Fertilisation is not a new beginning: Sperm environment affects offspring developmental success

Journal of Experimental Biology

Volumn 216, Issue 16, 2013, Pages 3104-3109

  Ritchie, Hannah ^a   Marshall, Dustin J ^a,b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Complex life cycles; Life history theory; Phenotypic plasticity; Stress

Indexed keywords

ANIMAL; ARTICLE; COMPLEX LIFE CYCLES; ENVIRONMENT; FERTILIZATION; GROWTH, DEVELOPMENT AND AGING; LARVA; LIFE-HISTORY THEORY; MALE; PHENOTYPIC PLASTICITY; PHYSIOLOGY; POLYCHAETA; SALINITY; SPERMATOZOON; STRESS;

COMPLEX LIFE CYCLES; LIFE-HISTORY THEORY; PHENOTYPIC PLASTICITY; STRESS;

ANIMALS; ENVIRONMENT; FERTILIZATION; GROWTH AND DEVELOPMENT; LARVA; MALE; POLYCHAETA; SALINITY; SPERMATOZOA;

EID: 84881140698     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.087221     Document Type: Article

References (54)

1. Allen, J. D. and Pechenik, J. A. (2010). Understanding the effects of low salinity on fertilization success and early development in the sand dollar Echinarachnius parma. Biol. Bull. 218, 189-199.
2. Andrews, J. C. and Anderson, D. T. (1962). The development and settling of the polychaete Galeolaria caespitosa Lamarck (Fam. Serpulidae). Proc. Linn. Soc. N. S. W. 2, 185-188.
3. Arnold, S. J. (1992). Constraints on phenotypic evolution. Am. Nat. 140 Suppl. 1, S85-S107.
4. Beckerman, A., Benton, T. G., Ranta, E., Kaitala, V. and Lundberg, P. (2002). Population dynamic consequences of delayed life-history effects. Trends Ecol. Evol. 17, 263-269.
5. Bergeron, C. M., Hopkins, W. A., Todd, B. D., Hepner, M. J. and Unrine, J. M. (2011). Interactive effects of maternal and dietary mercury exposure have latent and lethal consequences for amphibian larvae. Environ. Sci. Technol. 45, 3781-3787.
6. Birkhead, T. R. and Pizzari, T. (2002). Postcopulatory sexual selection. Nat. Rev. Genet. 3, 262-273.
7. Blows, M. W. (2007). A tale of two matrices: Multivariate approaches in evolutionary biology. J. Evol. Biol. 20, 1-8.
8. Bonduriansky, R. and Day, T. (2009). Nongenetic inheritance and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 40, 103-125.
9. Bonduriansky, R. and Head, M. (2007). Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae). J. Evol. Biol. 20, 2379-2388.
10. Bownds, C., Wilson, R. S. and Marshall, D. J. (2010). Why do colder mothers produce larger eggs? An optimality approach. J. Exp. Biol. 213, 3796-3801.
11. Crean, A. J., Monro, K. and Marshall, D. J. (2011). Fitness consequences of larval traits persist across the metamorphic boundary. Evolution 65, 3079-3089.
12. Crean, A. J., Dwyer, J. M. and Marshall, D. J. (2012). Fertilization is not a new beginning: The relationship between sperm longevity and offspring performance. PLoS ONE 7, e49167.
13. de Boer, P., Ramos, L., de Vries, M. and Gochhait, S. (2010). Memoirs of an insult: Sperm as a possible source of transgenerational epimutations and genetic instability. Mol. Hum. Reprod. 16, 48-56.
14. Dinnel, P. A., Link, J. M., Stober, Q. J., Letourneau, M. W. and Roberts, W. E. (1989). Comparative sensitivity of sea urchin sperm bioassays to metals and pesticides. Arch. Environ. Contam. Toxicol. 18, 748-755.
