The genetic structure of intertidal populations of two species of nudibranch molluscs with planktotrophic and pelagic lecithotrophic larval stages: Are pelagic larvae 'for' dispersal?

Journal of Experimental Marine Biology and Ecology

Volumn 228, Issue 1, 1998, Pages 1-28

  Todd, Christopher D ^a   Lambert, Walter J ^a,b   Thorpe, John P ^c  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b Wabash College   (United States)

^c NONE

Author keywords

Allozyme; Dispersal; F statistics; Genetic differentiation; Isolation by distance; Larva; Nudibranch

Indexed keywords

COLONIZATION; GENETIC STRUCTURE; INTERTIDAL COMMUNITY; INVERTEBRATE; LARVAL TRANSPORT;

ARTICLE; GENE FREQUENCY; GENE STRUCTURE; LARVA; LARVAL DEVELOPMENT; LIFE CYCLE; MOLLUSC; NONHUMAN; POPULATION GENETICS; POPULATION RESEARCH; STATISTICAL ANALYSIS;

UNITED KINGDOM;

ADALARIA PROXIMA; GASTROPODA; GONIODORIS NODOSA;

EID: 0032189734     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-0981(98)00005-7     Document Type: Article

References (100)

1. Anon., 1974. West coast of Scotland Pilot, N.P. 66, 11th ed. The Hydrographer of the Navy.
2. Anon., 1983. Admiralty Tidal Stream Atlas. North Coast of Ireland and West Coast of Scotland N.P. 218, 4th ed. The Hydrographic Department, Taunton.
3. Arntz, W.E., Brey, T., Gallardo, V.A., 1994. Antarctic zoobenthos. Oceanogr. Mar. Biol. Ann. Rev. 32, 241-304.
4. Ayre, D.J., 1990. Population subdivision in Australian temperate marine invertebrates: larval connections versus historical factors. Aust. J. Ecol. 15, 403-411.
5. Ayre, D.J., 1995. Localized adaptation of sea anemone clones: evidence from transplantation over two spatial scales. J. Anim. Ecol. 64, 186-206.
6. Ayre, D.J., Dufty, S., 1994. Evidence for restricted gene flow in the viviparous coral Seriatopora hystrix on Australia's Great Barrier Reef. Evolution 48, 1183-1201.
7. Benzie, J.A.H., 1992. Review of the genetics, dispersal and recruitment of crown-of-thorns starfish (Acanthaster planci). Aust. J. Mar. Freshwater Res. 43, 597-610.
8. Benzie, J.A.H., 1994. Patterns of gene flow in the Great Barrier Reef and Coral Sea. In: Beaumont, A.R. (Ed.), Genetics and Evolution of Aquatic Organisms. Chapman and Hall, pp. 67-79.
9. Benzie, J.A.H., Williams, S.T., 1997. Genetic structure of giant clam (Tridacna maxima) populations in the west Pacific is not consistent with dispersal by present-day ocean currents. Evolution 51, 768-783.
10. Bingham, B.L., Young, C.M., 1991. Larval behavior of the ascidian Ecteinascidia turbinata Herdman; an in situ experimental study of the effects of swimming on dispersal. J. Exp. Mar. Biol. Ecol. 145, 189-204.
11. Black, K.P., 1993. The relative importance of local retention and inter-reef dispersal of neutrally buoyant material on coral reefs. Coral Reefs 12, 43-53.
12. Boileau, M.G., Hebert, P.D.N., Schwartz, S.S., 1992. Nonequilibrium gene frequency divergence: persistent founder effects in natural populations. J. Evol. Biol. 5, 25-39.
13. Borsa, P., Jarne, P., Belkhir, K., Bonhomme, F., 1994. Genetic structure of the palourde Ruditapes decussatus L. in the Mediterranean. In: Beaumont, A.R. (Ed.), Genetics and Evolution of Aquatic Organisms. Chapman and Hall, pp. 103-113.
14. Bulnheim, H.-P., Scholl, A., 1986. Genetic differentiation between populations of Talitrus saltator and Talorchestia deshayesii (Crustacea: Amphipoda) from coastal areas of the north-western European continent. Mar. Biol. 92, 525-536.
15. Burton, R.S., 1983. Protein polymorphisms and genetic differentiation of marine invertebrate populations. Mar. Biol. Lett. 4, 193-206.
