More Than Bindin Divergence: Reproductive Isolation Between Sympatric Subspecies Of A Sea Urchin By Asynchronous Spawning

Evolution

Volumn 66, Issue 11, 2012, Pages 3545-3557

  Binks, Rachel M ^a   Prince, Jane ^a   Evans, Jonathan P ^a   Kennington, W Jason ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Heliocidaris erythrogramma armigera; Reproductive isolation; Speciation

Indexed keywords

CELL SURFACE RECEPTOR; CYTOCHROME C OXIDASE; EGG SURFACE SPERM RECEPTOR; MICROSATELLITE DNA; MITOCHONDRIAL DNA; RNA 16S;

DIVERGENCE; ECHINODERM; GENE EXPRESSION; GREEN ALGA; MITOCHONDRION; PHYLOGENETICS; PROTEIN; REPRODUCTIVE ISOLATION; SPAWNING; SYMPATRY;

ANIMAL; ANTHOCIDARIS; ARTICLE; AUSTRALIA; DNA SEQUENCE; FEMALE; GENETICS; MALE; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; REPRODUCTION; REPRODUCTIVE ISOLATION; SEQUENCE ALIGNMENT; SYMPATRY; TIME;

ANIMALS; ANTHOCIDARIS; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; FEMALE; MALE; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; PHYLOGENY; RECEPTORS, CELL SURFACE; REPRODUCTION; REPRODUCTIVE ISOLATION; RNA, RIBOSOMAL, 16S; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SYMPATRY; TIME FACTORS; WESTERN AUSTRALIA;

AUSTRALIA; WESTERN AUSTRALIA;

ECHINOIDEA; HELIOCIDARIS ERYTHROGRAMMA;

EID: 84868149758     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2012.01700.x     Document Type: Article

References (77)

