Patterns of self compatibility, inbreeding depression, outcrossing, and sex allocation in a marine bryozoan suggest the predominating influence of sperm competition

Biological Journal of the Linnean Society

Volumn 98, Issue 3, 2009, Pages 519-531

  Hughes, Roger N ^a   Wright, Peter J ^a   Carvalho, Gary R ^a   Hutchinson, William F ^b  

^a BANGOR UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF HULL   (United Kingdom)

Author keywords

AFLP; Celleporella hyalina; Geitonogamy; Mixed mating; Reproductive assurance; Self fertilization; Simultaneous hermaphroditism

Indexed keywords

ADAPTATION; AUTOGAMY; BRYOZOAN; GENET; GENETIC MARKER; GENOMICS; HERMAPHRODITE; INBREEDING DEPRESSION; OUTCROSSING; PATERNITY; PHYLOGENETICS; REPRODUCTIVE ISOLATION; SEX ALLOCATION; SPERM COMPETITION; SUBTIDAL ENVIRONMENT; SURVIVORSHIP;

BRYOZOA; CELLEPORELLA HYALINA; GYMNOLAEMATA; INVERTEBRATA; SPERMATOPHYTA;

EID: 70350547735     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2009.01312.x     Document Type: Article

References (77)

1. Ayre DJ, Miller K. 2006. Random mating in the brooding coral Acropora palifera. Marine Ecology Progress Series 307 : 155 160.
2. Baker HG. 1955. Self-compatibility and establishment after 'long-distance' dispersal. Evolution 9 : 347 348.
3. Bergquist PR. 1978. Sponges. London : Hutchinson.
4. Bishop JDD. 1998. Fertilization in the sea: are the hazards of broadcast spawning avoided when free-spawned sperm fertilize retained eggs? Proceedings of the Royal Society of London Series B, Biological Sciences 265 : 725 731.
5. Cancino JM. 1986. Marine macroalgae as a substratum for sessile invertebrates: a study of Celleporella hyalina (Bryozoa) on fronds of Laminaria saccharina (Phaeophyta). Monografías Biológicas 4 : 279 308.
6. Cancino JM, Hughes RN. 1988. The zooidal polymorphism and ontogeny of Celleporella hyalina (L.) (Bryozoa: Cheilostomata). Journal of Zoology, London 215 : 167 181.
7. Cancino JM, Hughes RN, Ramirez C. 1991. Environmental cues and the phasing of larval release in the bryozoan Celleporella hyalina (L.). Proceedings of the Royal Society of London Series B, Biological Sciences 246 : 39 45.
8. Charlesworth D, Charlesworth B. 1981. Allocation of resources to male and female functions in hermaphrodites. Biological Journal of the Linnean Society 15 : 57 74.
9. Charlesworth D, Charlesworth B. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18 : 237 268.
10. Charnov EL. 1979. Simultaneous hermaphroditism and sexual selection. Proceedings of the National Academy of Science of the United States of America 76 : 2480 2484.
11. Charnov EL. 1982. The theory of sex allocation. Princeton, NJ : Princeton University Press.
12. Charnov EL. 1987. On sex allocation and selfing in higher plants. Evolutionary Biology 1 : 30 36.
13. Coffroth MA, Lasker HR. 1998. Larval paternity and male reproductive success of a broadcast-spawning gorgonian, Plexaura kuna. Marine Biology 131 : 329 337.
14. Collin R. 2004. Phylogenetic effects, the loss of complex characters, and the evolution of development in clyptraeid gastropods. Evolution 58 : 1488 1502.
15. Craig SF, D'Amato ME, Harley M, Bishop M, Bishop J, Hughes R, Carvalho GR. 2001. Isolation and characterization of microsatellites in the bryozoan Crisia denticulata. Molecular Ecology Notes 1 : 281 282.
16. Cruden RW. 1977. Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31 : 32 46.
17. Darwin CR. 1876. The effects of cross- and self-fertilization in the vegetable kingdom. London : John Murray.
18. Darwin CR. 1877. The different forms of flowers on plants of the same species. London : John Murray.
19. Fautin DG. 2002. Reproduction of Cnidaria. Canadian Journal of Zoology 80 : 1735 1754.
20. Fisher RA. 1941. Average excess and average effect of a gene substitution. Annals of Eugenics 11 : 53 63.
21. Freeland JR, Jones CS, Noble LR, Okamura B. 1999. Polymorphic microsatellite loci identified in the highly clonal freshwater bryozoan Cristatella mucedo. Molecular Ecology 8 : 341 342.
22. Freeland JR, Noble LR, Okamura B. 2000. Genetic diversity of North American populations of Cristatella mucedo, inferred from microsatellite and mitochondrial DNA. Molecular Ecology 9 : 1375 1389.
23. Ghiselin MT. 1969. The evolution of hermaphroditism among animals. Quarterly Review of Biology 44 : 189 208.
