Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins

Evolution

Volumn 57, Issue 5, 2003, Pages 1049-1060

  Geyer, Laura B ^a,b   Palumbi, Stephen R ^b  

^a HARVARD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Bindin; Positive selection; Reinforcement; Reproductive character displacement; Sea urchins; Speciation

Indexed keywords

CHARACTER DISPLACEMENT; ECHINODERM; EVOLUTION; GAMETE; HYBRIDIZATION; REPRODUCTION; SPECIATION (BIOLOGY);

ECHINODERMATA; ECHINOIDEA; ECHINOMETRA OBLONGA; ECHINOMETRA SP.; INVERTEBRATA;

EID: 0037636007     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2003.tb00315.x     Document Type: Article

References (86)

1. Arakaki, Y., and T. Uehara. 1991. Physiological adaptations and reproduction of the four types of Echinometra mathaei (Blainville). Pp. 105-112 in T. Yanagisawa, I. Yasumasu, C. Oguro, N. Suzuki, and T. Motokawa, eds. Biology of echinodermata. Balkema, Rotterdam.
2. _. 1999. Morphological comparison of black Echinometra individuals among those in the Indo-West Pacific. Zool. Sci. 16: 551-558.
3. 1 backcrosses between two closely related tropical species of sea urchins (genus Echinometra) in Okinawa. Invertebr. Reprod. Dev. 31:1-3.
4. Bernatchez, L., J. A. Vuorinen, R. A. Bodaly, and J. J. Dodson. 1996. Genetic evidence for reproductive isolation and multiple origins of sympatric trophic ecotypes of whitefish. Evolution 50: 624-635.
5. Biermann, C. 1998. The molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae). Mol. Biol. Evol. 15:1761-1771.
6. Blair, W. F. 1955. Mating call and stage of speciation in the Microhyla oivacea-M. carolinensis complex. Evolution 9:469-480.
7. Bordenstein, S. R., M. D. Drapeau, and J. H. Werren. 2000. Intra-specific variation in sexual isolation in the jewel wasp Nasonia. Evolution 54:567-573.
8. Brown, W. L., and E. O. Wilson. 1956. Character displacement. Syst. Zool. 7:49-64.
9. Bush, G. L. 1969. Sympatric host race formation and speciation in frugivorous flies of genus Rhagoletis (Diptera, Tephritidae). Evolution 23:237-251.
10. Bush, G. L., and J. J. Smith. 1998. The genetics and ecology of sympatric speciation: a case study. Res. Popul. Ecol. 40: 175-187.
11. Butlin, R. 1987. Speciation by reinforcement. Trends Ecol. Evol. 2:8-13.
12. Cain, M. L., V. Andreasen, and D. J. Howard. 1999. Reinforcing selection is effective under a relatively broad set of conditions in a mosaic hybrid zone. Evolution 53:1343-1353.
13. Coyne, J. A., and H. A. Orr. 1989. Patterns of speciation in Drosophila. Evolution 43:362-381.
14. Dobzhansky, T. 1940. Speciation as a stage in evolutionary divergence. Am. Nat. 74:312-321.
15. Felsenstein, J. 1981. Skepticism towards Santa Rosalia, or why are the so few kinds of animals? Evolution 35:124-138.
16. Futuyma, D. J., and G. C. Mayer. 1980. Non-allopatric speciation in animals. Syst. Zool 29:254-271.
17. Gavrilets, S. 2000. Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403:886-889.
18. Grant, P. 1972. Convergent and divergent character displacement. Biol. J. Linn. Soc. 4:39-68.
19. Hall, D. W., M. Kirkpatrick, and B. West. 2000. Runaway sexual selection when female preferences are directly selected. Evolution 54:1862-1869.
20. Hatfield, T. 1997. Genetic divergence in adaptive characters between sympatric species of stickleback. Am. Nat. 149: 1009-1029.
21. Hatfield, T., and D. Schluter. 1996. A test for sexual selection on hybrids of two sympatric sticklebacks. Evolution 50:2429-2434.
22. Higgie, M., S. Chenoweth, and M. W. Blows. 2000. Natural selection and the reinforcement of mate recognition. Science 290: 519-521.
23. Howard, D. 1993. Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. Pp. 46-69 in R. G. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, Oxford, U.K.
24. Howard, D. J., and P. G. Gregory. 1993. Post-insemination signaling systems and reinforcement. Philos. Trans. R. Soc. Lond. B 340: 231-236.
25. Howard, D. J., G. L. Waring, C. A. Tibbets, and P. G. Gregory. 1993. Survival of hybrids in a mosaic hybrid zone. Evolution. 47:789-800.
26. Hudson, R. R. 1987. Estimating the recombination parameter of a finite population model without selection. Genet. Res. 50: 245-250.
27. 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.
28. Kelly, J. K., and M. A. Noor. 1996. Speciation by reinforcement: a model derived from studies of Drosophila. Genetics 143: 1485-1497.
