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Impact of growing up in a warmer, lower pH future on offspring performance: transgenerational plasticity in a pan-tropical sea urchin

  • Sam KarelitzEmail author
  • Miles D. Lamare
  • Benjamin Mos
  • Hattie De Bari
  • Symon A. Dworjanyn
  • Maria Byrne
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Abstract

Transgenerational plasticity (TGP) may be an important mechanism for marine organisms to acclimate to climate change stressors including ocean warming (OW) and ocean acidification (OA). Conversely, environmental stress experienced by one generation may have detrimental latent effects on subsequent generations. We examined TGP in the embryos and larvae of the pan-tropical sea urchin, Tripneustes gratilla, in response to OA (pH 7.77), OW (+2 °C), or both OA and OW, OAW (+2 °C, pH 7.77) using a parent (F0) generation reared in treatments from the early juvenile to the mature adult, incorporating gonadogenesis and germline differentiation. Embryos and larvae of acclimated parents were reared in all four treatments to the 2-day-old pluteus stage. Larvae from OA and OAW parents were resilient to the effects of acidification, while larvae from OW and OAW parents were more tolerant to warmer temperature (29 °C). Parental acclimation, however, had predominantly negative effects on the size of offspring with reductions in larval arm lengths by as much as 21.4%, while eggs were up to 21.8% smaller in females raised at 29 °C. We highlight the complexity and trade-offs of TGP in this first transgenerational climate change study on a marine macroinvertebrate where the F0 generation was acclimated over their reproductive life.

Keywords

Transgenerational plasticity Ocean warming Ocean acidification Climate change Acclimation Developmental plasticity 

Notes

Acknowledgements

This research was supported by a grant from the Australian Research Council (MB, SD) and the NSW Environmental Research Trust as well as a PhD scholarship from the University of Otago (SK). The authors would like to thank Eliot Hanrio and Huang-An Li as well as Rich Grainger and Dione Deaker for their assistance in the laboratory. We also thank the National Marine Science Centre at Southern Cross University for their logistical support. This is contribution number 250 of the Sydney Institute of Marine Science.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (DOCX 1053 kb)

