Optimal egg size in marine invertebrates: Theory and phylogenetic analysis of the critical relationship between egg size and development time in echinoids

American Naturalist

Volumn 156, Issue 2, 2000, Pages 175-192

  Levitan, Don R ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Comparative method; Development time; Echinoids; Egg size; Life history theory; Phylogeny

Indexed keywords

ECHINODERM; EGG SIZE; EVOLUTIONARY BIOLOGY; PHYLOGENETICS;

EID: 0033929369     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/303376     Document Type: Article

References (84)

1. Aiyar, R. G. 1935. Early development and metamorphosis of the tropical echinoid, Salmacis bicolor, Agassiz. Proceedings of the Indian Academy of Science 1:714-728.
2. Aslan, L. M., M. A. Rahman, and T. Vehara. 1999. Relationship between egg size and larval size of two closely related species of sea urchins genus Echinometra and the egg size effects to the larval size of their reciprocal hybrids. Biological Magazine (Okinawa) 37:67-73.
3. Biermann, C. H. 1998. The molecular evolution of sperm binding in six species of sea urchins (Echinoidea: Strongylocentrotidae). Molecular Biology and Evolution 15: 1761-1771.
4. Caldwell, J. W. 1972. Development, metamorphosis, and substrate selection of the larvae of the sand dollar Mellita quinquiesperforata (Leske, 1778). Master's thesis. University of Florida, Gainesville.
5. Cameron, R. A. 1986. Reproduction, larval occurrence and recruitment in Caribbean sea urchins. Bulletin of Marine Science 39:332-346.
6. Cameron, R. A., and S. C. Schroeter. 1980. Sea urchin recruitment: effect of substrate selection on juvenile distribution. Marine Ecology Progress Series 2:243-247.
7. Cameron, R. A., I. Boldron-Metairon, and O. Monterrosa. 1985. Does the embryonic response to temperature and salinity by four species of Caribbean sea urchins parallel the reproductive synchrony? Proceedings of the Fifth International Coral Reef Congress, Tahiti 5:273-275.
8. Caswell, H. 1981. The evolution of "mixed" life histories in marine invertebrates and elsewhere. American Naturalist 117:529-536.
9. Cellario, C., and S. George. 1990. Second generation of Paracentrotus lividus reared in the laboratory: egg quality tested. Pages 65-69 in C. de Ridder, P. Dubois, M. C. Lahaye, and M. Jangoux, eds. Echinoderm research. Balkema, Rotterdam.
10. Christiansen, F. B., and T. M. Fenchel. 1979. Evolution of marine invertebrate reproduction patterns. Theoretical Population Biology 16:267-282.
11. Clark, H. L. 1923. The echinoderm fauna of South America. Annals of the South African Museum 13:221-435.
12. D'Croz, L., and D. R. Robertson. 1997. Coastal oceanographic conditions affecting coral reefs on both sides of the Isthmus of Panama. Coral Reef Symposium 2: 2053-2058.
13. Eckert, G. L. 1998. Larval development, growth and morphology of the sea urchin Diadema antillarum. Bulletin of Marine Science 63:443-451.
14. Emlet, R. B. 1986. Facultative planktotrophy in the tropical echinoid Clypeaster rosaceus (Linnaeus) and a comparison with obligate planktotrophy in Clypeaster subdepressus (Gray) (Clypeasteroida: Echinoidea). Journal of Experimental Marine Biology and Ecology 95:183-202.
15. -. 1988. Larval form and metamorphosis of a "primitive" sea urchin, Eucidaris thoursi (Echinoidea: Cidaroida), with implications for development and phylogenetic studies. Biological Bulletin (Woods Hole) 174: 4-19.
16. -. 1995. Development mode and species geographic range in regular sea urchins (Echinodermata: Echinoidea). Evolution 49:476-498.
17. Emlet, R. B., and O. Hoegh-Guldberg. 1997. Effects of egg size on postlarval performance: experimental evidence from a sea urchin. Evolution 51:141-152.
