; GENE FLOW; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENETICS; HYBRIDIZATION; MALE; METABOLISM; PHYLOGENY; POPULATION GENETICS; SPECIES DIFFERENCE; SPERMATOZOON; STRONGYLOCENTROTUS;

ANIMALS; DNA, MITOCHONDRIAL; FERTILIZATION; GENE FLOW; GENETIC VARIATION; GENETICS, POPULATION; HYBRIDIZATION, GENETIC; MALE; MODELS, GENETIC; PHYLOGENY; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SPERMATOZOA; STRONGYLOCENTROTUS;

ECHINOIDEA; INVERTEBRATA; STRONGYLOCENTROTIDAE; STRONGYLOCENTROTUS; STRONGYLOCENTROTUS DROEBACHIENSIS; STRONGYLOCENTROTUS FRANCISCANUS; STRONGYLOCENTROTUS PALLIDUS; STRONGYLOCENTROTUS PURPURATUS;

EID: 61649107697     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04094.x     Document Type: Article

References (97)

1. Addison JA (2007) Simultaneous cloning of multiple nuclear genes by pooling PCR products of variable size: a cost effective method of improving efficiency in large-scale genetic analyses. Molecular Ecology Notes, 7, 389 392.
2. Addison JA, Hart MW (2005) Colonization, dispersal, and hybridization influence phylogeography of north Atlantic sea urchins (Strongylocentrotus droebachiensis). Evolution, 59, 532 543.
3. Arnold ML (1997) Natural Hybridization and Evolution. Oxford University Press, New York.
4. Arnold SJ, Verrell PA, Tilley SG (1996) The evolution of asymmetry in sexual isolation: a model and test case. Evolution, 50, 1024 1033.
5. Bachtrog D, Thornton K, Clark A, Andolfatto P (2006) Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group. Evolution, 60, 292 302.
6. Barton NH (2001) The role of hybridization in evolution. Molecular Ecology, 10, 551 568.
7. Barton NH, Bengtsson BO (1986) The barrier to genetic exchange between hybridising populations. Heredity, 57, 357 376.
8. Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16, 113 148.
9. Biermann CH (1998) The molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae). Molecular Biology and Evolution, 15, 1761 1771.
10. Biermann CH, Kessing BD, Palumbi SR (2003) Phylogeny and development of marine model species: strongylocentrotid sea urchins. Evolution and Development, 5, 360 371.
11. Bluhm BA, Piepenburg D, Von Juterzenka K (1998) Distribution, standing stock, growth, mortality and production of Strongylocentrotus pallidus (Echinodermata: Echinoidea) in the Northern Barents Sea. Polar Biology, 20, 325 334.
12. 1 hybrids in centrarchid fishes. Genetics, 178, 1037 1048.
13. Buggs RJA (2007) Empirical study of hybrid zone movement. Heredity, 99, 301 312.
14. Burgess KS, Morgan M, Deverno L, Husband BC (2005) Asymmetrical introgression between two Morus species (M. alba, M. rubra) that differ in abundance. Molecular Ecology, 14, 3471 3483.
15. Byrne M, Anderson MJ (1994) Hybridization of sympatric Patiriella species in New South Wales. Evolution, 48, 564 576.
16. Clement M, Posada D, Crandall KA (2000) tcs: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657 1660.
17. Coppard SE, Campbell AC (2005) Lunar periodicities of diadematid echinoids breeding in Fiji. Coral Reefs, 24, 324 332.
18. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, Massachusetts.
19. Debenham P, Brzezinski MA, Foltz KR (2000) Evaluation of sequence variation and selection in the bindin locus of the red sea urchin Strongylocentrotus franciscanus. Journal of Molecular Evolution, 51, 481 490.
20. Edmands S, Moberg PE, Burton RS (1996) Allozyme and mitochondrial DNA evidence of population subdivision in the purple sea urchin Strongylocentrotus purpuratus. Marine Biology, 126, 443 450.