References

  1. Allen JD (2008) Size-specific predation on marine invertebrate larvae. Biol Bull 214:42–49Google Scholar
  2. Allen JD (2012) Effects of egg size reductions on development time and juvenile size in three species of echinoid echinoderms: Implications for life history theory. J Exp Mar Bio Ecol 422–423:72–80Google Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  4. Angellitta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509Google Scholar
  5. Bell G (2013) Evolutionary rescue and the limits of adaptation. Philos Trans R Soc B Biol Sci 368:1–6Google Scholar
  6. Bell G, Collins S (2008) Adaptation, extinction and global change. Evol Appl 1:3–16Google Scholar
  7. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300Google Scholar
  8. Bernardo J (1996a) Maternal effects in animal ecology. Am Zool 36:83–105Google Scholar
  9. Bernardo J (1996b) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36:216–236Google Scholar
  10. Bonduriansky R, Crean AJ, Day T (2012) The implications of nongenetic inheritance for evolution in changing environments. Evol Appl 5:192–201Google Scholar
  11. Borges FO, Figueiredo C, Sampaio E, Rosa R, Grilo TF (2018) Transgenerational deleterious effects of ocean acidification on the reproductive success of a keystone crustacean (Gammarus locusta). Mar Environ Res 138:55–64Google Scholar
  12. Bronstein O, Kroh A, Miskelly AD, Smith SDA, Dworjanyn SA, Mos B, Byrne M (2019) Implications of range overlap in the commercially important pan-tropical sea urchin genus Tripneustes (Echinoidea: Toxopneustidae). Mar Biol 166:1–5Google Scholar
  13. Burton T, Metcalfe NB (2014) Can environmental conditions experienced in early life influence future generations? Proc R Soc B 281:1–8Google Scholar
  14. Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr Mar Biol 49:1–42Google Scholar
  15. Byrne M, Ho M, Koleits L (2013) Vulnerability of the calcifying larval stage of the Antarctic sea urchin Sterechinus newmayeri to near-future ocean acidification and warming. Glob Chang Biol 19:2264–2275Google Scholar
  16. Byrne M, Prowse TAA, Sewell MA, Dworjanyn S, Williamson JE, Vaïtilingon D (2008) Maternal provisioning for larvae and larval provisioning for juveniles in the toxopneustid sea urchin Tripneustes gratilla. Mar Biol 155:473–482Google Scholar
  17. Byrne M, Selvakumaraswamy P, Ho MA, Woolsey E, Nguyen HD (2011) Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules. Deep Res Part II Top Stud Oceanogr 58:712–719Google Scholar
  18. Chakravarti LJ, Jarrold MD, Gibbin EM, Christen F, Massamba-N’Siala G, Blier PU, Calosi P (2016) Can trans-generational experiments be used to enhance species resilience to ocean warming and acidification? Evol Appl 9:1133–1146Google Scholar
  19. Chevin LM, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory. PLoS Biol 8:1–8Google Scholar
  20. Clark D, Lamare M, Barker M (2009) Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species. Mar Biol 156:1125–1137Google Scholar
  21. Delorme NJ, Sewell MA (2016) Effects of warm acclimation on physiology and gonad development in the sea urchin Evechinus chloroticus. Comp Biochem Physiol Part A 198:33–40Google Scholar
  22. Derry AM, Arnott SE (2007) Adaptive reversals in acid rolerance in copepods from lakes recovering from historical stress. Ecol Appl 17:1116–1126Google Scholar
  23. Dickson A, Sabine C, Christian J (2007) Guide to best practices for ocean CO2 measurements. PICES Spec Publ 3:191Google Scholar
  24. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part A Oceanogr Res Pap 34:1733–1743Google Scholar
  25. Donelson JM, Salinas S, Munday PL, Shama LNS (2017) Transgenerational plasticity and climate change experiments: Where do we go from here? Glob Chang Biol 24:1–22Google Scholar
  26. Donelson JM, Wong M, Booth DJ, Munday PL (2016) Transgenerational plasticity of reproduction depends on rate of warming across generations. Evol Appl 9:1072–1081Google Scholar
  27. Dupont S, Dorey N, Stumpp M, Melzner F, Thorndyke M (2013) Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar Biol 160:1835–1843Google Scholar