16. Burton, R.S., 1986. Evolutionary consequences of restricted gene flow among natural populations of the copepod Tigriopus californicus. Bull. Mar. Sci. 39, 526-535.
17. Burton, R.S., 1997. Genetic evidence for long term persistence of marine invertebrate populations in an ephemeral environment. Evolution 51, 993-998.
18. Carvalho, G.R., 1989. Microgeographic genetic differentiation and dispersal capacity in the intertidal isopod, Jaera albifrons Leach. In: Ryland, J.S., Tyler, P.A. (Eds.), Reproduction, Genetics and Distribution of Marine Organisms. Olsen and Olsen, Fredensborg, Denmark, pp. 265-271.
19. Colgan, D.J., 1981. Spatial and temporal variation in the genotypic frequencies of the mussel Brachidontes rostratus. Heredity 46, 197-208.
20. Davis, A.R., Butler, A.J., 1989. Direct observations of larval dispersal in the colonial ascidian Podoclavella moluccensis Sluiter: evidence for closed populations. J. Exp. Mar. Biol. Ecol. 127, 189-203.
21. Day, R., McEdward, L., 1984. Aspects of the physiology and ecology of pelagic larvae of marine benthic invertebrates. In: Steidinger, K.A., Walker, L.M. (Eds.), Marine Plankton Life Cycle Strategies. CRC Press, Boca Raton, FL, pp. 93-120.
22. Duffy, J.E., 1993. Genetic population structure in two tropical sponge-dwelling shrimps that differ in dispersal potential. Mar. Biol. 116, 459-470.
23. Fisk, D.A., Harriott, V.J., 1990. Spatial and temporal variation in coral recruitment on the Great Barrier Reef: implications for dispersal hypotheses. Mar. Biol. 107, 485-490.
24. Fuller, I., Baxter, J.M., 1994. The biology of rocky and sedimentary shores around the Scottish islands. In: Baxter, J.M., Usher, M. (Eds.), The Islands of Scotland: A Living Marine Heritage. HMSO publications, pp. 128-143.
25. Gaines, S.D., Bertness, M.D., 1992. Dispersal of juveniles and variable recruitment in sessile marine species. Nature 360, 579-580.
26. Goudet, J., De Meeüs, T., Day, A.J., Gliddon, C.J., 1994. The different levels of population structuring of the dogwhelk, Nucella lapillus, along the south Devon coast. In: Beaumont, A.R. (Ed.), Genetics and Evolution of Aquatic Organisms. Chapman and Hall, pp. 81-95.
27. Grahame, J., Branch, G.M., 1985. Reproductive patterns of marine invertebrates. Oceanogr. Mar. Biol. Ann. Rev. 23, 373-398.
28. Grant, W.S., Utter, F.M., 1988. Genetic heterogeneity on different geographic scales in Nucella lamellosa (Prosobranchia, Thaididae). Malacologia 28, 275-287.
29. Hedgecock, D., 1986. Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bull. Mar. Sci. 39, 550-564.
30. Hellberg, M.E., 1996. Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution 50, 1167-1175.
31. Highsmith, R.C., 1985. Floating and algal rafting as potential dispersal mechanisms in brooding invertebrates. Mar. Ecol. Prog. Ser. 25, 169-179.
32. Hilbish, T.J., 1985. Demographic and temporal structure of an allele frequency cline in the mussel Mytilus edulis. Mar. Biol. 86, 163-171.
33. Hunt, A., 1993. Effects of contrasting patterns of larval dispersal on the genetic connectedness of local populations of two intertidal starfish, Patiriella calcar and P. exigua. Mar. Ecol. Prog. Ser. 92, 179-186.
34. Hunt, A., Ayre, D.J., 1989. Population structure in the sexually reproducing sea anemone Oulactis muscosa. Mar. Biol. 102, 537-544.
35. Jablonski, D., Lutz, R.A., 1983. Larval ecology of marine invertebrates: paleobiological implications. Biol. Rev. 58, 21-89.
