Comparison of gamete compatibility between two blue mussel species in sympatry and in allopatry

Biological Bulletin

Volumn 214, Issue 1, 2008, Pages 57-66

  Slaughter, Christin ^a,c   McCartney, Michael A ^a   Yund, Philip O ^b  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^b UNIVERSITY OF NEW ENGLAND   (United States)

^c NEW MEXICO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPATRY; BIVALVE; COMPARATIVE STUDY; ESTIMATION METHOD; GAMETE; HYBRIDIZATION; HYPOTHESIS TESTING; IDENTIFICATION METHOD; INTROGRESSION; SPERM; SYMPATRY;

COBSCOOK BAY; MAINE; NORTH AMERICA; UNITED STATES;

MYTILUS EDULIS;

EID: 39449091604     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.2307/25066660     Document Type: Article

References (75)

1. Bates, J. A., and D. J. Innes. 1995. Genetic variation among populations of Mytilus spp. in eastern Newfoundland. Mar. Biol. 124: 417-424.
2. Bayne, B. L. 1965. Growth and the delay of metamorphosis of the larvae of Mytilus edulis (L.). Ophelia 2: 1-47.
3. Beynon, C. M., and D. O. F. Skibinski. 1996. The evolutionary relationships between the species of mussel (Mytilus) based on anonymous DNA polymorphisms. J. Exp. Mar. Biol. Ecol. 203: 1-10.
4. Biermann, C. H. 1998. The molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae). Mol. Biol. Evol. 15: 1761-1771.
5. Bigelow, R. S. 1965. Hybrid zones and reproductive isolation. Evolution 19: 449-458.
6. Clark, N. L., J. E. Aagaard, and W. J. Swanson. 2006. Evolution of reproductive proteins from animals and plants. Reproduction 131: 11-22.
7. Comesaña, A. S., J. E. Toro, D. J. Innes, and R. J. Thompson. 1999. A molecular approach to the ecology of a mussel (Mytilis edulis-M. trossulus) hybrid zone on the east coast of Newfoundland, Canada. Mar. Biol. 133: 213-221.
8. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer Associates, Sunderland, MA.
9. Denny, M. W. 1988. Biology and Mechanics of the Wave-Swept Environment. Princeton University Press, Princeton, NJ.
10. Denny, M. W., and M. F. Shibata. 1989. Consequences of surf-zone turbulence for settlement and external fertilization. Am. Nat. 134: 859-889.
11. Felsenstein, J. 1981. Skepticism toward Santa Rosalia, or why are there so few kinds of animals? Evolution 35: 124-138.
12. Gardner, J. P. A. 1994. The structure and dynamics of naturally occurring hybrid Mytilus edulis Linneaus, 1758 and Mytilus galloprovincialis Lamarck, 1819 (Bivalvia: Mollusca) populations: a review and interpretation. Arch. Hydrobiol. Supp. 99: 37-71.
13. Gardner, J. P. A., and R. J. Thompson. 2001. The effects of coastal and estuarine conditions on the physiology and survivorship of the mussels Mytilus edulis, M. trossulus and their hybrids. J. Exp. Mar. Biol. Ecol. 265: 119-140.
14. 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.
15. Geyer, L. B., and S. R. Palumbi. 2005. Conspecific sperm precedence in two species of tropical sea urchins. Evolution 59: 97-105.
16. Geyer, W. R., R. P. Signell, D. A. Fong, J. Wang, D. M. Anderson, and B. A. Keafer. 2005. The freshwater transport and dynamics of the western Maine coastal current. Cont. Shelf Res. 24: 1339-1357.
17. Gosling, E. M. 1992. Genetics of Mytilus. Pp. 309-382 in The Mussel Mytilus: Ecology, Physiology, Genetics and Culture, E. Gosling, ed. Elsevier, Amsterdam.
18. Harper, F. M., E. A. Pomerlau, and P. D. Rawson. 2005. Species-specific egg-borne proteins in the blue mussels, Mytilus edulis and M. trossulus. Integr. Comp. Biol. 45: 1142-1142.
19. Heath, D. D., P. D. Rawson, and T. J. Hilbish. 1995. PCR-based nuclear markers identify alien blue mussel (Mytilus spp.) genotypes on the west coast of Canada. Can. J. Fish Aquat. Sci. 52: 2621-2627.
20. Hellberg, M. E., and V. D. Vacquier. 1999. Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol. Biol. Evol. 16: 839-848.
21. Hilbish, T. J., A. Mullinax, S. I. Dolven, A. Meyer, R. K. Koehn, and P. D. Rawson. 2000. Origin of the antitropical distribution pattern in marine mussels (Mytilus spp.): routes and timing of transequatorial migration. Mar. Biol. 136: 69-77.
22. Howard, D. J. 1993. Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. Pp. 46-69 in Hybrid Zones and the Evolutionary Process, R. G. Harrison, ed. Oxford University Press, New York.