  28. Dworjanyn SA, Byrne M (2018) Impacts of ocean acidification on sea urchin growth across the juvenile to mature adult life-stage transition is mitigated by warming. Proc R Soc B Biol Sci 285:1–10Google Scholar
  29. Eirin-Lopez JM, Putnam HM (2019) Marine environmental epigenetics. Annu Rev Mar Sci 11:335–368Google Scholar
  30. Emlet RB (1983) Locomotion, drag, and the rigid skeleton of larval echinoderms. Biol Bull 164:433–445Google Scholar
  31. Fernandez C, Boudouresque CF (2000) Nutrition of the sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) fed different artificial food. Mar Ecol Prog Ser 204:131–141Google Scholar
  32. Foo SA, Byrne M, Gambi MC (2018) Residing at low pH matters, resilience of the egg jelly coat of sea urchins living at a CO2 vent site. Mar Biol 165:97Google Scholar
  33. Gibbin EM, Massamba N’Siala G, Chakravarti LJ, Jarrold MD, Calosi P (2017) The evolution of phenotypic plasticity under global change. Sci Rep 7:1–8Google Scholar
  34. Ho DH, Burggren WW (2010) Epigenetics and transgenerational transfer: a physiological perspective. J Exp Biol 213:3–16Google Scholar
  35. Hobday AJ, Pecl GT (2014) Identification of global marine hotspots: sentinels for change and vanguards for adaptation action. Rev Fish Biol Fish 24:415–425Google Scholar
  36. Hoffmann AA, Sgró CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485Google Scholar
  37. Hughes AD, Kelly MS, Barnes DKA, Catarino AI, Black KD (2006) The dual functions of sea urchin gonads are reflected in the temporal variations of their biochemistry. Mar Biol 148:789–798Google Scholar
  38. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs JPA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the anthropocene. Science (80-) 359:80–83Google Scholar
  39. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs JPA, Hoogenboom MO, Kennedy EV, Kuo CY, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377Google Scholar
  40. IPCC (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate ChangeGoogle Scholar
  41. Karelitz SE, Uthicke S, Foo SA, Barker MF, Byrne M, Pecorino D, Lamare MD (2017) Ocean acidification has little effect on developmental thermal windows of echinoderms from Antarctica to the tropics. Glob Chang Biol 23:657–672Google Scholar
  42. Lamare MD, Barker MF (1999) In situ estimates of larval development and mortality in the New Zealand sea urchin Evechinus chloroticus (Echinodermata: Echinoidea). Mar Ecol Prog Ser 180:197–211Google Scholar
  43. Lane A, Campanati C, Dupont S, Thiyagarajan V (2015) Trans-generational responses to low pH depend on parental gender in a calcifying tubeworm. Sci Rep 5:1–7Google Scholar
  44. Lawrence JM, Agatsuma Y (2013) Tripneustes. Sea Urchins: Biology and Ecology. Academic Press, Croydon, UK, pp 491–507Google Scholar
  45. Lenton A, Mcinnes KL, Grady JGO (2015) Marine projections of warming and ocean acidification in the Australasian Region. Aust Meteorol Oceanogr J 65:S1–S28Google Scholar
  46. Lister KN, Lamare MD, Burritt DJ (2015) Pollutant resilience in embryos of the Antarctic sea urchin Sterechinus neumayeri reflects maternal antioxidant status. Aquat Toxicol 161:61–72Google Scholar
  47. Lister KN, Lamare MD, Burritt DJ (2016) Dietary pollutants induce oxidative stress, altering maternal antioxidant provisioning and reproductive output in the temperate sea urchin Evichinus chloroticus. Aquat Toxicol 177:106–115Google Scholar
  48. Lister KN, Lamare MD, Burritt DJ (2017) Maternal antioxidant provisioning mitigates pollutant-induced oxidative damage in embryos of the temperate sea urchin Evichinus chloroticus. Sci Rep 1954:1–7Google Scholar
  49. Magnan AK, Colombier M, Billé R, Joos F, Hoegh-Guldberg O, Pörtner HO, Waisman H, Spencer T, Gattuso JP (2016) Implications of the Paris agreement for the ocean. Nat Clim Chang 6:732–735Google Scholar
  50. Martinez G, Pérez H (2003) Effect of different temperature regimes on reproductive conditioning in the scallop Argopecten purpuratus. Aquaculture 228:153–167Google Scholar
  51. McAlister JS, Moran AL (2012) Relationships among egg size, composition, and energy: a comparative study of geminate sea urchins. PLoS Biol 7:1–8Google Scholar
  52. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907Google Scholar
