Multi-generational responses of a marine polychaete to a rapid change in seawater pCO2

Evolutionary Applications

Volumn 9, Issue 9, 2016, Pages 1082-1095

  Rodríguez Romero, Araceli ^a   Jarrold, Michael D ^b,c   Massamba N'Siala, Gloria ^d,e   Spicer, John I ^b   Calosi, Piero ^b,e  

^a INSTITUTO DE CIENCIAS MARINAS DE ANDALUCÍA   (Spain)

^b UNIVERSITY OF PLYMOUTH   (United Kingdom)

^c JAMES COOK UNIVERSITY   (Australia)

^d UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^e UNIVERSITÉ DU QUÉBEC À RIMOUSKI   (Canada)

Author keywords

adaptive potential; climate change; evolutionary adaptation; fecundity; multi generational experiment; ocean acidification; parental effects; trans generational plasticity

Indexed keywords

EID: 84951818234     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12344     Document Type: Article

References (93)

1. Åkesson, B. 1976. Temperature and life cycle in Ophryotrocha labronica (Polychaeta, Dorvilleidae). Ophelia 15:37–47.
2. 2 world. Proceedings of the Royal Society of London Series B: Biological Sciences 281:20132179.
3. Allen, R. M., and D. Marshall. 2014. Egg size effects across multiple life-history stages in the marine annelid Hydroides diramphus. PLoS One 9:e102253.
4. Angilletta, M. J. Jr. 2009. Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford University Press, New York.
5. Angilletta Jr, M. J., R. S. Wilson, C. A. Navas, and R. S. James. 2003. Tradeoffs and the evolution of thermal reaction norms. Trends in Ecology and Evolution 18:234–240.
6. Arendt, J. 2007. Ecological correlates of body size in relation to cell size and cell number: patterns in flies, fish, fruits and foliage. Biological Reviews 82:241–256.
7. Badyaev, A. V., and T. Uller. 2009. Parental effects in ecology and evolution: mechanisms, processes and implications. Philosophical Transactions of the Royal Society B: Biological Sciences 364:1169–1177.
8. Berglund, A. 1991. To change or not to change sex: a comparison between two Ophryotrocha species (Polychaeta). Evolutionary Ecology 5:128–135.
9. Bickle, M. J. 2009. Geological carbon storage. Nature Geoscience 2:815–818.
10. Bonduriansky, R., A. J. Crean, and D. Troy. 2012. The implications of nongenetic inheritance for evolution in changing environments. Evolutionary Applications 5:192–201.
11. Burton, T., and N. B. Metcalfe. 2014. Can environmental conditions experienced in early life influence future generations? Proceedings of the Royal Society of London Series B: Biological Sciences 281:20140311.
12. 2 vent system. Philosophical Transactions of the Royal Society B: Biological Sciences 368:20120444.
13. Cassai, C., and D. Prevedelli. 1999. Fecundity and reproductive effort in Ophryotrocha labronica (Polychaeta: Dorvilleidae). Marine Biology 133:489–494.
14. Chevin, L.-M., R. Lande, and G. M. Mace. 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biology 8:e1000357.
15. Christie, M. R., M. L. Marine, R. A. French, and M. S. Blouin. 2012. Genetic adaptation to captivity can occur in a single generation. Proceedings of the National Academy of Sciences of the United States of America 109:238–242.
16. Cripps, G., P. Lindeque, and K. J. Flynn. 2014. Have we been underestimating the effects of ocean acidification in zooplankton? Global Change Biology 20:3377–3385.
17. Crispo, E. 2007. The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61:2469–2479.
18. De Wit, P., S. Dupont, and P. Thor. 2015. Selection on oxidative phosphorylation and ribosomal structure as a multigenerational response to ocean acidification in the common copepod Pseudocalanus acuspes. Evolutionary Applications 9:1112–1123.
19. Dickson, A. G., and F. J. A. Millero. 1987. Comparison of the equilibrium constants for the dissociation of carbonic-acid in seawater media. Deep Sea Research Part A. Oceanographic Research Papers 34:1733–1743.
20. Donelson, J. M., P. L. Munday, M. I. McCormick, and C. R. Pitcher. 2012. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nature Climate Change 2:30–32.
21. 2 problem. Annual Review of Marine Science 1:169–192.