15. Droge-Young, E. M., Manier, M. K., Lüpold, S., Belote, J. M. and Pitnick, S. (2012). Covariance among premating, post-copulatory and viability fitness components in Drosophila melanogaster and their influence on paternity measurement. J. Evol. Biol. 25, 1555-1563.
16. Evans, J. P. and Marshall, D. J. (2005). Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59, 106-112.
17. Evans, J. P., Zane, L., Francescato, S. and Pilastro, A. (2003). Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421, 360-363.
18. Evans, J. P., García-González, F. and Marshall, D. J. (2007). Sources of genetic and phenotypic variation in sperm performance and larval traits in a sea urchin. Evolution 61, 2832-2838.
19. Fitzpatrick, J. L., Nadella, S., Bucking, C., Balshine, S. and Wood, C. M. (2008). The relative sensitivity of sperm, eggs and embryos to copper in the blue mussel (Mytilus trossulus). Comp. Biochem. Phys. C 147, 441-449.
20. Flanagan, J. M., Popendikyte, V., Pozdniakovaite, N., Sobolev, M., Assadzadeh, A., Schumacher, A., Zangeneh, M., Lau, L., Virtanen, C., Wang, S. C. et al. (2006). Intra-and interindividual epigenetic variation in human germ cells. Am. J. Hum. Genet. 79, 67-84.
21. Fox, C. W. and Czesak, M. E. (2000). Evolutionary ecology of progeny size in arthropods. Annu. Rev. Entomol. 45, 341-369.
22. Gasparini, C., Andreatta, G. and Pilastro, A. (2012). Ovarian fluid of receptive females enhances sperm velocity. Naturwissenschaften 99, 417-420.
23. Gur, Y. and Breitbart, H. (2006). Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev. 20, 411-416.
24. Hamilton, S. L., Regetz, J. and Warner, R. R. (2008). Postsettlement survival linked to larval life in a marine fish. Proc. Natl. Acad. Sci. USA 105, 1561-1566.
25. Hollows, C. F., Johnston, E. L. and Marshall, D. J. (2007). Copper reduces fertilization success and exacerbates Allee effects in the field. Mar. Ecol. Prog. Ser. 333, 51-60.
26. Hunter, F. M. and Birkhead, T. R. (2002). Sperm viability and sperm competition in insects. Curr. Biol. 12, 121-123.
27. Jablonka, E. and Raz, G. (2009). Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84, 131-176.
28. Konior, M., Radwan, J. and Keller, L. (2009). The sexually selected sperm hypothesis, maternal effects, and sperm competitive success in the bulb mite Rhizoglyphus robini. Evol. Ecol. Res. 11, 975-982.
29. Marsden, J. R. and Anderson, D. T. (1981). Larval development and metamorphosis of the serpulid polychaete Galeolaria caespitosa Lamarck. Aust. J. Mar. Freshwater Res. 32, 667-680.
30. Marshall, D. J. (2006). Reliably estimating the effect of toxicants on fertilization success in marine broadcast spawners. Mar. Pollut. Bull. 52, 734-738.
31. Marshall, D. J. and Evans, J. P. (2005a). The benefits of polyandry in the freespawning polychaete Galeolaria caespitosa. J. Evol. Biol. 18, 735-741.
32. Marshall, D. J. and Evans, J. P. (2005b). Does egg competition occur in marine broadcast-spawners? J. Evol. Biol. 18, 1244-1252.
33. Marshall, D. J. and Morgan, S. G. (2011). Ecological and evolutionary consequences of linked life-history stages in the sea. Curr. Biol. 21, R718-R725.
34. Marshall, D. J. and Uller, T. (2007). When is a maternal effect adaptive? Oikos 116, 1957-1963.
35. Marshall, D. J., Monro, K., Bode, M., Keough, M. J. and Swearer, S. (2010). Phenotype-environment mismatches reduce connectivity in the sea. Ecol. Lett. 13, 128-140.
