Local gamete competition explains sex allocation and fertilization strategies in the sea

American Naturalist

Volumn 184, Issue 2, 2014, Pages

  Henshaw, Jonathan M ^a   Marshall, Dustin J ^b   Jennions, Michael D ^a   Kokko, Hanna ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Broadcast spawning; Brooding; Hermaphroditism; Mode of fertilization; Sex roles; Sperm casting

Indexed keywords

ANIMAL; BODY SIZE; EVOLUTION; FEMALE; FERTILITY; FERTILIZATION; INVERTEBRATE; MALE; OOCYTE; PHYSIOLOGY; SEA; SPERMATOZOON;

ANIMALS; BIOLOGICAL EVOLUTION; BODY SIZE; FEMALE; FERTILIZATION; INVERTEBRATES; MALE; OCEANS AND SEAS; OVUM; SPERM-OVUM INTERACTIONS; SPERMATOZOA;

EID: 84904812658     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/676641     Document Type: Article

References (75)

1. Addison, J. A., and M. W. Hart.2005. Spawning, copulation and inbreeding coefficients in marine invertebrates. Biology Letters 1: 450-453.
2. Barazandeh, M., C. S. Davis, C. J. Neufeld, D. W. Coltman, and A. R. Palmer. 2013. Something Darwin didn't know about barnacles: spermcast mating in a common stalked species. Proceedings of the Royal Society B: Biological Sciences 280:20122919.
3. Beekey, M. A., and D. J. Hornbach. 2004. The effect of size-limited brood capacity on brood size in a freshwater bivalve. American Midland Naturalist 151:274-285.
4. Bishop, J. D. D., and A. J. Pemberton. 2006. The third way: spermcast mating in sessile marine invertebrates. Integrative and Comparative Biology 46:398-406.
5. Bode, M., and D. J. Marshall. 2007. The quick and the dead? sperm competition and sexual conflict in sea. Evolution 61:2693-2700.
6. Bulmer, M. G., and G. A. Parker. 2002. The evolution of anisogamy: a game-theoretic approach. Proceedings of the Royal Society B: Biological Sciences 269:2381-2388.
7. Clifton, K. E. 1997. Mass spawning by green algae on coral reefs. Science 275:1116-1118.
8. Cohen, S. 1990. Outcrossing in fieldpopulations of two species of self-fertile ascidians. Journal ofExperimental Marine Biology and Ecology 140:147-158.
9. Crampton, J. S., R. Cooper, A. G. Beu, M. Foote, and B. A. Marshall. 2010. Biotic influences on species duration: interactions between traits in marine molluscs. Paleobiology 36:204-223.
10. Crean, A. J., and D. J. Marshall. 2008. Gamete plasticity in a broadcast spawning marine invertebrate. Proceedings of the National Academy of Sciences of the USA 105:13508-13513.
11. Dusenbery, D. B. 2009. Living at micro scale: the unexpected physics of being small. Harvard University Press, Cambridge, MA.
12. Dusenbery, D. B. 2011. Gamete encounters. Pages 168-193in T. Togashi and P. A. Cox, eds. The evolution of anisogamy. Cambridge University Press, Cambridge, MA.
13. Einum, S., and I. A. Fleming. 2000. Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405:565-567.
14. Eppley, S. M., and L. K. Jesson. 2008. Moving to mate: theevolution of separate and combined sexes in multicellular organisms. Journal of Evolutionary Biology 21:727-736.
15. Evans, J. P., F. Garcia-Gonzalez, M. Almbro, O. Robinson, and J. L. Fitzpatrick. 2012. Assessing the potential for egg chemoattractants to mediate sexual selection in a broadcast spawning marine invertebrate. Proceedings of the Royal SocietyB: Biological Sciences 279:2855-2861.
16. Giese, A. C., and H. Kanatani. 1987. Maturation and spawning. Pages 252-329in A. C. Giese and J. S. Pearse, eds. Reproduction of marine invertebrates. Vol. 11. General aspects: seeking unity in diversity. Blackwell Scientific, Palo Alto, CA.
17. Giese, A. C., and J. S. Pearse. 1974. Introduction: general principles. Pages 1-49in A. C. Giese and J. S. Pearse, eds. Reproduction of marine invertebrates. Vol. 1. Acoelomateand pseudocoelomate metazoans. Academic Press, New York.
18. Gil, D. G., G. Escudero, and H. E. Zaixso. 2011. Brooding and development ofAnasterias minuta(Asteroidea: Forcipulata) in Patagonia, Argentina. Marine Biology 158:2589-2602.
19. Hansen, T. 1980. Influence of larval dispersal and geographic distribution on species longevity in neogastropods. Paleobiology 6: 193-207.
20. Hart, M. W., M. Byrne, and M. J. Smith. 1997. Molecular phylogenetic analysis of life-history evolution in asterinid starfish. Evolution 51:1848-1861.
21. Hayward, A., and J. F. Gillooly. 2011. The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS ONE 6:e16557.