29. Kelso, D. 1970. A comparative morphological and ecological study of two species of sea urchins, genus Echinometra in Hawaii. Ph.D. diss., University of Hawaii, Honolulu, HI.
30. Kirkpatrick, M. 2000. Reinforcement and divergence under assortative mating. Proc. R. Soc. Lond. B 267:1649-1655.
31. Kirkpatrick, M., and M. R. Servedio. 1999. The reinforcement of mating preferences on an island. Genetics 151:865-884.
32. Knowlton, N. 1993. Sibling species in the sea. Annu. Rev. Ecol. Syst. 24:189-216.
33. Kulathinal, R. J., and R. S. Singh. 2000. A biogeographic genetic approach for testing the role of reinforcement: the case of Drosophila pseudoobscura and D. persimilis. Evolution 54:210-217.
34. Kumar, S., K. Tamura, I. Jakobsen, and M. Nei. 2000. MEGA: molecular evolutionary genetics analysis. Ver. 2., Pennsylvania State Univ., University Park, PA.
35. Lande, R. 1981. Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. USA 78:3721-3725.
36. Lee, Y.-H., and V. D. Vacquier. 1992. The divergence of species-specific abalone sperm lysins is promoted by positive selection. Biol. Bull. 182:97-104.
37. Lee, Y.-H., T. Ota, and V. D. Vacquier. 1995. Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Mol. Biol. Evol 12:231-238.
38. Levin, D. A. 1985. Reproductive character displacement in Phlox. Evolution 39:1275-1281.
39. Liou, L. W., and T. D. Price. 1994. Speciation by reinforcement of premating isolation. Evolution 48:1451-1459.
40. Littlejohn, M. J., and J. J. Loftus Hills. 1968. And experimental evaluation of premating isolation in the Hyla ewingi complex (Anura: Hylidae). Evolution 22:659-663.
41. Lu, G. Q., and L. Bernatchez. 1998. Experimental evidence for reduced hybrid viability between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis Mitchill). Proc. R. Soc. Lond. B 265:1025-1030.
42. Macnair, M. R., and M. Gardner. 1998. The evolution of edaphic endemics. Pp. 157-171 in D. J. Howard and S. H. Berlocher, eds. Endless forms: species and speciation. Oxford Univ. Press, Oxford, U.K.
43. Maddison, W. P., and D. R. Maddison. 1992. MacClade: analysis of phylogeny and character evolution. Ver. 3. Sinauer Associates, Sunderland, MA.
44. Marshal, D. C., and J. R. Cooley. 2000. Reproductive character displacement and speciation in periodical cicadas, with description of a new species, 13-year Magicicada neotredecim. Evolution 54:1313-1325.
45. Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge, MA.
46. Mead, K. S. 1996. Sex in the surf zone: the effect of hydrodynamic shear stress on the fertilization and early development of free-spawning invertebrates. Ph.D. diss., Stanford University, Stanford, CA.
47. 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.
48. Metz, E. C., G. Gomez-Gutierrez, and V. D. Vacquier. 1998a. Mitochondrial DNA and bindin gene sequence evolution among allopatric species of the sea urchin genus Arbacia. Mol. Biol. Evol 15:185-195.
49. Metz, E. C., R. Robles-Sikisaka, and V. D. Vacquier. 1998b. Non-synonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. Proc. Natl. Acad. Sci. USA 95:10676-10681.
50. Nishihira, M., Y. Sato, Y. Arakaki, and M. Tsuchiya. 1991. Ecological distribution and habitat preference of four types of the sea urchin Echinometra mathaei on the Okinawan coral reefs. Pp. 91-104 in T. Yanagisawa, I. Yasumasu, C. Oguro, N. Suzuki, and T. Motokawa, eds. Biology of echinodermata. Balkema, Rotterdam.
51. Noor, M. A. F., N. A. Johnson, and J. Hey. 2000. Gene flow between Drosophila pseudoobscura and D. persimilis. Evolution 54:2174-2175.
52. Palumbi, S. R. 1992. Marine speciation on a small planet. Trends Ecol. Evol. 7:114-117.
53. _. 1996. What can molecular genetics contribute to marine biogeography? An urchin's tale. J. Exp. Mar. Biol. Ecol. 203:75-92.
54. _. 1999. All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc. Natl. Acad. Sci. USA 96:12632-12637.
55. Palumbi, S. R., and E. M. Metz. 1991. Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol. Biol. Evol. 8:227-239.
56. Palumbi, S. R., A. Martin, S. Romano, W. O. McMillan, L. Stice, and G. Grabowski. 1991. The simple fool's guide to PCR. Special Publication of the Department of Zoology, Univ. of Hawaii, Honolulu, HI.
57. Palumbi, S. R., G. Grabowsky, T. Duda, L. Geyer, and N. Tachino. 1997. Speciation and the evolution of population structure in tropical Pacific sea urchins. Evolution 51:1506-1517.
