Speciation on the coasts of the new world: Phylogeography and the evolution of bindin in the sea urchin genus Lytechinus

Evolution

Volumn 58, Issue 6, 2004, Pages 1225-1241

  Zigler, Kirk S ^a,b,c   Lessios, H A ^a  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b DUKE UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Echinoid; Gamete recognition; Hybridization; Selection; Speciation

Indexed keywords

DIVERGENCE; EVOLUTION; PHYLOGEOGRAPHY; SPECIATION (BIOLOGY);

ANIMALIA; ATLANTICUS; ECHINOIDA; ECHINOIDEA; INVERTEBRATA; LYTECHINUS; LYTECHINUS ANAMESUS; LYTECHINUS EUERCES; LYTECHINUS PANAMENSIS; LYTECHINUS PICTUS; LYTECHINUS SEMITUBERCULATUS; LYTECHINUS VARIEGATUS; LYTECHINUS VARIEGATUS CAROLINUS; LYTECHINUS VARIEGATUS VARIEGATUS; LYTECHINUS WILLIAMSI; SPHAERECHINUS GRANULARIS;

EID: 3042666523     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2004.tb01702.x     Document Type: Article

References (94)

1. Beddingfield, S. D., and J. B. McClintock. 1994. Environmentally induced catastrophic mortality of the sea urchin Lytechinus variegatus in shallow seagrass habitats of Saint Josephs Bay, Florida. Bull. Mar. Sci. 55:235-240.
2. Bermingham, E. B., and H. A. Lessios. 1993. Rate variation of protein and mtDNA evolution as revealed by sea urchins separated by the Isthmus of Panama. Proc. Natl. Acad. Sci. USA 90:2734-2738.
3. Biermann, C. H. 1998. The molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae). Mol. Biol. Evol. 15:1761-1771.
4. Cameron, R. A. 1984. Two species of Lytechinus (Toxopneustidae: Echinoidea: Echinodermata) are completely cross-fertile. Bull. So. Calif. Acad. Sci. 83:154-157.
5. _. 1986. Reproduction, larval occurrence and recruitment in Caribbean sea urchins. Bull. Mar. Sci. 39:332-346.
6. Camp, D. K., S. P. Cobb, and J. F. van Breedveld. 1973. Overgrazing of seagrasses by a regular urchin, Lytechinus variegatus. Bioscience. 23:37-38.
7. Chesher, R. H. 1968. Lytechinus williamsi, a new sea urchin from Panama. Breviora 305:1-13.
8. _. 1972. The status of knowledge of Panamanian echinoids, 1971, with comments on other echinoderms. Bull. Biol. Soc. Wash. 2:139-158.
9. Clark, H. L. 1940. Eastern Pacific expeditions of the New York Zoological Society. XXI. Notes on echinoderms from the west coast of Central America. Zoologica 25:331-355.
10. Coates, A. G., and J. A. Obando. 1996. The geologic evolution of the Central American Isthmus. Pp. 21-56 in J. B. C. Jackson, A. G. Coates, and A. Budd, eds. Evolution and environment in tropical America. Univ. of Chicago Press, Chicago.
11. Debenham, P., M. A. Brzezinski, and K. R. Foltz. 2000a. Evaluation of sequence variation and selection in the bindin locus of the red sea urchin, Strongylocentrotus franciscanus. J. Mol. Evol. 51:481-490.
12. Debenham, P., M. Brzezinski, K. Foltz, and S. Gaines. 2000b. Genetic structure of populations of the red sea urchin, Strongylocentrotus franciscanus. J. Exp. Mar. Biol. Ecol. 253:49-62.
13. Durham, W. J., C. Wagner, and D. P. Abbott. 1980. Echinoidea: the sea urchins. Pp. 160-176 in R. Morris, D. P. Abbott, and E. C. Hadderlie, eds. Intertidal invertebrates of California. Stanford Univ. Press, Stanford, CA.
14. Emlet, R. B. 1995. Developmental mode and species geographic range in regular sea urchins (Echinodermata: Echinoidea). Evolution 49:476-489.
15. Emlet, R. B., L. R. McEdward, and R. R. Strathmann. 1987. Echinoderm larval ecology viewed from the egg. Pp. 55-136 in M. Jangoux and J. M. Lawrence, eds. Echinoderm studies. Vol. 2. Balkema Press, Rotterdam.
16. Ettensohn, C. A. 1985. Gastrulation in the sea urchin embryo is accompanied by the rearrangement of invaginating epithelial cells. Dev. Biol. 112:383-390.
17. Ettensohn, C. A., and D. R. McClay. 1988. Cell lineage conversion in the sea urchin embryo. Dev. Biol. 125:396-409.
18. Frohman, M. A., M. K. Dush, and G. R. Martin. 1988. Rapid production of full-length cDNAs from rare transcripts by amplification using a single gene specific oligonucleotide primer. Proc. Natl. Acad. Sci. USA 85:8998-9002.