21. Edwards SV, Dillon M (2004) Hitchhiking and recombination in birds: evidence from Mhc-linked and unlinked loci in Red-winged Blackbirds (Agelaius phoeniceus). Genetical Research, 84, 175 192.
22. Ellstrand NC (1992) Gene flow by pollen: implications for plant conservation genetics. Oikos, 63, 77 86.
23. Fischer EA (1980) Speciation in the hamlets (Hypoplectrus: Serranidae) - a continuing enigma. Copeia, 1980, 649 659.
24. Flowers JM, Schroeter SC, Burton RS (2002) The recruitment sweepstakes has many winners: genetic evidence from the sea urchin Strongylocentrotus purpuratus. Evolution, 56, 1445 1453.
25. Gagnon JM, Gilkinson KD (1994) Discrimination and distribution of the sea-urchins Strongylocentrotus droebachiensis (O.F. Müller) and S. pallidus (G.O. Sars) in the northwest Atlantic. Sarsia, 79, 1 11.
26. Geyer LB, Palumbi SR (2003) Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins. Evolution, 57, 1049 1060.
27. Hellberg ME, Vacquier VD (1999) Rapid evolution of fertilization selectivity and lysine cDNA sequences in teguline gastropods. Molecular Biology and Evolution, 16, 839 848.
28. 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.
29. 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.
30. Illies MR, Peeler MT, Dechtirauk AM, Ettensohn CA (2002) Identification and developmental expression of new biomineralization proteins in the sea urchin Strongylocentrotus purpuratus. Development Genes and Evolution, 212, 419 431.
31. Jacobs HT, Elliott DJ, Math VB, Farquharson A (1988) Nucleotide-sequence and gene organization of sea-urchin mitochondrial DNA. Journal of Molecular Biology, 202, 185 217.
32. Jensen M (1974) Strongylocentrotidae (Echinoidea), a morphological and systematic study. Sarsia, 57, 113 148.
33. Kauserud H, Svegården IB, Decock C, Hallenberg N (2007) Hybridization among cryptic species of the cedar fungus Coniophora puteana (Basidiomycota). Molecular Ecology, 15, 389 399.
34. Kenny AP, Kozlowski DJ, Oleksyn DW, Angerer LM, Angerer RC (1999) SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres. Development, 126, 5473 5483.
35. Knowlton N, Weight LA, Solorzano LA, Mills DK, Bermingham E (1993) Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science, 260, 1629 1632.
36. Kumar S, Tamura K, Nei M (2004) mega3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics, 5, 150 163.
37. Lee Y-H (2003) Molecular phylogenies and divergence times of sea urchin species of Stronglyocentrotidae, Echinoida. Molecular Biology and Evolution, 20, 1211 1221.
38. Lee Y-H, Ota T, Vacquier VD (1995) Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Molecular Biology and Evolution, 12, 231 238.
39. Lee Y-H, Britten RJ, Davidson EH (1999) SM37, a skeletogenic gene of the sea urchin embryo linked to the SM50 gene. Development Growth and Differentiation, 41, 303 312.
40. Lessios HA (2007) Reproductive isolation between species of sea urchins. Bulletin of Marine Science, 81, 191 208.
41. Lessios HA, Cunningham CW (1990) Gametic incompatibility between species of the sea urchin Echinometra on the two sides of the Isthmus of Panama. Evolution, 44, 933 941.
42. Levitan DR (1998) Does Bateman's principle applies to broadcast-spawning organisms? Egg traits influence in situ fertilization rates among congeneric sea urchins. Evolution, 52, 1043 1056.
43. Levitan DR (2002a) Density-dependent selection on gamete traits in three congeneric sea urchins. Ecology, 83, 464 479.
44. Levitan DR (2002b) The relationship between conspecific fertilization success and reproductive isolation among three congeneric sea urchins. Evolution, 56, 1599 1609.
45. Levitan DR (2008) Gamete traits influence the variance in reproductive success, the intensity of sexual selection, and the outcome of sexual conflict among congeneric sea urchins. Evolution, 62, 1305 1316.
46. Levitan DR, Ferrell DL (2006) Selection on gamete recognition proteins depends on sex, density, and genotype frequency. Science, 312, 267 269.