  53. Mos B, Byrne M, Cowden KL, Dworjanyn SA (2015) Biogenic acidification drives density-dependent growth of a calcifying invertebrate in culture. Mar Biol 162:1541–1558Google Scholar
  54. Mos B, Byrne M, Dworjanyn SA (2016) Biogenic acidification reduces sea urchin gonad growth and increases susceptibility of aquaculture to ocean acidification. Mar Environ Res 113:39–48Google Scholar
  55. Mos B, Cowden KL, Nielsen SJ, Dworjanyn SA (2011) Do cues matter? Highly inductive settlement cues don’t ensure high post-settlement survival in sea urchin aquaculture. PLoS One 6Google Scholar
  56. Mousseau T, Fox C (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407Google Scholar
  57. Munday PL (2014) Transgenerational acclimation of fishes to climate change and ocean acidification. F1000Prime Rep 6:1–7Google Scholar
  58. Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605Google Scholar
  59. Okansen J, Blanchet F, Kindt R, Legendre P, Minchin P, O’Hara R, Simpson G, Solymos P, Stevens M, Wagner H (2015) Vegan: community ecology package. R package version 2.3-0Google Scholar
  60. Otero-Villanueva MDM, Kelly MS, Burnell G (2004) How diet influences energy partitioning in the regular echinoid Psammechinus miliaris; constructing an energy budget. J Exp Mar Bio Ecol 304:159–181Google Scholar
  61. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science (80-) 333:418–422Google Scholar
  62. Parker LM, Connor WAO, Raftos DA, Pörtner H, Ross PM (2015) Persistence of positive carryover effects in the oyster, Saccostrea glomerata, following transgenerational exposure to ocean acidification. PLoS One 10:1–19Google Scholar
  63. Parker LM, O’Connor WA, Byrne M, Coleman RA, Virtue P, Dove M, Gibbs M, Spohr L, Scanes E, Ross PM (2017) Adult exposure to ocean acidification is maladaptive for larvae of the Sydney rock oyster Saccostrea glomerata in the presence of multiple stressors. Biol Lett 13:1–5Google Scholar
  64. Parker LM, Ross PM, O’Connor WA, Borysko L, Raftos DA, Pörtner HO (2012) Adult exposure influences offspring response to ocean acidification in oysters. Glob Chang Biol 18:82–92Google Scholar
  65. Parmesan C (2006) Ecological and Evolutionary Responses to Recent Climate Change. Annu Rev Ecol Evol Syst 37:637–669Google Scholar
  66. Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrake TC, Chen IC, Clark TD, Colwell RK, Danielsen F, Evengård B, Falconi L, Ferrier S, Frusher S, Garcia RA, Griffis RB, Hobday AJ, Janion-Scheepers C, Jarzyna MA, Jennings S, Lenoir J, Linnetved HI, Martin VY, McCormack PC, McDonald J, Mitchell NJ, Mustonen T, Pandolfi JM, Pettorelli N, Popova E, Robinson SA, Scheffers BR, Shaw JD, Sorte CJB, Strugnell JM, Sunday JM, Tuanmu MN, Vergés A, Villanueva C, Wernberg T, Wapstra E, Williams SE (2017) Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355:1–9Google Scholar
  67. Pedersen SA, Håkedal OJ, Salaberria I, Tagliati A, Gustavson LM, Jenssen BM, Olsen AJ, Altin D (2014) Multigenerational exposure to ocean acidification during food limitation reveals consequences for copepod scope for growth and vital rates. Environ Sci Technol 48:12275–12284Google Scholar
  68. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2018) Linear and nonlinear mixed effects models. R Package version 3.1–140Google Scholar
  69. Prowse TAA, Sewell MA, Byrne M (2017) Three-stage lipid dynamics during development of planktotrophic echinoderm larvae. Mar Ecol Prog Ser 583:149–161Google Scholar
  70. Putnam HM, Gates RD (2015) Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J Exp Biol 218:2365–2372Google Scholar
  71. Rahman S, Tsuchiya M, Uehara T (2009) Effects of temperature on hatching rate, embryonic development and early larval survival of the edible sea urchin, Tripneustes gratilla. Biologia (Bratisl) 64:768–775Google Scholar
  72. Robbins L, Hansen M, Kleypas J, Meylan S (2010) CO2calc: a user-friendly carbon calculator for windows, Mac OS X, and iOS (iPhone): US Geol suvey open file Rep 2010–1280Google Scholar
  73. Rodríguez-Romero A, Jarrold MD, Massamba-N’Siala G, Spicer JI, Calosi P (2016) Multi-generational responses of a marine polychaete to a rapid change in seawater pCO2. Evol Appl 9:1082–1095Google Scholar