36. Jackson, G.A., Strathmann, R.R., 1981. Larval mortality from offshore mixing as a link between precompetent and competent periods of development. Am. Natur. 118, 16-26.
37. Janson, K., 1987. Allozyme and shell variation in two marine snails (Littorina, Prosobranchia) with different dispersal abilities. Biol. J. Linn. Soc. 30, 245-256.
38. Janson, K., Ward, R.T., 1984. Microgeographic variation in allozyme and shell characters in Littorina saxatilis Olivi (Prosobranchia: Littorinidae). Biol. J. Linn. Soc. 22, 289-307.
39. Johannesson, K., 1988. The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)? Mar. Biol. 99, 507-513.
40. Johannesson, K., 1992. Genetic variability and large scale differentiation in two species of littorinid gastropods with planktotrophic development, Littorina littorea (L.) and Melaraphe (Littorina) neritoides (L.) (Prosobranchia: Littorinacea), with notes on a mass occurrence of M. neritoides in Sweden. Biol. J. Linn. Soc. 47, 285-299.
41. Johannesson, K., Warmoes, T., 1990. Rapid colonization of Belgian breakwaters by the direct developer, Littorina saxatilis (Olivi) (Prosobranchia, Mollusca). In: Johannesson, K., Raffaelli, D.G., Hannaford Ellis, C.J. (Eds.), Progress in Littorinid and Muricid Biology. Kluwer Academic, Belgium, pp. 99-108.
42. Johnson, M.S., Black, R., 1982. Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Mar. Biol. 70, 157-164.
43. Johnson, M.S., Black, R., 1984. Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 38, 1371-1383.
44. Johnson, M.S., Threlfall, T.J., 1987. Fissiparity and population genetics of Coscinasterias calamaria. Mar. Biol. 93, 517-525.
45. Jokiel, P.L., 1990. Transport of reef corals into the Great Barrier Reef. Nature 347, 665-667.
46. Kempf, S.C., Todd, C.D., 1989. Feeding potential in the lecithotropic larvae of Adalaria proxima and Tritonia hombergi: an evolutionary perspective. J. Mar. Biol. Assn, U.K. 69, 659-682.
47. Knowlton, N., Keller, B.D., 1986. Larvae which fall far short of their potential: highly localized recruitment in an alpheid shrimp with extended larval development. Bull. Mar. Sci. 39, 213-223.
48. Koehn, R.K., Milkman, R., Mitton, J.B., 1976. Population genetics of marine pelecypods. IV. Selection, migration and genetic differentiation in the blue mussel Mytilus edulis. Evolution 30, 2-32.
49. Kwast, K.E., Foltz, D.W., Stickle, W.B., 1990. Population genetics and systematics of the Leptasterias hexactis (Echinodermata: Asteroidea) species complex. Mar. Biol. 105, 477-489.
50. Levin, L.A., 1990. A review of methods for labeling and tracking marine invertebrate larvae. Ophelia 32, 115-144.
51. Levinton, J.S., Suchanek, T.H., 1978. Geographic variation, niche breadth and genetic differentiation at different geographic scales in the mussels Mytilus californianus and Mytilus edulis. Mar. Biol. 49, 363-375.
52. Liu, L.L., Foltz, D.W., Stickle, W.B., 1991. Genetic population structure of the southern oyster drill Stramonita (= Thais) haemastoma. Mar. Biol. 111, 71-79.
53. MacLeod, J.A.A., Thorpe, J.P., Duggan, N.A., 1985. A biochemical genetic study of population structure in queen scallop (Chlamys opercularis) stocks in the northern Irish Sea. Mar. Biol. 87, 77-82.
54. Manly, B.F.J., 1985. The Statistics of Natural Selection on Animal Populations. Chapman and Hall, London.
55. Meehan, B.W., Carlton, J.T., Wenne, R., 1989. Genetic affinities of the bivalve Macoma balthica from the Pacific coast of North America: evidence for recent introduction and historical distribution. Mar. Biol. 102, 235-241.