24. Goodwillie C, Kalisz S, Eckert CG. 2005. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology and Systematics 36 : 47 79.
25. Gould SJ, Lewontin RC. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London Series B, Biological Sciences 205 : 581 598.
26. Gow JL, Noble LR, Rollinson D, Jones CS. 2005. High levels of selfing are revealed by a parent-offspring anaysis of the medically important freshwater snail, Bulinus forskalii (Gastropoda: Pulmonata). Journal of Molluscan Studies 71 : 175 180. (Pubitemid 40697278)
27. Grosberg RK. 1987. Limited dispersal and proximity-dependent mating success in the colonial ascidian Botryllus schlosseri. Evolution 41 : 372 384.
28. Gómez A, Hughes RN, Wright PJ, Carvalho GR, Lunt DH. 2007b. Mitochondrial DNA phylogeography and mating compatibility reveal marked genetic structuring and speciation in the NE Atlantic bryozoan Celleporella hyalina. Molecular Ecology 16 : 2173 2188.
29. Gómez A, Wright PJ, Lunt DH, Cancino JM, Carvalho GR, Hughes RN. 2007a. Mating trials validate the use of DNA barcoding to reveal cryptic speciation of a marine bryozoan taxon. Proceedings of the Royal Society of London Series B, Biological Sciences 274 : 199 207.
30. Harper JL. 1977. Population biology of plants. London : Academic Press.
31. Heath DJ. 1977. Simultaneous hermaphroditism: cost and benefit. Journal of Theoretical Biology 64 : 363 373.
32. Hoare K, Hughes RN. 2001. Inbreeding and hermaphroditism in the sessile-brooding bryozoan Celleporella hyalina. Marine Biology 139 : 147 162. (Pubitemid 32706753)
33. Hoare K, Hughes RN, Gliddon CJ. 1998. Polymorphic microsatellite markers isolated from the bryozoan Celleporella hyalina (L.). Molecular Ecology 7 : 355 356.
34. Hochberg Y. 1988. A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75 : 800 802.
35. Hughes DJ. 1989a. Variation in reproductive strategy among clones of the bryozoan Celleporella hyalina. Ecological Monographs 59 : 387 403.
36. Hughes RN. 1989b. A functional biology of clonal animals. London : Chapman and Hall.
37. Hughes RN. 2005. Lessons in modularity: the evolutionary ecology of colonial invertebrates. In: Marassé C, Abelló P, eds. Promoting Marine Science: Contributions to Celebrate the 50th Anniversary of Scientia Marina. Scientia Marina 69 (Suppl. 1 169 179.
38. Hughes RN, Manríquez PH, Bishop JDD. 2002a. Female investment is retarded pending reception of allosperm in a hermaphroditic colonial invertebrate. Proceedings of the National Academy of Sciences of the United States of America 99 : 14884 14886.
39. Hughes RN, Manríquez PH, Bishop JDD, Burrows MT. 2003. Stress promotes maleness in hermaphroditic modular animals. Proceedings of the National Academy of Sciences of the United States of America 100 : 10326 10330.
40. Hughes RN, Wright P, Manríquez PH, Bishop JDD. 2002b. Predominance of obligate outbreeding in the simultaneous hermaphrodite Celleporella hyalina sensu lato. In : Wyse Jackson PN, Buttler CJ, Spencer Jones M, eds. Bryozoan studies 2001: proceedings of the 12th International Bryozoology Association Conference, Dublin. Rotterdam : Balkema, 159 162.
41. Hunter E, Hughes RN. 1995. Environmental and genetic control of variation in sexual allocation in an epialgal bryozoan. Marine Ecology Progress Series 120 : 193 201.
42. Jackson JBC. 1977. Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. The American Naturalist 111 : 743 768.
43. Jain SK. 1976. The evolution of inbreeding in plants. Annual Review of Ecology and Systematics 7 : 469 495.
44. Jarne P, Auld JR. 2006. Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution 60 : 1816 1824.
45. Jarne P, Charlesworth D. 1993. The evolution of the selfing rate in functionally hermaphrodite plants and animals. Annual Review of Ecology and Systematics 24 : 441 466.
46. Johnson KP, McKinney F, Sorenson MD. 1999. Phylogenetic constraint on male parental care in the dabbling ducks. Proceedings of the Royal Society of London Series B, Biological Sciences 266 : 759 763.
47. Johnston MO, Das B, Hoeh WR. 1998. Negative correlation between male allocation and rate of self-fertilization in a hermaphroditic animal. Proceedings of the National Academy of Sciences of the United States of America 95 : 617 620.