22. Dupont, S., N. Dorey, M. Stumpp, F. Melzner, and M. Thorndyke. 2013. Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Marine Biology 160:1835–1843.
23. Fitzer, S. C., G. S. Caldwell, A. J. Close, A. S. Clare, R. C. Upstill-Goddard, and M. G. Bentley. 2012. Ocean acidification induces multi-generational decline in copepod naupliar production with possible conflict for reproductive resource allocation. Journal of Experimental Marine Biology Ecology 418–419:30–36.
24. Foo, S. A., S. A. Dworjanyn, A. G. Poore, and M. Byrne. 2012. Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and ocean acidification: performance of early embryos. PLoS One 7:e42497.
25. Frölicher, T. L., and F. Joos. 2010. Reversible and irreversible impacts of greenhouse gas emissions in multi-century projections with the NCAR global coupled carbon cycle-climate model. Climate Dynamics 35:1439–1459.
26. Gardner, J. L., A. Peters, M. R. Kearney, L. Joseph, and R. Heinsohn. 2011. Declining body size: a third universal response to warming? Trends in Ecology and Evolution 26:285–291.
27. 2 oceans. Nature Climate Change 5:678–682.
28. Ghalambor, C. K., J. K. McKay, S. P. Carroll, and D. N. Reznick. 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21:394–407.
29. Godbold, J. A., and P. Calosi. 2013. Ocean acidification and climate change: advances in ecology and evolution. Philosophical Transactions of the Royal Society B: Biological Sciences 368:20120448.
30. Gomez-Mestre, I., and R. Jovani. 2013. A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation, population viability and genetic variation. Proceedings of the Royal Society of London Series B: Biological Sciences 280:20131869.
31. Gonzalez, A., O. Ronce, R. Ferriere, and M. E. Hochberg. 2013. Evolutionary rescue: an emerging focus at the intersection between ecology and evolution. Philosophical Transactions of the Royal Society B: Biological Sciences 368:20120404.
32. Green, E. J., and D. E. Carrit. 1967. New table for oxygen saturation of seawater. Journal of Marine Research 25:140–147.
33. Ho, D. H., and W. W. Burggren. 2010. Epigenetics and transgenerational transfer: a physiological perspective. Journal of Experimental Biology 213:3–16.
34. Hoffmann, A. A. 1995. Acclimation: increasing survival at a cost. Trends in Ecology and Evolution 10:1–2.
35. Hoffmann, A. A., and C. Sgrò. 2011. Climate change and evolutionary adaptation. Nature 470:479–485.
36. Hofmann, G. E., J. E. Smith, K. S. Johnson, U. Send, L. A. Levin, F. Micheli, A. Paytan et al. 2011. High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS One 6:e28983.
37. IPCC, 2013. Climate Change 2013: The Physical Science Basis: Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York.
38. Jablonka, E., and G. Raz. 2009. Trans-generational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heretic and evolution. The Quarterly Review of Biology 84:131–176.
39. Jensen, N., R. M. Allen, and D. J. Marshall. 2014. Adaptive maternal and paternal effects: gamete plasticity in response to parental stress. Functional Ecology 28:724–733.
40. Kelly, M. W., J. L. Padilla-Gamino, and G. E. Hofmann. 2013. Natural variation, and the capacity to adapt to ocean acidification in the keystone sea urchin Strongylocentrotus purpuratus. Global Change Biology 19:2536–2546.
41. Klironomos, F. D., J. Berg, and S. Collins. 2012. How epigenetic mutations can affect genetic evolution: model and mechanisms. BioEssays 35:571–578.
42. Kroeker, K. J., R. L. Kordas, R. Crim, I. E. Hendriks, L. Ramajo, G. S. Singh, C. M. Duarte et al. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interactions with warming. Global Change Biology 19:1884–1896.
43. La Greca, M., and G. Bacci. 1962. Una nuova specie di Ophryotrocha delle coste tirreniche. Bolletino di zoologia 29:13–23.
44. Lande, R., and S. Shannon. 1996. The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50:434–437.
45. 2 gradients experienced by Artic copepods under winter sea ice. Proceedings of the National Academy of Sciences of the United States of America 110:E4960–E4967.
46. 2-exposure in oxygen minimum zones. Biogeosciences 9:747–757.