23. Howard, D. J. 1999. Conspecific sperm and pollen precedence and speciation. Annu. Rev. Ecol. Syst. 30: 109-132.
24. Howard, D. J., M. Reece, P. G. Gregory, J. Chu, and M. L. Cain. 1998. The evolution of barriers to fertilization between closely related organisms. Pp. 279-288 in Endless Forms: Species and Speciation, D. Howard and S. Berlocher, eds. Oxford University Press, Oxford.
25. Innes, D. J., and J. A. Bates. 1999. Morphological variation of Mytilus edulis and Mytilus trossulus in eastern Newfoundland. Mar. Biol. 133: 691-699.
26. Jiggins, C. D., and J. Mallet. 2000. Bimodal hybrid zones and speciation. Trends Ecol. Evol. 15: 250-255.
27. Koehn, R. K., R. Milkman, and J. B. Mitton. 1976. Population genetics of marine pelecypods. IV. Selection, migration and genetic differentiation in the blue mussel, Mytilus edulis. Evolution 30: 2-32.
28. Koehn, R. K., J. G. Hall, D. J. Innes, and A. J. Zera. 1984. Genetic differentiation of Mytilus edulis in eastern North America. Mar. Biol. 79: 117-126.
29. 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.
30. Lessios, H. A., and J. S. Pearse. 1996. Hybridization and introgression between Indo-Pacific species of Diadema. Mar. Biol. 126: 715-723.
31. Levitan, D. R. 1996. Effects of gamete traits on fertilization in the sea and the evolution of sexual dimorphism. Nature 382: 153-155.
32. Levitan, D. R. 1998. Does Bateman's principle apply to broadcast-spawning organisms? Egg traits influence in situ fertilization rates among congeneric sea urchins. Evolution 53: 1043-1056.
33. Levitan, D. R. 2002a. Density-dependent selection on gamete traits in three congeneric sea urchins. Ecology 83: 464-479.
34. Levitan, D. R. 2002b. The relationship between conspecific fertilization success and reproductive isolation among three congeneric sea urchins. Evolution 56: 1599-1609.
35. Liou, L. W., and T. D. Price. 1994. Speciation by reinforcement of premating isolation. Evolution 48: 1451-1459.
36. Mallet, A. L., and C. E. Carver. 1995. Comparative growth and survival patterns of Mytilus trossulus and M. edulis in Atlantic Canada. Can. J. Fish. Aquat. Sci. 52: 1873-1880.
37. Maloy, A. P., B. J. Barber, and P. D. Rawson. 2003a. Gametogenesis in a sympatric population of blue mussels, Mytilus edulis and Mytilus trossulus, from Cobscook Bay (USA). J. Shellfish Res. 22: 119-123.
38. Maloy, A. P., B. J. Barber, and P. D. Rawson. 2003b. Gametogenesis in a sympatric population of blue mussels, Mytilus edulis and Mytilus trossulus, from Cobscook Bay (USA). J. Shellfish Res. 22: 119-123.
39. Marshall, J. L., M. L. Arnold, and D. J. Howard. 2002. Reinforcement: the road not taken. Trends Ecol. Evol. 17: 558-563.
40. 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.
41. McCartney, M. A., and H. A. Lessios. 2004. Adaptive evolution of sperm bindin tracks egg incompatibility in neotropical sea urchins of the genus Echinometra. Mol. Biol. Evol. 21: 732-745.
42. McCartney, M. A., and T. G. Lima. 2007. Massive introgression of gamete recognition alleles in a blue mussel hybrid zone. Abstract: Society for Integrative And Comparative Biology, 2007 Annual Meeting, Phoenix, AZ, January 3-7, 2007. [Online] Available: http://sicb.org/meetings/2007/schedule/ abstractdetails.php3?id=710 [11 Nov 2007]
43. McDonald, J. H., R. Seed, and R. K. Koehn. 1991. Allozymes and morphometric characters of three species of Mytilus in the northern and southern hemispheres. Mar. Biol. 111: 323-334.
44. 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.
45. Owen, B., J. H. McLean, and R. J. Meyer. 1971. Hybridization in the eastern Pacific abalones (Haliotis). Nat. Hist. Mus. Los Angel. Cty. Sci. Bull. 9: 1-37.
46. Palumbi, S. R. 1998. Species formation and the evolution of gamete recognition loci. Pp. 271-278 in Endless Forms: Species and Speciation, D. J. Howard and S. H. Berlocher, eds. Oxford University Press, New York.
47. Palumbi, S. R. 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.
48. Palumbi, S. R., and E. C. Metz. 1991. Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol. Biol. Evol. 8: 227-239.