19. Fu, Y. X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915-925.
20. Geyer, L. B., and S. R. Palumbi. 2003. Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins. Evolution 57:1049-1060.
21. Glynn, P. W. 1968. Mass mortalities of echinoids and other reef flat organisms coincident with midday, low water exposures in Puerto Rico. Mar. Biol. 1:226-243.
22. Goodbody, I. M. 1961. Mass mortality of a marine fauna following tropical rains. Ecology 42:150-155.
23. Hardin, J. D., and L. Y. Cheng. 1986. The mechanisms of archenteron elongation during sea urchin gastrulation. Dev. Biol. 115:490-501.
24. Harvey, E. B. 1956. The American Arbacia and other sea urchins. Princeton Univ. Press, Princeton, NJ.
25. Hasegawa, M., H. Kishino, and T. Yano. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22:160-174.
26. Hendler, G., J. E. Miller, D. L. Pawson, and P. M. Kier. 1995. Sea stars, sea urchins, and allies: echinoderms of Florida and the Caribbean. Smithsonian Institution Press, Washington, DC.
27. Hudson, R. R. 1990. Gene genealogies and the coalescent process. Pp. 1-44 in D. Futuyma and J. D. Antonovics, eds. Oxford Surveys in Evolutionary Biology. Vol. 7. Oxford Univ. Press, New York.
28. Hudson, R. R., and N. L. Kaplan. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147-164.
29. Hudson, R, R., and M. Turelli. 2003. Stochasticity overrules the "three-times rule": Genetic drift, genetic draft, and coalescence times for nuclear loci versus mitochondrial DNA. Evolution 57:182-190.
30. Huelsenbeck, J. P., and F. Ronquist. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
31. Junqueira, A. D. R., C. R. R. Ventura, A. L. P. S. Decarvalho, and A. J. Schmidt. 1997. Population recovery of the sea urchin Lytechlnus variegatus in a seagrass flat (Araruama Lagoon, Brazil): the role of recruitment in a disturbed environment. Invertebr. Reprod. Dev. 31:143-150.
32. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitution through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
33. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA 2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244-1245.
34. Lessios, H. A. 1984. Annual reproductive periodicity in eight echinoid species on the Caribbean coast of Panama. Pp. 303-310 in B. F. Keegan and B. D. S. O'Connor, eds. Proceedings of the Fifth International Echinoderm Conference. A.A. Balkema, Boston.
35. _. 1988. Population dynamics of Diadema antillarum (Echinodermata: Echinoidea) following mass mortality in Panama. Mar. Biol. 99:515-526.
36. _. 1991. Presence and absence of monthly reproductive rhythms among eight Caribbean echinoids off the coast of Panama. J. Exp. Mar. Biol. Ecol. 153:27-47.
37. Lessios, H. A., and C. W. Cunningham. 1990. Gametic incompatibility between species of the sea urchin Echinometra on the two sides of the Isthmus of Panama. Evolution 44:933-941.
38. Lessios, H. A., and J. S. Pearse. 1996. Hybridization and introgression between Indo-Pacific species of Diadema. Mar. Biol. 126:715-723.
39. Lessios, H. A., B. D. Kessing, and D. R. Robertson. 1998. Massive gene flow across the world's most potent marine biogeographic barrier. Proc. R. Soc. Lond. B. 265:583-588.
40. Lessios, H. A., B. D. Kessing, D. R. Robertson, and G. Paulay. 1999. Phylogeography of the pantropical sea urchin Eucidaris in relation to land barriers and ocean currents. Evolution 53:806-817.
41. Lessios, H. A., B. D. Kessing, and J. S. Pearse. 2001. Population structure and speciation in tropical seas: Global phylogeography of the sea urchin Diadema. Evolution 55:955-975.
42. Lessios, H. A., J. Kane, and D. R. Robertson. 2003. Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans. Evolution 57:2026-2036.
43. Lewis, J. B. 1963. The food of some deep-water echinoids from Barbados. Bull. Mar. Sci. Gulf Caribb. 13:360-363.
