Fine-scale patterns of genetic divergence within and between morphologically variable subspecies of the sea urchin Heliocidaris erythrogramma (Echinometridae)

Biological Journal of the Linnean Society

Volumn 103, Issue 3, 2011, Pages 578-592

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

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Colour variation; Dispersal; Heliocidaris erythrogramma armigera; Life history; Microsatellites; Population structure; Spine morphology

Indexed keywords

COLOR MORPH; DISPERSAL; ECHINODERM; GENE FLOW; GENETIC MARKER; GENETIC VARIATION; LIFE HISTORY TRAIT; LIMESTONE; MARINE ECOSYSTEM; METAMORPHOSIS; MORPHOLOGY; POPULATION STRUCTURE;

AUSTRALIA; WESTERN AUSTRALIA;

ECHINOIDEA; ECHINOMETRIDAE; HELIOCIDARIS ERYTHROGRAMMA;

EID: 79959210292     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2011.01663.x     Document Type: Article

References (71)

1. Addison JA, Hart MW. 2004. Analysis of population genetic structure of the green sea urchin (Strongylocentrotus droebachiensis) using microsatellites. Marine Biology 144: 243-251.
2. Addison JA, Hart MW. 2005. Spawning, copulation and inbreeding coefficients in marine invertebrates. Biology Letters 1: 450-453.
3. Avise JC. 1994. Molecular markers, natural history and evolution. New York, NY: Chapman & Hall.
4. Banks SC, Piggott MP, Williamson JE, Bové U, Holbrook NJ, Beheregaray LB. 2007. Oceanic variability and coastal topography shape genetic structure in a long-dispersing sea urchin. Ecology 88: 3055-3064.
5. Bernardi G, Holbrook SJ, Schmitt RJ, Crane NL, DeMartini E. 2002. Species boundaries, populations and colour morphs in the coral reef three-spot damselfish (Dascyllus trimaculatus) species complex. Proceedings of the Royal Society of London Series B, Biological Sciences 269: 599-605.
6. Billet DSM, Hausen B. 1982. Abyssal aggregations of Kolga hyalina Danielssen and Koren (Echinometra: Holothuroidea) in the northeast Atlantic Ocean: a preliminary report. Deep-Sea Research 29: 799-818.
7. Binks RM, Evans JP, Kennington WJ, Prince J. 2011. Spatial patterns of variation in color and spine shape in the sea urchin Heliocidaris erythrogramma. Invertebrate Biology in press.
8. Binks RM, Lukehurst SS, Garcia-Gonzalez F, Evans JP. 2009. Characterization of microsatellite loci for the Australia sea urchin Heliocidaris erythrogramma. Molecular Ecology Resources 9: 1259-1261.
9. Chapuis MP, Estoup A. 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24: 621-631.
10. Clegg SM, Degnan SM, Moritz C, Estoup A, Kikkawa J, Owens IPF. 2002. Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a passerine bird. Evolution 56: 2090-2099.
11. Cornuet J-M, Luikart G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014.
12. Cresswell GR, Golding TJ. 1980. Observations of a south-flowing current in the southeastern Indian Ocean. Deep-Sea Research 27A: 449-466.
13. Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB. 1994. Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences of the United States of America 91: 3166-3170.
14. Dix TG. 1977. Reproduction in Tasmanian populations of Heliocidaris erythrogramma (Echinodermata: Echinometridae). Australian Journal of Marine and Freshwater Research 28: 509-520.
15. Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611-2620.
16. Evans JP, Garcia-González F, Marshall DJ. 2007. Sources of genetic and phenotypic variance in fertilization rates and larval traits in a sea urchin. Evolution 61: 2832-2838.
17. Excoffier L, Laval G, Schneider S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
18. Feng M, Slawinski D, Beckley LE, Keesing JK. 2010. Retention and dispersal of shelf waters influenced by interactions of ocean boundary current and coastal geography. Marine and Freshwater Research 61: 1259-1267.
19. Hardy OJ, Vekemans X. 2002. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2: 618-620.