18. Emlet, R. B., L. R. McEdward, and R. R. Strathmann. 1987. Echinoderm larval ecology viewed from the egg. Pages 55-136 in M. Jangoux and J. M. Lawrence, eds. Echinoderm studies. Vol. 2. Balkema, Rotterdam.
19. Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1-15.
20. Fenaux, L., M. F. Strathmann, and R. R. Strathmann. 1994. Five tests of food-limited growth of larvae in coastal waters by comparisons of rates of development and form of echinoplutei. Limnology and Oceanography 39: 84-98.
21. George, S. B., C. Cellario, and L. Fenaux. 1990. Population differences in egg quality of Arbacia lixula (Echinodermata Echinoidea): proximate composition of eggs and larval development. Journal of Experimental Marine Biology and Ecology 141:107-118.
22. Glynn, P. W. 1972. Observations on the ecology of the Caribbean and Pacific coasts of Panama. Bulletin of the Biological Society of Washington 2:13-30.
23. Hagström, B. E., and S. Lönning. 1967. Experimental studies of Strongylocentrotus droebachiensis and S. pallidus. Sarsia 29:165-176.
24. Hart, M. W. 1995. What are the costs of small egg size for a marine invertebrate with feeding planktonic larvae? American Naturalist 146:415-426.
25. -. 1996. Evolutionary loss of larval feeding: development, form, and function in a facultatively feeding larva, Brisaster latifrons. Evolution 50:174-187.
26. Hart, M. W., and R. R. Strathmann. 1994. Functional consequencies of phenotypic plasticity in echinoid larvae. Biological Bulletin (Woods Hole) 186:291-299.
27. Harvey, E. B. 1956. The American Arbacia and other sea urchins. Princeton University Press, Princeton, N.J.
28. Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford.
29. Havenhand, J. N. 1995. Evolutionary ecology of larval types. Pages 79-122 in L. R. McEdward, ed. Ecology of marine invertebrate larvae. CRC, Boca Raton, Fla.
30. Herrera, J. C., S. K. McWeeney, and L. R. McEdward. 1996. Diversity of energetic strategies among echinoid larvae and the transition from feeding to nonfeeding development. Oceanologica Acta 19:313-321.
31. Highsmith, R. C. 1982. Induced settlement and metamorphosis of sand dollar (Dendraster excentricus) larvae in predator-free sites: adult sand dollar beds. Ecology 63:329-337.
32. -. 1985. Floating and algal rafting as potential dispersal mechanisms in brooding marine invertebrates. Marine Ecology Progress Series 25:169-176.
33. Hoegh-Guldberg, O., and J. S. Pearse. 1995. Temperature, food availability, and the development of marine invertebrate larvae. American Zoologist 35:415-425.
34. Jaeckle, W. B. 1995. Variation in the size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development. Pages 49-77 in L. McEdward, ed. Ecology of marine invertebrate larvae. CRC, Boca Raton, Fla.
35. Lessios, H. A. 1990. Adaptation and phylogeny as determinants of egg size in echinoderms from the two sides of the Isthmus of Panama. American Naturalist 135: 1-13.
36. Levitan, D. R. 1993. The importance of sperm limitation to the evolution of egg size in marine invertebrates. American Naturalist 141:517-536.
37. -. 1995. The ecology of fertilization in free-spawning invertebrates. Pages 123-156 in L. McEdward, ed. Ecology of marine invertebrate larvae. CRC, Boca Raton, Fla.
38. -. 1996a. Distribution, abundance and water flow influence fertilization success in natural assemblages of sea urchins. American Zoologist 36:12A.
39. -. 1996b. Effects of gamete traits on fertilization in the sea and the evolution of sexual dimorphism. Nature (London) 382:153-155.
40. -. 1996c. Predicting optimal and unique egg sizes in free-spawning marine invertebrates. American Naturalist 148:174-188.