44. Li, W.-H. 1993. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol. 36:96-99.
45. Macía, S., and D. Lirman. 1999. Destruction of Florida Bay sea-grasses by a grazing front of sea urchins. Bull. Mar. Sci. 65:593-601.
46. Mayr, E. 1954. Geographic speciation in echinoids. Evolution 8:1-18.
47. Maddison, D. R., and W. P. Maddison. 2000. MacClade 4: analysis of phylogeny and character evolution. Ver. 4.0. Sinauer Associates, Sunderland, MA.
48. Mazur, J. E., and J. W. Miller. 1971. A description of the complete metamorphosis of the sea urchin Lytechinus variegatus cultured in synthetic sea water. Ohio J. Sci. 71:30-36.
49. McCartney, M. A., and H. A. Lessios. 2002. Quantitative analysis of gametic incompatibility between closely related species of neotropical sea urchins. Biol. Bull. 202:166-181.
50. McCartney, M. A., G. Keller, and H. A. Lessios. 2000. Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol. Ecol. 9:1391-1400.
51. McDonald, J. H., and M. Kreitman. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654.
52. McMillan, W. O., R. A. Raff, and S. R. Palumbi. 1992. Population genetic consequences of developmental evolution in sea urchins (genus Hellocidaris). Evolution 46:1299-1312.
53. Metz, E. C., and S. R. Palumbi. 1996. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Biol. Evol. 13:397-406.
54. Metz, E. C., G. Gómez-Gutiérrez, and D. Vacquier. 1998. Mitochondrial DNA and bindin gene sequence evolution among allopatric species of the sea urchin genus Arbacia. Mol. Biol. Evol. 15:185-195.
55. Minor, J. E., D. R. Fromson, R. J. Britten, and E. H. Davidson. 1991. Comparison of the bindin proteins of Strongylocentrotus franciscanus, S. purpuratus, and Lytechinus variegatus: sequences involved in the species specificity of fertilization. Mol. Biol. Evol. 8:781-795.
56. Moore, W. S. 1995. Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718-726.
57. Mortensen, T. 1921. Studies of the development and larval forms of echinoderms. G.E.C. Gad, Copenhagen.
58. _. 1943. A monograph of the Echinoidea III(2): Camarodonta. I. Orthopsidae, Glycocyphidae, Temnopleuridae and Toxopneustidae. C.A. Reitzel, Copenhagen.
59. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583-590.
60. Palumbi, S. R. 1996. What can molecular genetics contribute to marine biogeography? An urchin's tale. J. Exp. Mar. Biol. Ecol. 203:75-92.
61. Palumbi, S. R., and B. D. Kessing. 1991. Population biology of the transarctic exchange: mtDNA sequence similarity between Pacific and Atlantic sea urchins. Evolution 45:1790-1805.
62. Palumbi, S. R., and A. C. Wilson. 1990. Mitochondrial DNA diversity in the sea urchins Strongylocentrotus purpuratus and S. droebachiensis. Evolution 44:403-415.
63. Palumbi, S. R., G. Grabowsky, T. Duda, L. Geyer, and N. Tachino. 1997. Speciation and population genetic structure in tropical Pacific sea urchins. Evolution 51:1506-1517.
64. Palumbi, S. R., F. Cipriano, and M. P. Hare. 2001. Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution 55:859-868.
65. Pamilo, P., and N. O. Bianchi. 1993. Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol. Biol. Evol. 10:271-281.
66. Pawson, D. L., and J. E. Miller. 1982. Studies of genetically controlled phenotypic characters in laboratory-reared Lytechinus variegatus (Lamarck) (Echinodermata:Echinoidea). Pp. 165-171 in J. M. Lawrence, ed. Proceedings of the International Echinoderm Conference, Tampa Bay. A.A. Balkema, Rotterdam.
67. Posada, D., and K. A. Crandall. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-818.
68. Rambaut, A. 1996. Se-Al: sequence alignment editor. University of Oxford, Oxford, U.K. Available at http://evolve.zoo.ox.ac.uk/.
69. Rogers, A. R. 1995. Genetic evidence for a Pleistocene population explosion. Evolution 49:608-615.
70. Rogers, A. R., and H. Harpending. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9:552-569.