20. Harley CDG, Pankey MS, Wares JP, Grosberg RK, Wonham MJ. 2006. Colour polymorphism and genetic structure in the sea star Pisaster ochraceus. Biological Bulletin 211: 248-262.
21. Harriot VJ. 1985. Reproductive biology of three congeneric sea cucumber species, Holothuria atra, H. impatiens and H. edulis, at Heron Reef, Great Barrier Reef. Australian Journal of Marine and Freshwater Research 36: 51-57.
22. Hedgecock D. 1986. Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bulletin of Marine Science 39: 550-564.
23. Johannesson K, Johannesson B, Rolan-Alvarez E. 1993. Morphological differentiation and genetic cohesiveness over a microenvironmental gradient in the marine snail Littorina saxatilis. Evolution 47: 1770-1787.
24. Johnson MS, Black R. 2006. Islands increase genetic subdivision and disrupt patterns of connectivity of intertidal snails in a complex archipelago. Evolution 60: 2498-2506.
25. Kai Y, Nakayama K, Nakabo T. 2002. Genetic differences among three colour morphotypes of the black rockfish, Sebastes inermis, inferred from mtDNA and AFLP analyses. Molecular Ecology 11: 2591-2598.
26. Knowlton N, Weigt LA, Solórzano LA, Mills DK, Bermingham E. 1993. Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science 260: 1629-1632.
27. Laegdsgaard P, Byrne M, Anderson DT. 1991. Reproduction of sympatric populations of Heliocidaris erythrogramma and H. tuberculata (Echinoidea) in New South Wales. Marine Biology 110: 359-374.
28. Lee HJE, Boulding EG. 2009. Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: the effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers. Molecular Ecology 18: 2165-2184.
29. Legeckis R, Cresswell G. 1981. Satellite observations of sea-surface temperature fronts off the coast of western and southern Australia. Deep-Sea Research 28A: 297-306.
30. Lessios HA. 1984. Possible prezygotic reproductive isolation in sea urchin separated by the Isthmus of Panama. Evolution 38: 1144-1148.
31. Lessios HA. 2007. Reproductive isolation between species of sea urchins. Bulletin of Marine Science 81: 191-208.
32. Lessios HA, Cunningham CW. 1990. Gamete incompatibility between species of the sea urchin Echinometra on the two sides of the Isthmus of Panama. Evolution 44: 933-941.
33. Lessios HA, Kessing BD, Pearse JS. 2001. Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55: 955-975.
34. Levitan DR, Fukami H, Jara J, Kline D, McGovern TM, McGhee KE, Swanson CA, Knowlton N. 2004. Mechanisms of reproductive isolation among sympatric broadcast spawning corals of the Monastraea annularis species complex. Evolution 58: 308-323.
35. Luikart G, Allendorf FW, Cornuet J-M, Sherwin WB. 1998. Distortion of allele frequency distributions provides a test for recent population bottlenecks. American Genetic Association 89: 238-247.
36. Luikart G, Cornuet JM. 1998. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conservation Biology 12: 228-237.
37. McMillan WO, Raff RA, Palumbi SR. 1992. Population genetic consequences of developmental evolution in sea urchins (genus Heliocidaris). Evolution 46: 1299-1312.
38. Martínez P, Zardoya R. 2005. Genetic structure of bigeye tuna (Thunnus obesus) in the Atlantic Ocean. Collective Volume of Scientific Papers (ICCAT) 57: 195-205.
39. Medioni E, Lecomte Finiger R, Louveiro N, Planes S. 2001. Genetic and demographic variation among colour morphs of cabrilla sea bass. Journal of Fish Biology 58: 1113-1124.
40. 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.
41. Mortensen T. 1943. A monograph of the Echinoidea III (3). Camarodonta. II. Echinidae, Strongylocentrotidae, Parasaleniidae, Echinometridae. Copenhagen: C.A. Rietzel.
42. Palumbi SR. 1994. Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics 25: 547-572.
43. Palumbi SR. 2004. Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annual Review of Environmental Resources 29: 31-68.
44. Palumbi SR. 2009. Speciation and the evolution of gamete recognition genes: pattern and process. Heredity 102: 66-76.