56. Mitton, J.B., Berg, C.J., Orr, K.S., 1989. Population structure, larval dispersal, and gene flow in the queen conch Strombus gigas, of the Caribbean. Biol. Bull. 177, 356-362.
57. Palmer, A.R., Strathmann, R.R., 1981. Scale of dispersal in varying environments and its implication for life history of marine invertebrates. Oecologia 48, 308-318.
58. Palumbi, S.R., 1992. Marine speciation on a small planet. Trends Ecol. Evol. 7, 114-118.
59. Parsons, K.E., 1996. The genetic effects of larval dispersal depend upon spatial scale and habitat characteristics. Mar. Biol. 126, 403-414.
60. Pechenik, J.A., 1990. Delayed metamorphosis by larvae of benthic marine invertebrates: does it occur? Is there a price to pay? Ophelia 32, 63-94.
61. Prince, J.D., Sellers, T.L., Ford, W.B., Talbot, S.R., 1987. Experimental evidence for limited dispersal of haliotid larvae (genus Haliotis; Mollusca: Gastropoda). J. Exp. Mar. Biol. Ecol. 106, 243-263.
62. Ricker, W.E., 1973. Linear regressions in fishery research. J. Fish. Res. Bd. Can. 30, 409-434.
63. Sammarco, P.W., Andrews, J.C., 1988. Localized dispersal and recruitment in Great Barrier Reef corals: the Helix experiment. Science 239, 1422-1424.
64. Sammarco, P.W., Andrews, J.C., 1989. The Helix experiment: differential localized dispersal and recruitment patterns in Great Barrier Reef corals. Limnol. Oceanogr. 34, 896-912.
65. Scheltema, R.S., 1986. Long distance dispersal by planktonic larvae of shoal-water benthic invertebrates among central Pacific islands. Bull. Mar. Sci. 39, 241-256.
66. Shepherd, S.A., Lowe, D., Partington, D., 1992. Studies on southern Australian abalone (genus Haliotis) XIII: larval dispersal and recruitment. J. Exp. Mar. Biol. Ecol. 164, 247-260.
67. Skibinski, D.O.F., Beardmore, J.A., Cross, T.F., 1983. Aspects of the population genetics of Mytilus (Mytilidae; Mollusca). Biol. J. Linn. Soc. 19, 137-183.
68. Slatkin, M., 1987. Gene flow and the geographic structure of natural populations. Science 236, 787-792.
69. Slatkin, M., 1993. Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47, 264-279.
70. Slatkin, M., 1994. Cladistic analysis of DNA sequence data from subdivided populations. In: Real, L.A. (Ed.), Ecological Genetics. Princeton University Press, Princeton, NJ, pp. 18-34.
71. Slatkin, M., Maddison, W.P., 1990. Detecting isolation by distance using phylogenies of genes. Genetics 126, 249-260.
72. Strathmann, R.R., 1974. The spread of sibling larvae of sedentary marine invertebrates. Am. Natur. 108, 29-44.
73. Strathmann, R.R., 1980. Why does a larva live so long? Paleobiology 6, 373-376.
74. Strathmann, R.R., 1985. Feeding and nonfeeding larval development and life history evolution in marine invertebrates. Ann. Rev. Ecol. Syst. 16, 339-361.
75. Strathmann, R.R., 1986. What controls the type of larval development? Summary statement for the evolutionary session. Bull. Mar. Sci. 39, 616-622.
76. Strathmann, R.R., 1990. Why life histories evolve differently in the sea. Am. Zool. 30, 197-207.
77. Strathmann, R.R., 1993. Hypotheses on the origins of marine larvae. Ann. Rev. Ecol. Syst. 24, 89-117.
78. Sutherland, J.P., Karlson, R.H., 1977. Development and stability of the fouling community at Beaufort North Carolina. Ecol. Monogr. 47, 425-446.
79. Svane, I., Young, C.M., 1989. The ecology and behaviour of ascidian larvae. Oceanogr. Mar. Biol. Ann. Rev. 27, 45-90.
80. Theisen, B.F., 1978. Allozyme clines and evidence of strong selection in three loci in Mytilus edulis L. (Bivalvia) from Danish waters. Ophelia 17, 135-142.