47. Malvezzi, A. J., C. S Murray, K. A. Feldheim, J. D. DiBattista, D. Garant, C. J. Gobler, D. D. Chapman et al. 2015. A quantitative genetic approach to assess the evolutionary potential of a coastal marine fish to ocean acidification. Evolutionary Applications 8:352–362.
48. Marshall, D. J., and T. Uller. 2007. When is a maternal effect adaptive? Oikos 116:1957–1963.
49. Massamba-N'Siala, G., R. Simonini, P. Cossu, F. Maltagliati, A. Castelli, and D. Prevedelli. 2011. Life-history and demographic spatial variation in Mediterranean populations of the opportunistic polychaete Ophryotrocha labronica (Polychaeta, Dorvilleidae). Marine Biology 158:1523–1535.
50. Massamba-N'Siala, G., P. Calosi, D. T. Bilton, D. Prevedelli, and R. Simonini. 2012. Life-history and thermal tolerance traits display different thermal plasticities and relationships with temperature in the marine polychaete Ophryotrocha labronica La Greca and Bacci (Dorvilleidae). Journal of Experimental Marine Biology and Ecology 438:109–117.
51. Mehrbach, C., C. H. Culberson, J. E. Hawley, and R. M. Pytkowicz. 1973. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18:897–907.
52. Melzner, F., J. Thomsen, W. Koeve, A. Oschlies, M. A. Gutowska, H. W. Bange, H. P. Hansen et al. 2013. Future ocean acidification will be amplified by hypoxia in coastal habitats. Marine Biology 160:1875–1888.
53. 2 on a coral reef fish. Nature Climate Change 2:858–861.
54. Miller, N. A., A. W. Paganini, and J. H. Stillman. 2013. Differential thermal tolerance and energetic trajectories during ontogeny in porcelain crabs, genus Petrolisthes. Journal of Thermal Biology 38:79–85.
55. Mousseau, T. A., and C. W. Fox. 1998. The adaptive significance of maternal effects. Trends in Ecology and Evolution 13:403–407.
56. Munday, P. L. 2014. Transgenerational acclimation of fishes to climate change and ocean acidification. F1000 Prime Reports 6:99.
57. Munday, P. L., R. R. Warner, K. Monro, J. M. Pandolfi, and D. J. Marshall. 2013. Predicting evolutionary responses to climate change in the sea. Ecology Letters 16:1488–1500.
58. Murray, C. S., A. Malvezzi, C. J. Gobler, and H. Baumann. 2014. Offspring sensitivity to ocean acidification changes seasonally in a coastal marine fish. Marine Ecology Progress Series 504:1–11.
59. Parker, L. M., W. A. O'Connor, D. A. Raftos, H.-O. Pörtner, and P. M. Ross. 2015. Persistence of positive carryover effects in the Oyster, Saccostrea glomerata, following transgenerational exposure to ocean acidification. PLoS One 10:e0132276.
60. Pedersen, S. A., O. J. Håkedal, I. Salaberria, A. Tagliati, L. M. Gustavson, B. M. Jenssen, A. J. Olsen et al. 2014. Multigenerational exposure to ocean acidification during food limitation reveals consequences for copepod scope for growth and vital rates. Environmental Science and Technology 48:12275–12284.
61. Pespeni, M. H., E. Sanford, B. Gaylord, T. M. Hill, J. D. Hosfelt, H. K. Jaris, M. LaVigne et al. 2013. Evolutionary change during experimental ocean acidification. Proceedings of the National Academy of Sciences of the United States of America 110:6937–6942.
62. Peters, R. H. 1983. The Ecological Implications of Body Size. Cambridge University Press, Cambridge.
63. 2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory. US Department of Energy, Oak Ridge, Tennessee.
64. Pigliucci, M., C. J. Murren, and C. D. Schlichting. 2006. Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology 209:2362–2367.
65. Pistevos, J. C. A., P. Calosi, S. Widdicombe, and J. D. D. Bishop. 2011. Will variation among genetic individuals influence species response to global climate change? Oikos 120:675–689.
66. Pörtner, H.-O. 2008. Ecosystem effects of ocean acidification in times of ocean warming: a physiologist's view. Marine Ecology Progress Series 373:203–217.
67. 2 concentrations: lessons from animal physiology and earth history. Journal of Oceanography 60:705–718.
68. Prevedelli, D., G. Massamba-N'Siala, and R. Simonini. 2005. The seasonal dynamics of six species of Dorvilleidae (Polychaeta) in the harbour of La Spezia (Italy). Marine Ecology 26:286–293.