1. Barluenga, M., K. N. Stölting, W. Salzburger, M. Muschick, and A. Meyer. 2006. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439:719-723.
2. Biermann, C. H. 1998. The molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae). Mol. Biol. Evol. 15:1761-1771.
3. Billet, D. S. M., and B. Hausen. 1982. Abyssal aggregations of Kolga hyalina Danielssen and Koren (Echinometra: Holothuroidea) in the northeast Atlantic Ocean: a preliminary report. Deep-Sea Res. 29:799-818.
4. Binks, R. M. 2012. Investigating the evolutionary significance of morphological variation in the Australian sea urchin Heliocidaris erythrogramma. Ph.D. thesis, School of Animal Biology, University of Western Australia Perth, Western Australia.
5. Binks, R. M., J. P. Evans, W. J. Kennington, and J. Prince. 2011a. Spatial patterns of variation in color and spine shape in the sea urchin Heliocidaris erythrogramma. Invertebr. Biol. 130:161-174.
6. Binks, R. M., J. P. Evans, J. Prince, and W. J. Kennington. 2011b. Fine-scale patterns of genetic divergence within and between morphologically variable subspecies of the sea urchin Heliocidaris erythrogramma (Echinometridae). Biol. J. Linn. Soc. 103:578-592.
7. Clement, M., D. Posada, and K. Crandall. 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9:1657-1660.
8. Cresswell, G. R., and T. J. Golding. 1980. Observations of a south-flowing current in the southeastern Indian Ocean. Deep-Sea Res. 27A:449-466.
9. Danilowicz, B. S. 1995. Spatial patterns of spawning in the coral-reef damselfish Dascyllus albisella. Mar. Biol. 122:145-155.
10. Dix, T. G. 1977. Reproduction in Tasmanian populations of Heliocidaris erythrogramma (Echinodermata: Echinometridae). Aust. J. Mar. Freshw. Res. 28:509-520.
11. Dobzhansky, T. 1970. Genetics of the evolutionary process. Columbia Univ. Press, New York.
12. Evans, J. P., F. Garcia-González, and D. J. Marshall. 2007. Sources of genetic and phenotypic variance in fertilization rates and larval traits in a sea urchin. Evolution 61:2832-2838.
13. Excoffier, L., G. Laval, and S. Schneider. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1:47-50.
14. Feder, J. L., C. A. Chilcote, and G. L. Bush. 1988. Genetic differentiation between sympatric host races of the apple maggot fly Rhagoletis pomonella. Nature 336:61-64.
15. Fitzpatrick, J. L., F. Garcia-Gonzalez, and J. P. Evans. 2010. Linking sperm length and velocity: the importance of intramale variation. Biol. Lett. 6:797-799.
16. Gonor, J. J. 1972. Gonad growth in the sea urchin, Strongylocentrotus purpuratus (Stimpson) (Echinodermata: Echinoidea) and the assumptions of gonad index methods. J. Exp. Mar. Biol. Ecol. 10:89-103.
17. Harriot, V. J. 1985. Reproductive biology of three congeneric sea cucumber species, Holothuria atra, H. impatiens and H. edulis, at Heron Reef, Great Barrier Reef. Aust. J. Mar. Freshw. Res. 36:51-57.
18. Hey, J., and R. Nielsen. 2007. Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc. Natl. Acad. Sci. 104:2785-2790.
19. Jeffery, C. H., R. B. Emlet, and D. T. J. Littlewood. 2003. Phylogeny and evolution of developmental mode in temnopleurid echinoids. Mol. Phylogenet. Evol. 28:99-118.
20. Johnson, M. S., and R. Black. 2006. Islands increase genetic subdivision and disrupt patterns of connectivity of intertidal snails in a complex archipelago. Evolution 60:2498-2506.
21. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
22. Kruse, I., M. Strasser, and F. Thiermann. 2004. The role of ecological divergence in speciation between intertidal and subtidal Scoloplos armiger (Polychaeta, Orbiniidae). J. Sea Res. 51:53-62.
23. Laegdsgaard, P. 1989. The reproduction of two co-occurring species of the sea urchin Heliocidaris in the Sydney region. Honours thesis, University of Sydney, NSW, Australia.
24. Laegdsgaard, P., M. Byrne, and D. T. Anderson. 1991. Reproduction of sympatric populations of Heliocidaris erythrogramma and H. tuberculata (Echinoidea) in New South Wales. Mar. Biol. 110:359-374.
25. Legeckis, R., and G. Cresswell. 1981. Satellite observations of sea-surface temperature fronts off the coast of western and southern Australia. Deep-Sea Res. 28A:297-306.
26. Lessios, H. A. 1984. Possible prezygotic reproductive isolation in sea urchins separated by the Isthmus of Panama. Evolution 38:1144-1148.
27. Lessios, H. A. 2007. Reproductive isolation between species of sea urchins. Bull. Mar. Sci. 81:191-208.
28. Lessios, H. A., and C. W. Cunningham. 1990. Gamete incompatibility between species of the sea urchin Echinometra on the two sides of the Isthmus of Panama. Evolution 44:933-941.
29. 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.
30. Levitan, D. R., H. Fukami, J. Jara, D. Kline, T. M. McGovern, K. E. McGhee, C. A. Swanson, and N. Knowlton. 2004. Mechanisms of reproductive isolation among sympatric broadcast spawning corals of the Monastraea annularis species complex. Evolution 58:308-323.
31. Li, Q., N. P. James, Y. Bone, and B. McGowran. 1999. Palaeoceanographic significance of recent foraminiferal biofacies on the southern shelf of Western Australia: a preliminary study. Palaeogeogr. Palaeoclimatol. Palaeoecol. 147:101-120.
32. Mangubhai, S., and P. L. Harrison. 2009. Extended breeding seasons and asynchronous spawning among equatorial reef corals in Kenya. Mar. Ecol. Prog. Ser. 374:305-310.
33. Mayr, E. 1942. Systematics and the origin of species. Columbia Univ. Press, New York.
34. Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge, MA.
35. McClary, D. J., and M. A. Sewell. 2003. Hybridization in the sea: gametic and developmental constraints on fertilization in sympatric species of Pseudochinus (Echinodermata: Echinoidea). J. Exp. Mar. Biol. Ecol. 284:51-70.
36. McGowran, B., Q. Li, J. Cann, D. Padley, D. M. McKirdy, and S. Shafik. 1997. Biogeographic impact of the Leeuwin current in southern Australia since the late middle Eocene. Palaeogeogr. Palaeoclimatol. Palaeoecol. 136:19-40.