47. Levitan DR, terHorst CP, Fogarty ND (2007) The risk of polyspermy in three congeneric sea urchins and its implications for gamete compatibility and reproductive isolation. Evolution, 61, 2009 2016.
48. Lillie FR (1921) Studies of fertilization. IX. On the question of superposition of fertilization of parthenogenesis in Strongylocentrotus purpuratus. Biological Bulletin, 40, 23 31.
49. Lyon JD, Vacquier VD (1999) Interspecies chimeric sperm lysins identify regions mediating species-specific recognition of the abalone egg vitelline envelope. Developmental Biology, 214, 151 159.
50. Mallet J (2005) Hybridization as an invasion of the genome. Trends in Ecology & Evolution, 20, 229 237.
51. Mavarez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, Linares M (2006) Speciation by hybridization in Helconius butterflies. Nature, 441, 868 871.
52. Mayr E (1963) Animal Species and Evolution. Belknap Press, Cambridge, Massachusetts.
53. McCartney MA, Lessios HA (2002) Quantitative analysis of gamete incompatibility between closely related species of neotropical sea urchins. Biological Bulletin, 202, 166 181.
54. McCartney MA, Lessios HA (2004) Adaptive evolution of sperm bindin tracks egg incompatibility in neotropical sea urchins of the genus Echinometra. Molecular Biology and Evolution, 21, 732 745.
55. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature, 351, 652 654.
56. McVean G, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics, 160, 1231 1241.
57. Metz EC, Palumbi SR (1996) Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Molecular Biology and Evolution, 13, 397 406.
58. Metz EC, Robles-Sikisaka R, Vacquier VD (1998a) Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. Proceedings of the National Academy of Sciences, USA, 95, 10676 10681.
59. Metz EC, Gómez-Gutiérrez Vacquier VD (1998b) Mitochondrial DNA and bindin gene sequence evolution among allopatric species of the sea urchin genus Arbacia. Molecular Biology and Evolution, 15, 185 195.
60. Miller KM, Supernault KJ, Li S, Withler RE (2006) Population structure in two marine invertebrate species Panopea abrupta and Strongylocentrotus franciscanus targeted for aquaculture enhancement in British Columbia. Journal of Shellfish Research, 25, 33 42.
61. Moberg PE, Burton RS (2000) Genetic heterogeneity among adult and recruit red sea urchins, Strongylocentrotus franciscanus. Marine Biology, 136, 773 784.
62. Moore JC, Sumerel JL, Schnackenberg BJ et al 2002) Cyclin D and cdk4 are required for normal development beyond the blastula stage in sea urchin embryos. Molecular and Cellular Biology, 22, 4863 4875.
63. Nielsen R, Wakeley J (2001) Distinguishing isolation from migration: a Markov chain Monte Carlo approach. Genetics, 158, 885 896.
64. 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.
65. Nylander JAA (2004) MrModeltest version 2. Program distributed by the author. Evolutionary Biology Center, Uppsala University, Uppsala, Sweden (available online at. http://www.abc.se/∼nylander/).
66. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics, 25, 547 572.
67. Palumbi SR (1998) Species formation and the evolution of gamete recognition loci. In : Endless Forms. Species and Speciation (eds Howard DJ, Berlocher SH pp. 271 278. Oxford University Press, New York.
68. Palumbi SR (1999) All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proceedings of the National Academy of Sciences, USA, 96, 12632 12637.
69. Palumbi SR, Lessios HA (2005) Evolutionary animation: how do molecular phylogenies compare to Mayr's reconstruction of speciation patterns in the sea? Proceedings of the National Academy of Sciences, USA, 102, 6566 6572.
70. Palumbi SR, Wilson AC (1990) Mitochondrial DNA diversity in the sea urchins Strongylocentrotus purpuratus and S. droebachiensis. Evolution, 44, 403 415.
71. Pernet B (1999) Gamete interactions and genetic differentiation among three sympatric polychaetes. Evolution, 53, 435 446.