81. Thorson, G., 1946. Reproduction and larval development of Danish marine bottom invertebrates. Medd. Komm. Danm. Fisk-og Havenders, ser. Plankton 4, 1-523.
82. Todd, C.D., 1981. The ecology of nudibranch molluscs. Oceanogr. Mar. Biol. Ann. Rev. 19, 141-234.
83. Todd, C.D., 1985. Reproductive strategies of north-temperate rocky shore invertebrates. In: Moore, P.G., Seed, R. (Eds.), The Ecology of Rocky Coasts. Hodder and Stoughton, London, pp. 203-219.
84. Todd, C.D., Havenhand, J.N., Thorpe, J.P., 1988. Genetic differentiation, pelagic larval transport and gene flow between local populations of the intertidal marine mollusc Adalaria proxima (Alder and Hancock). Funct. Ecol. 2, 441-451.
85. Todd, C.D., Bentley, M.G., Havenhand, J.N., 1991. Larval metamorphosis of the opisthobranch mollusc Adalaria proxima (Gastropoda: Nudibranchia): the effects of choline and elevated potassium ion concentration. J. Mar. Biol. Assn, U.K. 71, 53-72.
86. Todd, C.D., Lambert, W.J., Thorpe, J.P., 1994. The genetic structure of intertidal populations of two species of mollusc on the Scottish west coast: some biogeographic considerations and an assessment of realized larval dispersal. In: Baxter, J.M., Usher, M. (Eds.), The Islands of Scotland: A Living Marine Heritage. HMSO publications, pp. 67-87.
87. Underwood, A.J., Fairweather, P.G., 1989. Supply-side ecology and benthic marine assemblages. Trends Ecol. Evol. 4, 16-20.
88. Väinölä, R., Varvio, S.-L., 1989. Biosystematics of Macoma balthica in northwestern Europe. In: Ryland, J.S., Tyler, P.A. (Eds.), Reproduction, Genetics and Distribution of Marine Organisms. Olsen and Olsen, Fredensborg, Denmark, pp. 309-316.
89. Wade, M.J., McCauley, D.E., 1988. Extinction and recolonization: their effects on the genetic differentiation of local populations. Evolution 42, 995-1005.
90. Ward, R.D., 1990. Biochemical genetic variation in the genus Littorina (Prosobranchia: Mollusca). Hydrobiologia 193, 53-69.
91. Ward, R.D., Warwick, T., 1980. Genetic differentiation in the molluscan species Littorina rudis and Littorina arcana (Prosobranchia: Littorinidae). Biol. J. Linn. Soc. 14, 417-428.
92. Watts, R.J., Johnson, M.S., Black, R., 1990. Effects of recruitment on genetic patchiness in the urchin Echinometra mathaei in Western Australia. Mar. Biol. 105, 145-151.
93. Weir, B.S., 1990. Genetic Data Analysis. Methods for Discrete Population Data. Sinauer Associates, Sunderland, MA.
94. Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358-1370.
95. Williams, S.T., Benzie, J.A.H., 1993. Genetic consequences of long larval life in the starfish Linckia laevigata (Echinodermata: Asteroidea) on the Great Barrier Reef. Mar. Biol. 117, 71-77.
96. Williams, S.T., Benzie, J.A.H., 1996. Genetic uniformity of widely separated populations of the coral reef starfish Linckia laevigata from the East Indian and West Pacific Oceans, revealed by allozyme analysis. Mar. Biol. 126, 99-107.
97. Willis, B.L., Oliver, J.K., 1990. Direct tracking of coral larvae: implications for dispersal studies of planktonic larvae in topographically complex environments. Ophelia 32, 145-162.
98. Worcester, S.E., 1994. Adult rafting vs. larval swimming: dispersal and recruitment of a botryllid ascidian on eelgrass. Mar. Biol. 121, 309-317.
99. Wright S., 1969. Evolution and the Genetics of Populations. The Theory of Gene Frequencies, vol.2. University of Chicago Press, Chicago.
100. Wright, S., 1978. Evolution and the Genetics of Populations. Variability Within and Among Natural Populations, vol. 4. University of Chicago Press, Chicago.