  74. Ross PM, Parker L, Byrne M (2016) Transgenerational responses of molluscs and echinoderms to changing ocean conditions. ICES J Mar Sci 73:537–549Google Scholar
  75. Russell MP (1998) Resource allocation plasticity in sea urchins: rapid, diet induced, phenotypic changes in the green sea urchin, Strongylocentrotus droebachiensis (Müller). J Exp Mar Bio Ecol 220:1–14Google Scholar
  76. Salinas S, Brown SC, Mangel M, Munch SB (2013) Non-genetic inheritance and changing environments. Non-Genetic Inherit 1:38–50Google Scholar
  77. Schneider C, Rasband W, Eliceiri K (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675Google Scholar
  78. Shama L, Wegner K (2014) Grandparental effects in marine sticklebacks: transgenerational plasticity across multiple generations. Evol Biol 27:2297–2307Google Scholar
  79. Shama LNS, Mark FC, Strobel A, Lokmer A, John U, Mathias Wegner K (2016) Transgenerational effects persist down the maternal line in marine sticklebacks: gene expression matches physiology in a warming ocean. Evol Appl 9:1096–1111Google Scholar
  80. Shama LNS, Strobel A, Mark FC, Wegner KM (2014) Transgenerational plasticity in marine sticklebacks: Maternal effects mediate impacts of a warming ocean. Funct Ecol 28:1482–1493Google Scholar
  81. Sheppard Brennand H, Soars N, Dworjanyn SA, Davis AR, Byrne M (2010) Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS One 5:1–7Google Scholar
  82. Shu L, Suter MJF, Laurila A, Räsänen K (2015) Mechanistic basis of adaptive maternal effects: egg jelly water balance mediates embryonic adaptation to acidity in Rana arvalis. Oecologia 179:617–628Google Scholar
  83. Strathmann RR (1975) Larval feeding in echinoderms. Am Zool 15:717–730Google Scholar
  84. Suckling CC, Clark MS, Beveridge C, Brunner L, Hughes D, Harper EM, Cook EJ, Davies AJ, Peck S, Suckling CC, Clark MS, Beveridge C, Brunner L, Hughes AD, Harper EM, Cook EJ, Davies AJ, Peck LS (2014) Experimental influence of pH on the early life-stages of sea urchins II: increasing parental exposure times gives rise to different responses. Invertebr Reprod Dev 58:161–175Google Scholar
  85. Suckling CC, Clark MS, Richard J, Morley SA, Thorne MAS, Harper EM, Peck LS (2015) Adult acclimation to combined temperature and pH stressors significantly enhances reproductive outcomes compared to short-term exposures. J Anim Ecol 84:773–784Google Scholar
  86. R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  87. Thor P, Dupont S (2015) Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob Chang Biol 21:2261–2271Google Scholar
  88. Torda G, Donelson JM, Aranda M, Barshis DJ, Bay L, Berumen ML, Bourne DG, Cantin N, Foret S, Matz M, Miller DJ, Moya A, Putnam HM, Ravasi T, Van Oppen MJH, Thurber RV, Vidal-Dupiol J, Voolstra CR, Watson SA, Whitelaw E, Willis BL, Munday PL (2017) Rapid adaptive responses to climate change in corals. Nat Clim Chang 7:627–636Google Scholar
  89. Utting S, Millican P (1997) Techniques for the hatchery conditioning of bivalve broodstocks and the subsequent effect on egg quality and larval viability. Aquaculture 155:45–55Google Scholar
  90. Uthicke S, Soars N, Foo S, Byrne M (2013) Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei. Mar Biol 160:1913–1926Google Scholar
  91. Uthicke S, Liddy M, Nguyen HD, Byrne M (2014) Interactive effects of near-future temperature increase and ocean acidification on physiology and gonad development in adult Pacific sea urchin, Echinometra sp. A. Coral Reefs 33:831–845Google Scholar
  92. Wong JM, Kozal LC, Leach TS, Hoshijima U, Hofmann GE (2019) Transgenerational effects in an ecological context: conditioning of adult sea urchins to upwelling conditions alters maternal provisioning and progeny phenotype. J Exp Mar Bio Ecol 517:65–77Google Scholar

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Authors and Affiliations

  1. 1.Department of Marine ScienceUniversity of OtagoDunedinNew Zealand
  2. 2.National Marine Science CentreSouthern Cross UniversityCoffs HarbourAustralia
  3. 3.School of Medical Sciences and School of Life and Environmental SciencesUniversity of SydneySydneyAustralia

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