72. Pogson GH, Mesa KA, Boutilier RG (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.
73. Quesada H, Posada D, Caballero A, Moran P, Rolan-Alvarez E (2007) Phylogenetic evidence for multiple sympatric ecological diversification in a marine snail. Evolution, 61, 1600 1612.
74. Rambaut A, Drummond A (2005) Tracer version 1.3: a program for analyzing results from Bayesian MCMC programs such as BEAST and MrBayes. Distributed by the authors at: http://evolove.zoo.ox.ac.uk/software.html?id=tracer.
75. Rieseberg LH (2000) Crossing relationships among ancient and experimental sunflower hybrid lineages. Evolution, 54, 859 865.
76. Robert J (2003) Evolution of heat shock protein and immunity. Developmental and Comparative Immunology, 27, 449 464.
77. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572 1574.
78. Rozas J, Sánchez-De I, Barrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496 2497.
79. Savolainen V, Anstett MC, Lexer C et al 2006) Sympatric speciation in palms on an oceanic island. Nature, 441, 210 213.
80. Sea Urchin Genome Sequencing Consortium (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science, 314, 941 952.
81. Seto J, Zhang Y, Hamilton P, Wilt F (2004) The localization of occluded matrix proteins in calcareous spicules of sea urchin larvae. Journal of Structural Biology, 148, 123 130.
82. Shaw KL, Lugo E (2001) Mating asymmetry and the direction of evolution in the Hawaiian cricket genus Laupala. Molecular Ecology, 10, 751 759.
83. Smith LC, Chang L, Britten RJ, Davidson EH (1996) Sea urchin genes expressed in activated coelomocytes are identified by expressed sequence tags. Complement homologues and other putative immune response genes suggest immune system homology within deuterostomes. Journal of Immunology, 156, 593 602.
84. Stein AC, Uy JAC (2006) Unidirectional introgression of a sexually selected trait across an avian hybrid zone: a role for female choice? Evolution, 60, 1476 1485.
85. Strathmann RR (1978) Length of pelagic period in echinoderms with feeding larvae from the northwest Pacific. Journal of Experimental Marine Biology and Ecology, 34, 23 27.
86. Strathmann RR (1981) On barriers to hybridization between Strongylocentrotus droebachiensis (O.F. Müller) and S. pallidus (G. O. Sars). Journal of Experimental Marine Biology and Ecology, 55, 39 47.
87. Su̧snik S, Weiss S, Odak T, Delling B, Treer T, Snoj A (2007) Reticulate evolution: ancient introgression of the Adriatic brown trout mtDNA in softmouth trout Salmo obtusirostris (Teleostei: Salmonidae). Biological Journal of the Linnean Society, 90, 139 152.
88. Swan EF (1953) The Strongylocentrotidae (Echinoidea) of the northeast Pacific. Evolution, 7, 269 273.
89. Swofford D (2000) paup*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, Massachusetts.
90. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585 595.
91. Tiffin P, Olson MS, Moyle LC (2001) Asymmetrical crossing barriers in angiosperms. Proceedings of the Royal Society B: Biological Sciences, 268, 861 867.
92. Turelli M, Moyle LC (2007) Asymmetric postzygotic isolation: Darwin's corollary to Haldane's rule. Genetics, 176, 1059 1088.
93. Vacquier VD (1998) Evolution of gamete recognition proteins. Science, 281, 1995 1998.
94. Vasseur EV (1952) Geographic variation in the Norwegian sea-urchins, Strongylocentrotus droebachiensis and S. pallidus. Evolution, 6, 87 100.
95. Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006) The role of hybridization in the evolution of reef corals. Annual Review of Ecology, Evolution, and Systematics, 37, 489 517.
96. Zigler KS, Lessios HA (2003) Evolution of bindin in the pantropical sea urchin Tripneustes: comparisons to bindin of other genera. Molecular Biology and Evolution, 20, 220 231.
97. Zigler KS, McCartney MA, Levitan DR, Lessios HA (2005) Sea urchin bindin divergence predicts gamete compatibility. Evolution, 59, 2399 2404.