49. Pettigrew, N. R., D. W. Townsend, H. Xue, J. P. Wallinga, P. J. Brickley, and R. D. Hetland. 1998. Observations of the Eastern Maine Coastal Current and its offshore extensions in 1994. J. Geophys. Res: Oceans 103: 30623-30639.
50. Rawson, P. D., and T. J. Hilbish. 1995. Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex. Mol. Biol. Evol. 12: 893-901.
51. Rawson, P. D., and T. J. Hilbish. 1998. Asymmetric introgression of mitochondrial DNA among European populations of blue mussels (Mytilus spp.). Evolution 52: 100-108.
52. Rawson, P. D., K. L. Joyner, K. Meetze, and T. J. Hilbish. 1996. Evidence of intragenic recombination within a novel genetic marker that distinguishes mussels in the Mytilus edulis species complex. Heredity 77: 599-607.
53. Rawson, P. D., S. Hayhurst, and B. Vanscoyoc. 2001. Species composition of blue mussel populations in the northeastern Gulf of Maine. J. Shellfish Res. 20: 31-38.
54. Rawson, P. D., C. Slaughter, and P. O. Yund. 2003. Patterns of gamete incompatibility between the blue mussels Mytilus edulis and M. trossulus. Mar. Biol. 143: 317-325.
55. Rawson, P. D., P. O. Yund, and S. M. Lindsay. 2007. Comment on "Divergent induced responses to an invasive predator in marine mussel populations." Science 316: 53.
56. Rice, W. R., and B. Holland. 1997. The enemies within: intergenomic conflict, interlocus contest evolution (ICE) and the intraspecific Red Queen. Behav. Ecol. Sociobiol. 41: 1-10.
57. Riginos, C., and C. W. Cunningham. 2005. Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Mol. Ecol. 14: 381-400.
58. Riginos, C., and J. H. McDonald. 2003. Positive selection on an acrosomal sperm protein, M7 lysin, in three species of the mussel genus Mytilus. Mol. Biol. Evol. 20: 200-207.
59. Saavedra, C., D. T. Stewart, R. R. Stanwood, and E. Zouros. 1996. Species-specific segregation of gender-associated mitochondrial DNA types in an area where two mussel species (Mytilus edulis and M. trossulus) hybridize. Genetics 143: 1359-1367.
60. Sambrook, J., and D. W. Russell. 2000. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
61. Servedio, M. R., and M. A. F. Noor. 2003. The role of reinforcement in speciation: theory and data. Annu. Rev. Ecol. Syst. 34: 339-364.
62. Servedio, M. R., and M. Kirkpatrick. 1997. The effects of gene flow on reinforcement. Evolution 51: 1764-1772.
63. Slaughter, C. 2005. The role of geography in the evolution of gamete incompatibility in hybridizing blue mussels. Master's thesis, University of North Carolina, Wilmington.
64. Sokal, R. R., and F. J. Rohlf. 1994. Biometry. W. H. Freeman, New York.
65. Springer, S. A., and B. J. Crespi. 2007. Adaptive gamete-recognition divergence in a hybridizing Mytilus population. Evolution 61: 772-783.
66. Swanson, W. J., and V. D. Vacquier. 2002. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3: 137-144.
67. Takagi, T., A. Nakamura, R. Deguchi, and K. I. Kyozuka. 1994. Isolation, characterization, and primary structure of three major proteins obtained from Mytilus edulis sperm. J. Biochem. 116: 598-605.
68. Toro, J., D. J. Innes, and R. J. Thompson. 2004. Genetic variation among life-history stages of mussels in a Mytilus edulis-M. trossulus hybrid zone. Mar. Biol. 145: 713-725.
69. 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.
70. Vermeij, G. J. 1991. Anatomy of an invasion: the trans-Arctic interchange. Paleobiology 17: 281-307.
71. Vogel, H., G. Czihak, P. Chang, and W. Wolf. 1982. Fertilization kinetics of sea urchin eggs. Math. Biosci. 58: 189-216.
72. Wilhelm, R., and T. J. Hilbish. 1998. Assessment of natural selection in a hybrid population of mussels: evaluation of exogenous vs endogenous selection models. Mar. Biol. 131: 505-514.
73. Zigler, K. S., and H. A. Lessios. 2003. 250 million years of bindin evolution. Biol. Bull. 205: 8-15.
74. Zigler, K. S., M. A. McCartney, D. R. Levitan, and H. A. Lessios. 2005. Sea urchin bindin divergence predicts gamete compatibility. Evolution 59: 2399-2404.
75. Zouros, E., A. O. Ball, C. Saavedra, and K. R. Freeman. 1994. An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc. Natl. Acad. Sci. USA 91: 7463-7467.