58. 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.
59. Pigeon, D., A. Chouinard, and L. Bernatchez. 1997. Multiple modes of speciation involved in the parallel evolution of sympatric morphotypes of lake whitefish (Coregonus clupeaformis, Salmonidae). Evolution 51:196-205.
60. Rahman, M. A., T. Uehara, and L. M. Aslan. 2000. Comparative viability and growth of hybrids between two sympatric species of sea urchins (genus Echinometra) in Okinawa. Aquaculture 183:45-56.
61. Rahman, M. A., T. Uehara, and J. S. Pearse. 2001. Hybrids of two closely related tropical sea urchins (genus Echinometra): evidence against postzygotic isolating mechanisms. Biol. Bull. 200:97-106.
62. Rice, W. R. 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232-234.
63. Rice, W. R., and G. W. Salt. 1990. The evolution of reproductive isolation as a correlated character under sympatric conditions: experimental evidence. Evolution 44:1140-1152.
64. Rozas, J., and R. Rozas. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175.
65. Rundle, H. D., and D. Schluter. 1998. Reinforcement of stickleback mate preferences: sympatry breeds contempt. Evolution 52:200-208.
66. Rundle, H. D., L. Nagel, J. W. Boughman, and D. Schluter. 2000. Natural selection and parallel speciation in sympatric sticklebacks. Science 287:306-308.
67. Russo, A. R. 1977. Water flow and the distribution and abundance of Echinoids (genus Echinometra) on an Hawaiian reef. Aust. J. Mar. Freshw. Res. 28:693-702.
68. Sætre, G.-P., T. Moum, S. Bures, M. Král, M. Adamjan, and J. Moreno. 1997. A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387:589-592.
69. Sætre, G.-P., M. Král, S. Bures, and R. Ims. 1999. Dynamics of a clinal hybrid zone and a comparison with island hybrid zones of flycatchers (Ficeduta hypoleuca and F. albicollis). J. Zool. 247:53-64.
70. Schneider, S., D. Roessli, and L. Escoffier. 2000. Arlequin ver. 2.000: A software for population genetics data analysis. Genetics and Biometry Laboratory, Univ. of Geneva, Switzerland.
71. Servedio, M. R. 2000. Reinforcement and the genetics of nonrandom mating. Evolution 54:21-29.
72. Servedio, M. R., and M. Kirkpatrick. 1997. The effects of gene flow on reinforcement. Evolution 51:1764-1772.
73. Simon, C., J. Tang, S. Dalwadi, G. Staley, J. Deniega, and T. R. Unnasch. 2000. Genetic evidence for assortative mating between 13-year cicadas and sympatric "17-year cicadas with 13-year life cycles" provides support for allochronic speciation. Evolution 54:1326-1336.
74. Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236:787-792
75. _. 1991. Inbreeding coefficients and coalescence times. Genet. Res. Camb. 58:167-175.
76. Stockley, P. 1997. Sexual conflict resulting from adaptations to sperm competition. Trends Ecol. Evol. 12:154-159.
77. 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.
78. Swofford, D. L. 2001. PAUP*: phylogenetic analysis using parsimony *and other methods. Ver. 4. Sinauer, Sunderland, MA.
79. Tsaur, S.-C., and C.-I. Wu. 1997. Positive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila. Mol. Biol. Evol 14:544-549.
80. Tsuchiya, M., and M. Nishihira. 1984. Ecological distribution of two types of the sea-urchin, Echinometra mathaei (Blainville), on Okinawan reef flat. Galaxea 3:131-143.
81. Uehara, T., M. Shingaki, and K. Taira. 1986. Taxonomic studies in the sea urchin, genus Echinometra, from Okinawa and Hawaii. Zool. Sci. 3:1114.
82. Uehara, T., H. Asakura, and Y. Arakaki. 1990. Fertilization and hybridization among species of sea urchins. Pp. 305-310 in M. Hoshi and O. Yamashita, eds. Advances in invertebrate reproduction. Vol. 5. Elsevier, New York.
83. Vacquier, V. D., W. J. Swanson, and M. E. Hellberg. 1995. What have we learned about sea urchin sperm bindin? Dev. Growth Differ. 37:1-10.
84. Vacquier, V. D., W. J. Swanson, and Y. H. Lee. 1997. Positive Darwinian selection on two homologous fertilization proteins: What is the selective pressure driving their divergence? J. Mol. Evol. 44:S15-S22.
85. Waage, J. K. 1979. Reproductive character displacement in Calopteryx (Odonata: Calopterygidae). Evolution 33:104-116.
86. Zouros, E., and C. J. D'Entremont. 1980. Sexual isolation among populations of Drosophila mojavensis: response to pressure from a related species. Evolution 34:421-430.