22. Heath, D. J. 1977. Simultaneous hermaphroditism; cost and benefit. Journal of Theoretical Biology 64:363-373.
23. Heath, D. J. 1979. Brooding and the evolution of hermaphroditism. Journal of Theoretical Biology 81:151-155.
24. Heller, J. 1993. Hermaphroditism in molluscs. Biological Journal of the Linnean Society 48:19-42.
25. Henshaw, J. M., D. J. Marshall, M. J. Jennions, and H. Kokko. 2014. Data from: Local gamete competition explainssex allocation and fertilization strategies in the sea. American Naturalist, Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.1mp91.
26. Hess, H. C. 1993. The evolution of parental care in brooding spirorbid polychaetes: the effect of scaling constraints. American Naturalist 141:577-596.
27. Hutchinson, J. M. C., and P. M. Waser. 2007. Use, misuse and extensions of "ideal gas" models of animal encounter. Biological Reviews 82:335-359.
28. Iyer, P., and J. Roughgarden. 2008. Dioecy as a specialization promoting sperm delivery. Evolutionary Ecology Research 10:867-892.
29. Jarne, P., and J. R. Auld. 2006. Animals mix it up too: the distribution of self-fertilization among hermaphroditicanimals. Evolution 60: 1816-1824.
30. Jarne, P., and D. Charlesworth. 1993. The evolution ofthe selfing rate in functionally hermaphrodite plants and animals. Annual Review of Ecology and Systematics 24:441-466.
31. Jones, G. P., G. R. Almany, G. R. Russ, P. F. Sale, R. S. Steneck, M. J. H. Oppen, and B. L. Willis. 2009. Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307-325.
32. Jørgensen, C., S. K. Auer, and D. N. Reznick. 2011. A model for optimal offspring size in fish, including live-bearing and parental effects. American Naturalist 177:E119-E135.
33. Kahn, A. T., H. Kokko, and M. D. Jennions. 2013. Adaptive sex allocation in anticipation of changes inoffspring mating opportunities. Nature Communications 4:1603.
34. Kerr, A., A. Baird, and T. Hughes. 2011. Correlated evolution of sex and reproductive mode in corals (Anthozoa: Scleractinia). Proceedings of the Royal Society B:Biological Sciences 278:75-81.
35. Kiørboe, T., and M. Sabatini. 1995. Scaling of fecundity, growth and development in marine planktonic copepods. Marine Ecology Progress Series 120:285-298.
36. Kupriyanova, E. K., E. Nishi, H. A. tenHove, and A. V Rzhavsky. 2001. Life-history patterns in serpulimorph polychaetes: ecological and evolutionary perspectives. Oceanography andMarine Biology: An Annual Review 39:1-101.
37. Levitan, D. R. 1991. Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate. Biological Bulletin 181:261-268.
38. Levitan, D. R. 1993. The importance of sperm limitation to the evolution of egg size in marine invertebrates. American Naturalist 4:517-536.
39. Levitan, D. R. 1998. Sperm competition, gamete competition, and sexual selection in external fertilizers. Pages 175-217 in T. R. Birkhead and A. P. Møller, eds. Sperm competition and sexual selection. Academic Press, San Diego, CA.
40. Levitan, D. R., and C. Petersen. 1995. Sperm limitation in the sea. Trends in Ecology and Evolution 10:228-231.
41. Marquet, P. A., S. A. Navarrete, and J. C. Castilla. 1990. Scaling population density to body size in rocky intertidal communities. Science 250:1125-1127.
42. Marshall, D. J. 2002. In situ measuresof spawning synchrony and fertilization success in an intertidal, free-spawning invertebrate. Marine Ecology Progress Series 236:113-119.
43. Marshall, D. J., and J. P. Evans. 2005. Does egg competition occur in marine broadcast-spawners? Journal of Evolutionary Biology 18:1244-1252.
44. Marshall, D. J., and M. J. Keough.2006. Complex lifecycles and offspring provisioning in marine invertebrates. Integrative and Comparative Biology 46:643-651.
45. McFadden, C. S., R. Donahue, B. K. Hadland, and R. Weston. 2001. A molecular phylogenetic analysis of reproductive trait evolution in the soft coral genus Alcyonium. Evolution 55:54-67.
46. Niklas, K. J. 1997. The evolutionary biology of plants. University of Chicago Press, Chicago.
47. Otto, S. P., and T. Day. 2007. A biologist's guide to mathematical modeling in ecology and evolution. Princeton University Press, Princeton, NJ.
48. Parker, G. A. 2011. The origin and maintenance of two sexes (anisogamy), and their gamete sizes by gamete competition. Pages 17-74in T. Togashi and P. A. Cox, eds. The evolution of anisogamy. Cambridge University Press, Cambridge, MA.