37. McMillan, W. O., R. A. Raff, and S. R. Palumbi. 1992. Population genetic consequences of developmental evolution in sea urchins (genus Heliocidaris) Evolution 46:1299-1312.
38. Metz, E. C., G. Gómez Gutiérrez, and V. 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.
39. 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.
40. Miller, R. L. 1979. Sperm chemotaxis in the Hydromedusae. I. Species-specificity and sperm behavior. Mar. Biol. 53:99-114.
41. Miller, R. L. 1997. Specificity of sperm chemotaxis among Great Barrier Reef shallow-water Holothurians and Ophiuroids. J. Exp. Zool. 279:189-200.
42. Mortensen, T. 1943. A monograph of the Echinoidea. III (3). Camarodonta. II. Echinidae, Strongylocentrotidae, Parasaleniidae, Echinometridae. C.A. Rietzel, Copenhagen, Denmark.
43. Palumbi, S. R. 1994. Genetic divergence, reproductive isolation, and marine speciation. Ann. Rev. Ecol. Syst. 25:547-572.
44. Palumbi, S. R. 2009. Speciation and the evolution of gamete recognition genes: pattern and process. Heredity 102:66-76.
45. 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.
46. 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.
47. Pearse, J. S., and B. F. Phillips. 1968. Continuous reproduction in the Indo-Pacific sea urchin Echinometra mathaei at Rottnest Island, Western Australia. Aust. J. Mar. Freshw. Res. 19:161-172.
48. Pearson, G. A., and E. A. Serrão 2006. Revisiting synchronous gamete release by fucoid algae in the intertidal zone: fertilisation success and beyond? Integr. Comp. Biol. 46:587-597.
49. Peters, J. L., Y. Zhuravlev, I. Fefelov, A. Logie, and K. E. Omland. 2007. Nuclear loci and coalescent methods support ancient hybridization as cause of mitochondrial paraphyly between Gadwall and Falcated Duck (Anas SPP.). Evolution 61:1992-2006.
50. Pennington, J. T. 1985. The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol. Bull. 169:417-430.
51. Pernet, B. 1999. Gamete interactions and genetic differentiation among three sympatric polychaetes. Evolution 53:435-446.
52. Posada, D., and K. Crandall. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-818.
53. Raff, E. C., E. M. Popodi, B. J. Sly, F. R. Turner, J. T. Villinski, and R. A. Raff. 1999. A novel ontogenetic pathway in hybrid embyros between species with different modes of development. Development 126:1937-1945.
54. Rahman, S. M., 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.
55. 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.
56. Riffell, J. A., P. J. Krug, and R. K. Zimmer. 2004. The ecological and evolutionary consequences of sperm chemoattraction. Proc. Natl. Acad. Sci. 101:4501-4506.
57. Rychlik, W. 2007. OLIGO 7 primer analysis software. In A. Yuryev, ed. Methods in molecular biology: PCR primer design. Humana Press, Totiwa, NJ.
58. Sherman, C. D. H., A. Hunt, and D. J. Ayre. 2008. Is life history a barrier to dispersal? Contrasting patterns of genetic differentiation along an oceanographically complex coast. Biol. J. Linn. Soc. 95:106-116.
59. Simmons, L. W., M. Beveridge, N. Wedell, and T. Tregenza. 2006. Postcopulatory inbreeding avoidance by female crickets only revealed by molecular markers. Mol. Ecol. 15:3817-3824.
60. Smith, M. S., S. Collins, and R. A. Raff. 2009. Morphogenetic mechanisms of coelom formation in the direct-developing sea urchin Heliocidaris erythrogramma. Dev. Genes Evol. 219:21-29.
61. Strathman, M. 1987. Reproduction and development of marine invertebrates of the Northern Pacific Coast. Univ. of Washington Press, Seattle, WA.
62. Stuart-Andrews, C. 2005. Spatial and temporal patterns of recruitment of Heliocidaris erythrogramma (Valenciennes, 1846) on the central Western Australian coast. B.Sc. (Honours) thesis, University of Western Australia, Perth, Western Australia.
63. Swanson, W. J., and V. D. Vacquier. 2002. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3:137-144.
64. Swofford, D. L. 2003. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA.
65. 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.
66. Toro, J. E., R. J. Thompson, and D. J. Innes. 2002. Reproductive isolation and reproductive output in two sympatric mussel species (Mytilis edulis, M. trossulus) and their hybrids from Newfoundland. Mar. Biol. 141:897-909.
67. 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.
68. Williams, D. H. C., and D. T. Anderson. 1975. The reproductive system, embryonic development, larval development and metamorphosis of the sea urchin Heliocidaris erythrogramma (Val.) (Echinoidea: Echinometridae). Aust. J. Zool. 23:371-403.
69. Wilson, J. R., and P. L. Harrison. 2003. Spawning patterns of scleractinian corals at the Solitary Islands-a high latitude coral community in eastern Australia. Mar. Ecol. Prog. Ser. 260:115-123.
70. Wilson, K. A., M. E. Andrews, F. R. Turner, and R. A. Raff. 2005. Major regulatory factors in the evolution of development: the roles of goosecoid and Msx in the evolution of the direct-developing sea urchin Heliocidaris erythrogramma. Evol. Dev. 7:416-428.
71. Won, Y.-J., and J. Hey. 2005. Divergence population genetics of chimpanzees. Mol. Biol. Evol. 22:297-307.
72. Zar, J. H. 1984. Biostatistical analysis. Prentice Hall Inc., New Jersey.
73. Zigler, K. S., and H. A. Lessios. 2003a. 250 million years of bindin evolution. Biol. Bull. 205:8-15.
74. Zigler, K. S., and H. A. Lessios. 2003b. Evolution of bindin in the Pantropical sea urchin Tripneustes: comparisons to bindin of other Genera. Mol. Biol. Evol. 20:220-231.
75. Zigler, K. S., and H. A. Lessios. 2004. Speciation on the coasts of the New World: phylogeography and the evolution of bindin in the sea urchin genus Lytechinus. Evolution 58:1225-1241.
76. 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.
77. 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.