41. -. 1998. Does Bateman's principle apply to broadcast-spawning organisms? egg traits influence in situ fertilization rates among congeneric sea urchins. Evolution 52:1043-1056.
42. Levitan, D. R., and C. Petersen. 1995. Sperm limitation in the sea. Trends in Ecology & Evolution 10:228-231.
43. Littlewood, D. T. J., and A. B. Smith. 1995. A combined morphological and molecular phylogeny for sea urchins (Echinoidea: Echinodermata). Philosophical Transactions of the Royal Society of London B, Biological Sciences 347:213-234.
44. Maddison, W. P. 1991. Squared-change parsimony reconstructions of ancestral states for continuous-valued characters on a phylogenetic tree. Systematic Zoology 40:304-314.
45. Maddison, W. P., and D. R. Maddison. 1992. MacClade. Version 3: analysis of phylogeny and character evolution. Sinauer, Sunderland, Mass.
46. McEdward, L. R. 1985. Effects of temperature on the body form, growth, electron transport system activity, and development rate of an echinopluteus. Journal of Experimental Marine Biology and Ecology 93:169-181.
47. -. 1986. Comparative morphometrics of echinoderm larvae. II. Larval size, shape, growth, and the scaling of feeding and metabolism in echinoplutei. Journal of Experimental Marine Biology and Ecology 96:267-286.
48. -. 1997. Reproductive strategies of marine benthic invertebrates revisited: facultative feeding by planktonic larvae. American Naturalist 150:48-72.
49. McPherson, B. F. 1968. Contributions to the biology of the sea urchin Eucidaris tribuloides (Lamarck). Bulletin of Marine Science 18:400-443.
50. Mazur, J. E., and J. W. Miller. 1971. A description of the complete metamorphosis of the sea urchin Lytechinus variegatus cultured in synthetic sea water. Ohio Journal of Science 71:30-36.
51. Mileikovsky, S. A. 1971. Types of larval development in marine bottom invertebrates, their distribution and ecological significance: a re-evaluation. Marine Biology 10: 193-213.
52. Mooi, R. 1987. A cladistic analysis of the sand dollars (Clypeasteroida: Scutellina) and the interpretation of heterochronic phenomenona. Ph.D. diss. University of Toronto.
53. -. 1990. Paedomorphosis, Aristotle's lantern, and the origin of the sand dollars (Echinodermata: Clypeasteroida). Paleobiology 16:25-48.
54. Mortensen, T. 1937. Contributions to the study of the development and larval forms of echinoderms. III. Kongelige Danske Videnskabernes Selskab Skrifter, Naturvidenskabelig og Mathematisk Afdeling Series 9, 7(1): 1-59.
55. -. 1938. Contributions to the study of the development and larval forms of echinoderms. IV. Kongelige Danske Videnskabernes Selskab Skrifter, Naturvidenskabelig og Mathematisk Afdeling Series 9, 7(3):1-59.
56. Olson, R. R., and M. H. Olson. 1989. Food limitation of planktotrophic marine invertebrate larvae: does it control recruitment success? Annual Review of Ecology and Systematics 20:225-247.
57. Onoda, K. 1931. Notes on the development of Heliocidaris crassispina with special reference to the larval body. Memoirs of the College of Science, Kyoto Imperial University, Series B 7:103-134.
58. -. 1936. Notes on the development of some Japanese echinoids with special reference to the structure of the larval body. Japanese Journal of Zoology 6:637-654.
59. Pagel, M. D., and P. H. Harvey. 1989. Comparative methods for examining adaptation depend on evolutionary models. Folia Primatologica 53:203-220.
60. Patel, B., and D. J. Crisp. 1960. The influence of temperature on the breeding and moulting activities of some warm-water species of operculate barnacles. Journal of the Marine Biological Association of the United Kingdom 39:667-680.
61. Pennington, J. T., S. S. Rumrill, and F. S. Chia. 1986. Stage-specific predation upon embryos and larvae of the Pacific sand dollar, Dendraster excentricus, by eleven species of common zooplankton predators. Bulletin of Marine Science 39:234-240.