45. Palumbi SR, Metz EC. 1991. Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Molecular Biology and Evolution 8: 227-239.
46. Peakall R, Smouse PE. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288-295.
47. Pearce A, Pattiaratchi C. 1999. The Capes Current: a summer countercurrent flowing past Cape Leeuwin and Cape Naturaliste, Western Australia. Continental Shelf Research 19: 401-420.
48. Pernet B. 1999. Gamete interactions and genetic differentiation among three sympatric polychaetes. Evolution 53: 435-446.
49. Planes S, Doherty PJ. 1997. Genetic and color interactions at a contact zone of Acanthochromis polyacanthus: a marine fish lacking pelagic larvae. Evolution 51: 1232-1243.
50. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
51. Rahman MA, Uehara T, Aslan LM. 2000. Comparative viability and growth of hybrids between two sympatric species of sea urchins (genus Echinometra) in Okinawa. Aquaculture 183: 45-56.
52. Rahman MA, Uehara T, Lawrence JM. 2005. Growth and heterosis of hybrids of two closely related species of Pacific sea urchins (genus Echinometra) in Okinawa. Aquaculture 245: 121-133.
53. Rahman SM, Uehara T, Pearse JS. 2001. Hybrids of two closely related tropical sea urchins (genus Echinometra): evidence against postzygotic isolating mechanisms. Biological Bulletin 200: 97-106.
54. Raymond M, Rousset F. 1995. Population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248-249.
55. Rice WR. 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.
56. Rousset F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219-1228.
57. Sandoval-Castellanos E, Uribe-Alcocer M, Díaz-Jaimes P. 2010. Population genetic structure of the Humboldt squid (Dosidicus gigas d'Orbigny, 1835) inferred by mitochondrial DNA analysis. Journal of Experimental Marine Biology and Ecology 385: 73-78.
58. Schultz JK, Pyle RL, DeMartini E, Bowen BW. 2007. Genetic connectivity among colour morphs and Pacific archipelagos for the flame angelfish, Centropyge loriculus. Marine Biology 151: 167-175.
59. Sherman CDH, Hunt A, Ayre DJ. 2008. Is life history a barrier to dispersal? Contrasting patterns of genetic differentiation along an oceanographically complex coast. Biological Journal of the Linnean Society 95: 106-116.
60. Simmons LW, Beveridge M, Wedell N, Tregenza T. 2006. Postcopulatory inbreeding avoidance by female crickets only revealed by molecular markers. Molecular Ecology 15: 3817-3824.
61. Slatkin M. 1985. Gene flow in natural populations. Annual Review of Ecology and Evolutionary Systematics 16: 393-430.
62. Slatkin M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457-462.
63. Swanson WJ, Vacquier VD. 2002. The rapid evolution of reproductive proteins. Nature Reviews 3: 137-144.
64. Uehara T, Shingaki M. 1985. Taxonomic studies on the four types of sea urchin, Echinometra mathaei from Okinawa, Japan. Zoological Science 2: 1009.
65. Underwood JN, Smith LD, Van Oppen MJH, Gilmour JP. 2007. Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Molecular Ecology 16: 771-784.
66. Underwood JN, Smith LD, van Oppen MJH, Gilmour JP. 2009. Ecologically relevant dispersal of corals on isolated reefs: implications for managing resilience. Ecological Applications 19: 18-29.
67. Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH. 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology and Evolution 10: 212-217.
68. Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
69. Williams DHC, Anderson DT. 1975. The reproductive system, embryonic development, larval development and metamorphosis of the sea urchin Heliocidaris erythrogramma (Val.) (Echinoidea: Echinometridae). Australian Journal of Zoology 23: 371-403.
70. Zieritz A, Hoffman JI, Amos W, Aldridge DC. 2010. Phenotypic plasticity and genetic isolation-by-distance in the freshwater mussel Unio pictorum (Mollusca: Unionoida). Evolutionary Ecology 24: 923-938.
71. Zigler KS, Raff EC, Popodi E, Raff RA, Lessios HA. 2003. Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57: 2293-2302.