48. de Jong TJ, Klinkhamer PGL, Rademaker MCJ. 1999. How geitonogamous selfing affects sex allocation in hermaphrodite plants. Journal of Evolutionary Biology 12 : 166 176.
49. Knowlton N, Jackson JBC. 1993. Inbreeding and outbreeding in marine invertebrates. In : Thornhill NW, ed. The natural history of inbreeding and outbreeding: Theoretical and empirical perspectives. Chicago, IL : Chicago University Press, 200 249.
50. Lande R, Schemske DW. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39 : 24 40. (Pubitemid 16276773)
51. Levitan DR, Petersen C. 1995. Sperm limitation in the sea. Trends in Ecology and Evolution 10 : 228 231.
52. Lloyd DG. 1979. Some reproductive factors affecting the selection of self fertilization in plants. American Naturalist 113 : 67 79.
53. Lloyd DG. 1992. Self- and cross-fertilization in plants. II. The selection of self-fertilization. International Journal of Plant Science 153 : 370 380.
54. Lloyd DG, Bawa KS. 1984. Modification of the gender of seed plants in varying conditions. Evolutionary Biology 17 : 255 338.
55. McCartney MA. 1997. Sex allocation and male fitness gain in a colonial, hermaphroditic marine invertebrate. Evolution 51 : 127 140.
56. Manríquez PH. 1999. Mate choice and reproductive investment in the cheilostome bryozoan Celleporella hyalina (L.). PhD thesis. Bangor : University of Wales, Bangor.
57. Manríquez PH, Hughes RN, Bishop JDD. 2001. Age-dependent loss of fertility in water-borne sperm of the bryozoan Celleporella hyalina. Marine Ecology Progress Series 224 : 87 92.
58. Maynard Smith J. 1978. The evolution of sex. Cambridge : Cambridge University Press.
59. Meudt HM, Clarke AC. 2007. Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends in Plant Science 12 : 106 117.
60. Pagel M. 1999. Inferring the historical patterns of biological evolution. Nature 401 : 877 884.
61. Parker GA, Simmons LW, Kirk H. 1990. Analysing sperm competition data: simple models for predicting mechanisms. Behavioral Ecology and Sociobiology 27 : 55 65.
62. Pemberton AJ, Hughes RN, Manríquez PH, Bishop JDD. 2003. Efficient utilization of very dilute sperm: sperm competition may be more likely than sperm limitation when eggs are retained. Proceedings of the Royal Society of London Series B, Biological Sciences 270 (Suppl. S223 S226.
63. Poulin R. 1997. Egg production in adult trematodes: adaptation or constraint? Parasitology 114 : 195 204.
64. Ryland JS. 1970. Bryozoans. London : Hutchinson University Library.
65. Ryland JS. 1976. Physiology and ecology of marine bryozoans. Advances in Marine Biology 14 : 285 443.
66. Schemske DW, Lande R. 1985. The evolution of self-fertilization and inbreeding depression in plants. II. Empirical observations. Evolution 39 : 41 52. (Pubitemid 16276774)
67. Schoen DJ. 1982. Male reproductive effort and breeding system in an hermaphroditic plant. Oecologia 53 : 255 257.
68. Sherman CDH. 2008. Mating system variation in the hermaphroditic brooding coral, Seriatopora hystrix. Heredity 100 : 296 303.
69. Simes JR. 1986. An improved Bonferroni procedure for multiple tests of significance. Biometrika 73 : 75 754.
70. Stebbins GL. 1950. Variation and evolution in plants. New York, NY : Columbia University Press.
71. Tallamy DW, Brown WP. 1999. Semelparity and the evolution of maternal care in insects. Animal Behaviour 57 : 727 730.
72. Taylor PD, Ernst A. 2004. Bryozoans. In : Webby BD, Paris F, Droser ML, Percival IG, eds. The great Ordovician biodiversification event. New York, NY : Columbia University Press, 147 156.
73. Tomimatsu H, Ohara M. 2006. Evolution of hierarchical floral resource allocation associated with mating system in an animal-pollinated hermaphroditic herb, Trillium camschatcense (Trilliaceae). American Journal of Botany 93 : 134 141.
74. Tysklind N, Taylor MI, Lyons BP, McCarthy ID, Carvalho GR. 2009. Development of 30 microsatellite markers for dab (Limanda limanda L.): a key UK marine biomonitoring species. Molecular Ecology Resources 9 : 951 955.
75. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau S. 1995. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23 : 4407 4414.
76. Yund PO. 1998. The effect of sperm competition on male gain curves in a colonial marine invertebrate. Ecology 79 : 328 339.
77. Yund PO, McCartney MA. 1994. Male reproductive success in sessile invertebrates - competition for fertilizations. Ecology 75 : 2151 2167.