62. Podolsky, R. D., and R. R. Strathmann. 1996. Evolution of egg size in free-spawners: consequences of the fertilization-fecundity trade-off. American Naturalist 148: 160-173.
63. Roff, D. A. 1992. The evolution of life histories: theory and analysis. Chapman & Hall, London.
64. Rumrill, S. S. 1987. Differential predation upon embryos and larvae of temperate Pacific echinoderms. Ph.D. diss. University of Alberta, Edmonton.
65. -. 1990. Natural mortality of marine invertebrate larvae. Ophelia 32:163-198.
66. Rumrill, S. S., J. T. Pennington, and F. S. Chia. 1985. Differential susceptibility of marine invertebrate larvae: laboratory predation of sand dollar, Dendraster excentricus (Eschscholtz), embryos, and larvae by zoeae of the red crab, Cancer productus Randall. Journal of Experimental Marine Biology and Ecology 90:193-208.
67. Shearer, C., W. Morgan, and H. M. Fuchs. 1913. On the experimental hybridization of echinoids. Philosophical Transactions of the Royal Society of London 204: 255-362.
68. Sinervo, B., and L. R. McEdward. 1988. Developmental consequences of an evolutionary change in egg size: an experimental test. Evolution 42:885-899.
69. Smith, A. B. 1988. Phylogenetic relationship, divergence times, and rates of molecular evolution for camarodont sea urchins. Molecular Biology and Evolution 5: 345-365.
70. Smith, C. C., and S. D. Fretwell. 1974. The optimal balance between size and number of offspring. American Naturalist 108:499-506.
71. Strathmann, M. 1987a. Reproduction and development of marine invertebrates of the northern Pacific coast. University of Washington Press, Seattle.
72. Strathmann, R. R. 1971. The feeding behavior of planktotrophic echinoderm larvae: mechanisms, regulation, and rates of suspension-feeding. Journal of Experimental Marine Biology and Ecology 6:109-160.
73. -. 1978a. The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:894-906.
74. -. 1978b. Length of pelagic period in echinoderms with feeding larvae from the northeast Pacific. Journal of Experimental Marine Biology and Ecology 34:23-27.
75. -. 1979. Echinoid larvae from the northeast Pacific (with a key and comment on an unusual type of planktotrophic development). Canadian Journal of Zoology 57:610-616.
76. -. 1985. Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Annual Review of Ecology and Systematics 16:339-361.
77. -. 1987b. Larval feeding. Pages 465-550 in A. C. Giese, J. S. Pearse, and V. Pearse, eds. Reproduction in marine invertebrates. Vol. 9. General aspects: seeking unity in diversity. Blackwell Scientific, Palo Alto, Calif.
78. Strathmann, R. R., and K. Vedder. 1977. Size and organic content of eggs of echinoderms and other invertebrates as related to developmental strategies and egg eating. Marine Biology 39:305-309.
79. Thorson, G. 1946. Reproduction and larval development of Danish marine bottom invertebrates. Meddelelser fra Kommissionen for Danmarks Fiskeri-og Havundersogelser, Serie Plankton, vol. 4, Copenhagen.
80. -. 1950. Reproductive and larval ecology of marine bottom invertebrates. Biological Reviews of the Cambridge Philosophical Society 25:1-45.
81. Vance, R. R. 1973a. More on reproductive strategies in marine bottom invertebrates. American Naturalist 107: 352-361.
82. -. 1973b. On reproductive strategies in marine bottom invertebrates. American Naturalist 107:339-352.
83. Vogel, H., G. Czihak, P. Chang, and W. Wolf. 1982. Fertilization kinetics of sea urchin eggs. Mathematical Biosciences 58:189-216.
84. Wray, G. A., and R. A. Raff. 1991. The evolution of developmental strategy in marine invertebrates. Trends in Ecology & Evolution 6:45-50.