71. Rosenberg, V. A., and R. P. Wain. 1982. Isozyme variation and genetic differentiation in the decorator sea urchin, Lytechinus variegatus (Lamarck, 1816). Pp. 193-197 in J. M. Lawrence, ed. Proceedings of the International Echinoderm Conference, Tampa Bay. A.A. Balkema, Rotterdam.
72. Rose, C. D., W. C. Sharp, W. J. Kenworthy, J. H. Hunt, W. G. Lyons, E. J. Prager, J. F. Valentine, M. O. Hall, P. E. Whitfield, and J. W. Fourqurean. 1999. Overgrazing of a large seagrass bed by the sea urchin Lytechinus variegatus in Outer Florida Bay. Mar. Ecol. Progr. Ser. 190:211-222.
73. Rozas, J., and R. Rozas. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175.
74. Schneider, S., and L. Excoffier. 1999. Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079-1089.
75. Schneider, S., D. Roessli, and L. Excoffier. 2000. Arlequin. Ver. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland.
76. Serafy, D. K. 1973. Variation in the polytypic sea urchin Lytechinus variegatus (Lamarck, 1816) in the western Atlantic (Echinodermata: Echinoidea). Bull. Mar. Sci. 23:525-534.
77. Sherwood, D. R., and D. R. McClay. 1999. LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo. Development 126:1703-1713.
78. Swanson, W. J., C. F. Aquadro, and V. D. Vacquier. 2001. Polymorphism in abalone fertilization proteins is consistent with the neutral evolution of the egg's receptor for lysin (VERL) and positive Darwinian selection of sperm lysin. Mol. Biol. Evol. 18:376-383.
79. Swofford, D. L. 2001. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Ver. 4. Sinauer Associates, Sunderland, MA.
80. Swofford, D. L., and R. B. Selander. 1989. BIOSYS-1. A computer program for the analysis of allelic variation in population genetics and biochemical systematics. Illinois Natural History Survey, Champaign, IL.
81. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
82. Tamura, K., and M. Nei. 1993. Estimating the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512-526.
83. Ulrich, A. S., M. Otter, C. G. Glabe, and D. Hoekstra. 1998. Membrane fusion is induced by a distinct peptide sequence of the sea urchin fertilization protein bindin. J. Biol. Chem. 273:16748-16755.
84. Ulrich, A. S., W. Tichelaar, G. Forster, O. Zschornig, S. Weinkauf, and H. W. Meyer. 1999. Ultrastructural characterization of peptide-induced membrane fusion and peptide self-assembly in the lipid bilayer. Biophys. J. 77:829-841.
85. Vacquier, V. D., and G. W. Moy. 1977. Isolation of bindin: the protein responsible for adhesion of sperm to sea urchin eggs. Proc. Natl. Acad. Sci. USA 74:2456-2460.
86. VanDoorn, G. S., P. C. Luttikhuizen, and F. J. Weissing. 2001. Sexual selection at the protein level drives the extraordinary divergence of sex-related genes during sympatric speciation. Proc. R. Soc. Lond. B. 268:2155-2161.
87. Watts, S. A., J. B. McClintock, and J. M. Lawrence. 2001. The ecology of Lytechinus variegatus. Pp. 375-393 in J. M. Lawrence, ed. Edible sea urchins: biology and ecology. Elsevier, Amsterdam.
88. Workman, P. L., and J. D. Niswander. 1970. Population studies on southwestern Indian tribes. II. Local genetic differentiation in the Papago. Am. J. Hum. Genet. 22:24-29.
89. Yang, Z. 2000. Phylogenetic analysis by maximum likelihood (PAML). Ver. 3.0. University College London, London.
90. Yang, Z., R. Nielsen, N. Goldman, and A-M. K. Pedersen. 2000. Codon substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431-449.
91. Zhang, J., S. Kumar, and M. Nei. 1997. Small-sample tests of episodic evolution: a case study of primate lysosymes. Mol. Biol. Evol. 14:1335-1338.
92. Zigler, K. S., and H. A. Lessios. 2003a. Evolution of the gamete recognition protein bindin across six orders of sea urchins. Biol. Bull. 205:8-15.
93. _. 2003b. Evolution of bindin in the pantropical sea urchin Tripneustes: comparisons to bindin of other genera. Mol. Biol. Evol. 20:220-231.
94. Zigler, K. S., E. C. Raff, E. Popodi, R. A. Raff, and H. A. Lessios. 2003. Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57:2293-2302.