49. Pemberton, A. J., L. R. Noble, and J. D. D. Bishop. 2003. Frequency dependence in matings with water-borne sperm. Journal of Evolutionary Biology 16:289-301.
50. Pemberton, A. J., A. D. Sommerfeldt, C. A. Wood, H. C. Flint, L. R. Noble, K. R. Clarke, and J. D. D. Bishop. 2004. Plant-like mating in an animal: sexual compatibility and allocation trade-offs in a simultaneous hermaphrodite with remote transfer of sperm. Journal of Evolutionary Biology 17:506-518.
51. Peters, R. H. 1983. The ecological implications of body size. Cambridge University Press, Cambridge.
52. Puurtinen, M., and V. Kaitala. 2002. Mate-search efficiency can determine the evolution of separate sexes and the stability of hermaphroditism in animals. American Naturalist 160:645-660.
53. Riisgård, H. U. 2001. On measurement of filtration rates in bivalves-the stony road to reliable data: review and interpretation. Marine Ecology Progress Series 211:275-291.
54. Rius, M., X. Turon, G. M. Dias, and D. J. Marshall. 2010. Propagule size effects across multiple life-history stages in a marine invertebrate. Functional Ecology 24:685-693.
55. Roff, D. A. 2002. Life history evolution. Sinauer, Sunderland, MA.
56. Rosenstiel, T. N., E. E. Shortlidge, A. N. Melnychenko, J. F. Pankow, and S. M. Eppley. 2012. Sex-specificvolatile compoundsinfluence microarthropod-mediated fertilization of moss. Nature 489:431-433.
57. Rouse, G., and K. Fitzhugh. 1994. Broadcasting fables: is external fertilization really primitive? sex, size, and larvae in sabellid polychaetes. Zoologica Scripta 23:271-312.
58. Sargent, R. C., P. D. Taylor, and M. R. Gross. 1987. Parental care and the evolution of egg size in fishes. American Naturalist 129: 32-46.
59. Schärer, L. 2009. Tests of sex allocation theory in simultaneously hermaphroditic animals. Evolution 63:1377-1405.
60. Scheltema, R. S. 1977. Dispersal of marine invertebrate organisms: paleobiogeographic and biostratigraphic implications. Pages 73-108inE. G. Kauffman and J. E. Hazel, eds. Concepts and methods of biostratigraphy. Down, Hutchinson and Ross, Stroudsburg, PA.
61. Sewell, M. A. 1994. Small size, brooding, and protandry in the apodid sea cucumberLeptosynapta clarki. Biological Bulletin 187:112-123.
62. Shaw, R. F., and J. D. Mohler. 1953. The selective significance of the sex ratio. American Naturalist 87:337-342.
63. Shine, R. 1978. Propagule size and parental care: the "safe harbor" hypothesis. Journal of Theoretical Biology 75:417-424.
64. Smith, C. C., and S. D. Fretwell. 1974. The optimal balance between size and number of offspring. American Naturalist 108:499-506.
65. Strathmann, R. R. 1990. Why life histories evolve differently in the sea. American Zoologist 30:197-207.
66. Strathmann, R. R., and M. F. Strathmann. 1982. The relationship between adult size and brooding in marine invertebrates. American Naturalist 119:91-101.
67. Strathmann, R. R., M. F. Strathmann, and R. H. Emson. 1984. Does limited brood capacity link adult size, brooding, and simultaneous hermaphroditism? a test with the starfish Asterina phylactica. American Naturalist 123:796-818.
68. Vance, R. R. 1973. On reproductive strategies in marine benthic invertebrates. American Naturalist 107:339-352.
69. Weeks, S. C. 2012. The role of androdioecy and gynodioecy in mediating evolutionary transitions between dioecy and hermaphroditism in the animalia. Evolution 66:3670-3686.
70. West, S. 2009. Sex allocation. Princeton University Press, Princeton, NJ.
71. White, E. P., S. K. M. Ernest, A. J. Kerkhoff, and B. J. Enquist. 2007. Relationships between body size and abundancein ecology. Trends in Ecology and Evolution 22:323-330.
72. Williams, G. C. 1975. Sex and Evolution. Princeton University Press, Princeton, NJ.
73. Yund, P. O. 2000. How severe is sperm limitation in natural populations of marine free-spawners? Trends in Ecology and Evolution 15:10-13.
74. Yund, P. O., and S. K. Meidel. 2003. Sea urchin spawning in benthic boundary layers: are eggs fertilized before advecting away from females? Limnology and Oceanography 48:795-801.
75. Zizzari, Z. V., A. Braakhuis, N. M. van Straalen, and J. Ellers. 2009. Female preference and fitness benefits of mate choice in a species with dissociated sperm transfer. Animal Behaviour 78:1261-1267.