69. Reusch, T. B. H. 2014. Climate change in the oceans: evolutionary versus phenotypically plastic responses of marine animals and plants. Evolutionary Applications 7:104–122.
70. Reznick, D. 1983. The structure of guppy life histories: the trade-off between growth and reproduction. Ecology 64:862–873.
71. Reznick, D. N., and C. K. Ghalambor. 2001. The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112–113:183–198.
72. Salinas, S., S. C. Brown, M. Mangel, and S. B. Munch. 2013. Non-genetic inheritance and changing environments. Non-Genetic Inheritance 1:38–50.
73. Shama, L. N. S., A. Strobel, F. C. Mark, and K. M. Wegner. 2014. Transgenerational plasticity in marine stickleback: maternal effects mediate impacts of a warming ocean. Functional Ecology 28:1482–1493.
74. Shaw, E. C., B. I. McNeil, and B. Tilbrook. 2012. Impacts of ocean acidification in naturally variable coral reef flat ecosystems. Journal of Geophysical Research 117:C03038.
75. Sheridan, J. A., and D. Bickford. 2011. Shrinking body size as an ecological response to climate change. Nature Climate Change 1:401–406.
76. Simonini, R., and D. Prevedelli. 2003. Life history and demography of three populations of Ophryotrocha japonica (Polychaeta: Dorvilleidae). Marine Ecology Progress Series 258:171–180.
77. Simonini, R., V. Grandi, G. Massamba-N'Siala, and D. Prevedelli. 2009. Distribution of the genus Ophryotrocha (Polychaeta) in Italy: new reports and comments on the biogeography of Mediterranean species. Vie et Milieu, 59:79–88.
78. Sokal, R. R., and F. J. Rohlf 1995. Biometry: The Principles and Practice of Statistics in Biological Research, 3rd edn. Freeman W. H., New York.
79. Solan, M., B. J. Cardinale, A. L. Downing, K. A. M. Engelhardt, J. L. Ruesink, and D. S. Srivastava. 2004. Extinction and ecosystem function in the marine benthos. Science 306:1177–1180.
80. Stearns, S. C. 1992. The Evolution of Life Histories. Oxford University Press, New York.
81. Stockwell, C. A., A. P. Hendry, and M. T. Kinnison. 2003. Contemporary evolution meets conservation biology. Trends in Ecology and Evolution 18:94–101.
82. Strong, A. L., K. J. Kroeker, L. T. Teneva, L. A. Mease, and R. P. Kelly. 2014. Ocean acidification 2.0: managing our changing coastal ocean chemistry. BioScience 64:581–592.
83. 2 induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 160:331–340.
84. Suckling, C. C., M. S. Clark, C. Beveridge, L. Brunner, A. D. Hughes, E. M. Harper, E. J. Cook et al. 2014. Experimental influence of pH on the early life-stages of sea urchins II: increasing parental exposure times gives rise to different responses. Invertebrate Reproduction and Development 58:161–175.
85. Sunday, J. M., R. N. Crim, C. D. G. Harley, and M. W. Hart. 2011. Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS One 6:e22881.
86. Sunday, J. M., P. Calosi, S. Dupont, P. L. Munday, J. H. Stillman, and T. B. H. Reusch. 2014. Evolution in an acidifying ocean. Trends in Ecology and Evolution 29:117–125.
87. Szulczewski, M. L., C. W MacMinn, H. J. Herzog, and R. Juanes. 2012. Lifetime of carbon capture and storage as a climate-change mitigation technology. Proceedings of the National Academy of Sciences of the United States of America 109:5185–5189.
88. Thor, P., and S. Dupont. 2015. Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Global Change Biology 21:2261–2271.
89. Tills, O., T. Bitterli, P. Culverhouse, J. I. Spicer, and S. D. Rundle. 2013. A novel application of motion analysis for detecting stress responses in embryos at different stages of development. BMC Bioinformatics 14:37.
90. Underwood, A. J. 1997. Experiments in Ecology. Cambridge University Press, Cambridge.
91. Van Oppen, M. J. H., J. K. Oliver, H. M. Putnam, and R. D. Gates. 2015. Building coral reef resilience through assisted evolution. Proceedings of the National Academy of Sciences of the United States of America 112:2307–2313.
92. West-Eberhard, M. J. 2003. Developmental Plasticity and Evolution. Oxford University Press, Oxford.
93. Wittmann, A. C., and H.-O. Pörtner. 2013. Sensitivities of extant animal taxa to ocean acidification. Nature Climate Change 3:995–1001.