Adaptive maternal and paternal effects: Gamete plasticity in response to parental stress

Functional Ecology

Volumn 28, Issue 3, 2014, Pages 724-733

  Jensen, Natasha ^a   Allen, Richard M ^b,c   Marshall, Dustin J ^d  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b DALHOUSIE UNIVERSITY   (Canada)

^c MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^d MONASH UNIVERSITY   (Australia)

Author keywords

Epigenetics; Non genetic parental effects; Transgenerational phenotypic plasticity

Indexed keywords

ACIDIFICATION; ADAPTATION; ANNELID; ENVIRONMENTAL CHANGE; ENVIRONMENTAL STRESS; GAMETE; HERITABILITY; PARENT-OFFSPRING INTERACTION; PHENOTYPIC PLASTICITY; SALINITY TOLERANCE; TRADE-OFF;

HYDROIDES; TUBICOLAE;

EID: 84900552812     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12195     Document Type: Article

References (54)

1. Agrawal, A.A., Laforsch, C. & Tollrian, R. (1999) Transgenerational induction of defences in animals and plants. Nature, 401, 60-63.
2. Allen, R.M. & Marshall, D.J. (2010) The larval legacy: cascading effects of recruit phenotype on post-recruitment interactions. Oikos, 119, 1977-1983.
3. Allen, J.D. & Pechenik, J.A. (2010) Understanding the effects of low salinity on fertilization success and early development in the sand dollar Echinarachnius parma. Biological Bulletin, 218, 189-199.
4. Basttida-Zavala, J.R. & Ten Hove, H.A. (2002) Revision of Hydroides Gunnerus, 1968 (Polychaeta: Serpulidae) from the western Atlantic region. Beaufortia, 52, 103-178.
5. Birkhead, T.R. & Pizzari, T. (2002) Postcopulatory sexual selection. Nature Reviews Genetics, 3, 262-273.
6. Bonduriansky, R. & Day, T. (2009) Nongenetic inheritance and its evolutionary implications. Annual Review of Ecology Evolution and Systematics, 40, 103-125.
7. Bonduriansky, R. & Head, M. (2007) Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae). Journal of Evolutionary Biology, 20, 2379-2388.
8. Burgess, S.C. & Marshall, D.J. (2011) Temperature-induced maternal effects and environmental predictability. Journal of Experimental Biology, 214, 2329-2336.
9. Byrne, M. (2012) Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Marine Environmental Research, 76, 3-15.
10. Byrne, M., Ho, M., Selvakumaraswamy, P., Nguyen, H.D., Dworjanyn, S.A. & Davis, A.R. (2009) Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proceedings of the Royal Society B-Biological Sciences, 276, 1883-1888.
11. Charmantier, G. (1998) Ontogeny of osmoregulation in crustaceans: a review. Invertebrate Reproduction & Development, 33, 177-190.
12. Chen, Q., Peng, H.Y., Lei, L., Zhang, Y., Kuang, H.B., Cao, Y.J. et al. (2011) Aquaporin3 is a sperm water channel essential for postcopulatory sperm osmoadaptation and migration. Cell Research, 21, 922-933.
13. Crean, A.J., Dwyer, J.M. & Marshall, D.J. (2012) Fertilization is not a new beginning: the relationship between sperm longevity and offspring performance. PLoS One, 7, e49167.
14. Crean, A.J., Dwyer, J.M. & Marshall, D.J. (in press) Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance Ecology.
15. Crean, A.J. & Marshall, D.J. (2008) Adaptive gamete plasticity in a broadcast spawning marine invertebrate. Proceedings of the National Academy of Sciences of the United States of America, 105, 13508-13513.
16. Crean, A.J. & Marshall, D.J. (2009) Coping with environmental uncertainty: dynamic bet-hedging as a maternal effect. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 1087-1096.
17. DeWitt, T.J., Sih, A. & Wilson, D.S. (1998) Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution, 13, 77-81.
18. Gage, M.J.G. & Morrow, E.H. (2003) Experimental evidence for the evolution of numerous, tiny sperm via sperm competition. Current Biology, 13, 754-757.
19. Galloway, L.F. (2001) The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula americana (Campanulaceae). American Journal of Botany, 88, 832-840.
20. Havenhand, J.N. & Schlegel, P. (2009) Near-future levels of ocean acidification do not affect sperm motility and fertilization kinetics in the oyster Crassostrea gigas. Biogeosciences, 6, 3009-3015.
21. Havenhand, J.N., Buttler, F.R., Thorndyke, M.C. & Williamson, J.E. (2008) Near-future levels of ocean acidification reduce fertilization success in a sea urchin. Current Biology, 18, R651-R652.
22. Hintz, J.L. & Lawrence, J.M. (1994) Acclimation of gametes to reduced salinity prior to spawning in Luidia clathrata (Echinodermata, Asteroidea). Marine Biology, 120, 443-446.
23. Hollows, C.F., Johnston, E.L. & Marshall, D.J. (2007) Copper reduces fertilization success and exacerbates Allee effects in the field. Marine Ecology Progress Series, 333, 51-60.
24. Hunt, H.L. & Sheibling, R.E. (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Marine Ecology Progress Series, 155, 269-301.