36. Mead, K. S. and Denny, M. W. (1995). The effects of hydrodynamic shear stress on fertilization and early development of the purple sea urchin Strongylocentrotus purpuratus. Biol. Bull. 188, 46-56.
37. Morgan, S. G. and Anastasia, J. R. (2008). Behavioral tradeoff in estuarine larvae favors seaward migration over minimizing visibility to predators. Proc. Natl. Acad. Sci. USA 105, 222-227.
38. Mousseau, T. A. and Fox, C. W. (1998). The adaptive significance of maternal effects. Trends Ecol. Evol. 13, 403-407.
39. Ng, T. Y. T. and Keough, M. J. (2003). Delayed effects of larval exposure to Cu in the bryozoan Watersipora subtorquata. Mar. Ecol. Prog. Ser. 257, 77-85.
40. Ng, S. F., Lin, R. C. Y., Laybutt, D. R., Barres, R., Owens, J. A. and Morris, M. J. (2010). Chronic high-fat diet in fathers programs ß-cell dysfunction in female rat offspring. Nature 467, 963-966.
41. Pechenik, J. A. (2006). Larval experience and latent effect-metamorphosis is not a new beginning. Integr. Comp. Biol. 46, 323-333.
42. Pechenik, J. A., Gleason, T., Daniels, D. and Champlin, D. (2001). Influence of larval exposure to salinity and cadmium stress on juvenile performance of two marine invertebrates (Capitella sp. I and Crepidula fornicata). J. Exp. Mar. Biol. Ecol. 264, 101-114.
43. Quinn, G. P. and Keough, M. J. (2002). Experimental Design and Data Analysis for Biologists. Cambridge: Cambridge University Press.
44. Relyea, R. A. (2001). The lasting effects of adaptive plasticity: Predator-induced tadpoles become long-legged frogs. Ecology 82, 1947-1955.
45. Ross, K. E. and Bidwell, J. R. (2001). A 48-h larval development toxicity test using the marine polychaete Galeolaria caespitosa Lamarck (Fam. Serpulidae). Arch. Environ. Contam. Toxicol. 40, 489-496.
46. Schluter, D., Price, T. D. and Rowe, L. (1991). Conflicting selection pressures and life-history trade-offs. Proc. R. Soc. Lond. B. Bio. 246, 11-17.
47. Simmons, L. W., Roberts, J. D. and Dziminski, M. A. (2009). Egg jelly influences sperm motility in the externally fertilizing frog, Crinia georgiana. J. Evol. Biol. 22, 225-229.
48. Slatyer, R. A., Mautz, B. S., Backwell, P. R. Y. and Jennions, M. D. (2012). Estimating genetic benefits of polyandry from experimental studies: A meta-analysis. Biol. Rev. Camb. Philos. Soc. 87, 1-33.
49. Suarez, S. S. and Pacey, A. A. (2006). Sperm transport in the female reproductive tract. Hum. Reprod. Update 12, 23-37.
50. Tait, N. N., Atapattu, D. and Browne, R. (1981). Field and laboratory studies on salinity tolerance and osmotic behaviour in the polychaete Galeolaria caespitosa (Serpulidae). Aust. J. Mar. Freshwater Res. 32, 769-774.
51. Tait, N. N., Atapattu, D. and Browne, R. (1984). Effect of salinity change on early development in Galeolaria caespitosa (Polychaeta: Serpulidae). Aust. J. Mar. Freshwater Res. 35, 483-486.
52. Uller, T. (2008). Developmental plasticity and the evolution of parental effects. Trends Ecol. Evol. 23, 432-438.
53. Visconti, P. E., Johnson, L. R., Oyaski, M., Fornés, M., Moss, S. B., Gerton, G. L. and Kopf, G. S. (1997). Regulation, localization, and anchoring of protein kinase A subunits during mouse sperm capacitation. Dev. Biol. 192, 351-363.
54. Zigler, K. S., McCartney, M. A., Levitan, D. R. and Lessios, H. A. (2005). Sea urchin bindin divergence predicts gamete compatibility. Evolution 59, 2399-2404.