25. Kraaijeveld, A.R. & Godfray, H.C.J. (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature, 389, 278-280.
26. Levitan, D.R. (1995) The ecology of fertilization in free-spawning invertebrates. Ecology of Marine Larvae (ed. L.R. McEdward), pp. 124-152. CRC Press, Inc., Boca Raton.
27. Levitan, D.R. & Petersen, C. (1995) Sperm limitation in the sea. Trends in Ecology & Evolution, 10, 228-231.
28. Marshall, D.J. (2006) Reliably estimating the effect of toxicants on fertilization success in marine broadcast spawners. Marine Pollution Bulletin, 52, 734-738.
29. Marshall, D.J. (2008) Transgenerational plasticity in the sea: a context-dependent maternal effect across life-history stages. Ecology, 89, 418-427.
30. Marshall, D.J. & Morgan, S.G. (2011) Ecological and evolutionary consequences of linked life-history stages in the sea. Current Biology, 21, R718-R725.
31. Marshall, D.J. & Uller, T. (2007) When is a maternal effect adaptive? Oikos, 116, 1957-1963.
32. Marshall, D.J., Monro, K., Bode, M., Keough, M.J. & Swearer, S. (2010) Phenotype-environment mismatches reduce connectivity in the sea. Ecology Letters, 13, 128-140.
33. McCormick, M.I. (2006) Mothers matter: crowding leads to stressed mothers and smaller offspring in marine fish. Ecology, 87, 1104-1109.
34. Miller, G.M., Watson, S.A., Donelson, J.M., McCormick, M.I. & Munday, P.L. (2012) Parental environment mediates impacts of increased carbon dioxide on a coral reef fish. Nature Climate Change, 2, 858-861.
35. Moran, N.A. (1994) Adaptation and constraint in the complex life-cycles of animals. Annual Review of Ecology and Systematics, 25, 573-600.
36. Moran, D., Muniz Dias, G. & Marshall, D.J. (2010) Associated costs and benefits of a defended phenotype across multiple environments. Functional Ecology, 24, 1299-1305.
37. Mousseau, T.A. & Fox, C.W. (1998) The adaptive significance of maternal effects. Trends in Ecology & Evolution, 13, 403-407.
38. Parker, L.M., Ross, P.M. & O'Connor, W.A. (2009) The effect of ocean acidification and temperature on the fertilization and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850). Global Change Biology, 15, 2123-2136.
39. Parker, L.M., Ross, P.M., O'Connor, W.A., Borysko, L., Raftos, D.A. & Portner, H.O. (2012) Adult exposure influences offspring response to ocean acidification in oysters. Global Change Biology, 18, 82-92.
40. Pechenik, J.A., Pearse, J.S. & Qian, P. (2007) Effects of salinity on spawning and early development of the tube-building polychaete Hydroides elegans in Hong Kong: not just the sperm's fault. Biological Bulletin, 212, 151-160.
41. Pineda, J., Hare, J.A. & Sponaugle, S. (2007) Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography, 20, 22-39.
42. Quinn, G.P. & Keough, M.J. (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.
43. Reed, T.E., Schindler, D.E. & Waples, R.S. (2011) Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conservation Biology, 25, 56-63.
44. Relyea, R.A. (2001) The lasting effects of adaptive plasticity: predator-induced tadpoles become long-legged frogs. Ecology, 82, 1947-1955.
45. Relyea, R.A. (2002) Costs of phenotypic plasticity. American Naturalist, 159, 272-282.
46. Relyea, R.A. (2003) Predators come and predators go: the reversibility of predator-induced traits. Ecology, 84, 1840-1848.
47. Remy, A., Le Galliard, J.F., Gundersen, G., Steen, H. & Andreassen, H.P. (2011) Effects of individual condition and habitat quality on natal dispersal behaviour in a small rodent. Journal of Animal Ecology, 80, 929-937.
48. Reuter, K.E., Lotterhos, K.E., Crim, R.N., Thompson, C.A. & Harley, C.D.G. (2011) Elevated pCO(2) increases sperm limitation and risk of polyspermy in the red sea urchin Strongylocentrotus franciscanus. Global Change Biology, 17, 163-171.
49. Ritchie, H. & Marshall, D.J. (2013) Fertilisation is not a new beginning: sperm environment affects offspring developmental success. Journal of Experimental Biology, 216, 3104-3109.
50. Roller, R.A. & Stickle, W.B. (1994) Effects of adult salinity acclimation on larval survival and early development of Strongylocentrotus droebachiensis and Strongylocentrotus pallidus (Echinodermata, Echinoidea). Canadian Journal of Zoology-Revue Canadienne De Zoologie, 72, 1931-1939.
51. Schluter, D., Price, T.D. & Rowe, L. (1991) Conflicting selection pressures and life-history trade-offs. Proceedings of the Royal Society of London Series B-Biological Sciences, 246, 11-17.
52. Stamps, J.A. (2006) The silver spoon effect and habitat selection by natal dispersers. Ecology Letters, 9, 1179-1185.
53. Tait, N., Atapattu, D. & Browne, R. (1984) Effect of salinity change on early development in Galeolaria caespitosa (Polychaeta: Serpulidae). Marine and Freshwater Research, 35, 483-486.
54. Uller, T. (2008) Developmental plasticity and the evolution of parental effects. Trends in Ecology & Evolution, 23, 432-438.