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.
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References
Allen JD (2008) Size-specific predation on marine invertebrate larvae. Biol Bull 214:42–49
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 422–423:72–80
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
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 44:498–509
Bell G (2013) Evolutionary rescue and the limits of adaptation. Philos Trans R Soc B Biol Sci 368:1–6
Bell G, Collins S (2008) Adaptation, extinction and global change. Evol Appl 1:3–16
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300
Bernardo J (1996a) Maternal effects in animal ecology. Am Zool 36:83–105
Bernardo J (1996b) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36:216–236
Bonduriansky R, Crean AJ, Day T (2012) The implications of nongenetic inheritance for evolution in changing environments. Evol Appl 5:192–201
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 138:55–64
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 166:1–5
Burton T, Metcalfe NB (2014) Can environmental conditions experienced in early life influence future generations? Proc R Soc B 281:1–8
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 49:1–42
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 19:2264–2275
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 155:473–482
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 58:712–719
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 9:1133–1146
Chevin LM, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory. PLoS Biol 8:1–8
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 156:1125–1137
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 198:33–40
Derry AM, Arnott SE (2007) Adaptive reversals in acid rolerance in copepods from lakes recovering from historical stress. Ecol Appl 17:1116–1126
Dickson A, Sabine C, Christian J (2007) Guide to best practices for ocean CO2 measurements. PICES Spec Publ 3:191
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 34:1733–1743
Donelson JM, Salinas S, Munday PL, Shama LNS (2017) Transgenerational plasticity and climate change experiments: Where do we go from here? Glob Chang Biol 24:1–22
Donelson JM, Wong M, Booth DJ, Munday PL (2016) Transgenerational plasticity of reproduction depends on rate of warming across generations. Evol Appl 9:1072–1081
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 160:1835–1843
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 285:1–10
Eirin-Lopez JM, Putnam HM (2019) Marine environmental epigenetics. Annu Rev Mar Sci 11:335–368
Emlet RB (1983) Locomotion, drag, and the rigid skeleton of larval echinoderms. Biol Bull 164:433–445
Fernandez C, Boudouresque CF (2000) Nutrition of the sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) fed different artificial food. Mar Ecol Prog Ser 204:131–141
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 165:97
Gibbin EM, Massamba N’Siala G, Chakravarti LJ, Jarrold MD, Calosi P (2017) The evolution of phenotypic plasticity under global change. Sci Rep 7:1–8
Ho DH, Burggren WW (2010) Epigenetics and transgenerational transfer: a physiological perspective. J Exp Biol 213:3–16
Hobday AJ, Pecl GT (2014) Identification of global marine hotspots: sentinels for change and vanguards for adaptation action. Rev Fish Biol Fish 24:415–425
Hoffmann AA, Sgró CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485
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 148:789–798
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-) 359:80–83
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 543:373–377
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 Change
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 23:657–672
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 180:197–211
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 5:1–7
Lawrence JM, Agatsuma Y (2013) Tripneustes. Sea Urchins: Biology and Ecology. Academic Press, Croydon, UK, pp 491–507
Lenton A, Mcinnes KL, Grady JGO (2015) Marine projections of warming and ocean acidification in the Australasian Region. Aust Meteorol Oceanogr J 65:S1–S28
Lister KN, Lamare MD, Burritt DJ (2015) Pollutant resilience in embryos of the Antarctic sea urchin Sterechinus neumayeri reflects maternal antioxidant status. Aquat Toxicol 161:61–72
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 177:106–115
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 1954:1–7
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 6:732–735
Martinez G, Pérez H (2003) Effect of different temperature regimes on reproductive conditioning in the scallop Argopecten purpuratus. Aquaculture 228:153–167
McAlister JS, Moran AL (2012) Relationships among egg size, composition, and energy: a comparative study of geminate sea urchins. PLoS Biol 7:1–8
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 18:897–907
Mos B, Byrne M, Cowden KL, Dworjanyn SA (2015) Biogenic acidification drives density-dependent growth of a calcifying invertebrate in culture. Mar Biol 162:1541–1558
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 113:39–48
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 6
Mousseau T, Fox C (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407
Munday PL (2014) Transgenerational acclimation of fishes to climate change and ocean acidification. F1000Prime Rep 6:1–7
Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605
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 2.3-0
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 304:159–181
Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science (80-) 333:418–422
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 10:1–19
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 13:1–5
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 18:82–92
Parmesan C (2006) Ecological and Evolutionary Responses to Recent Climate Change. Annu Rev Ecol Evol Syst 37:637–669
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 355:1–9
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 48:12275–12284
Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2018) Linear and nonlinear mixed effects models. R Package version 3.1–140
Prowse TAA, Sewell MA, Byrne M (2017) Three-stage lipid dynamics during development of planktotrophic echinoderm larvae. Mar Ecol Prog Ser 583:149–161
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 218:2365–2372
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) 64:768–775
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 2010–1280
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 9:1082–1095
Ross PM, Parker L, Byrne M (2016) Transgenerational responses of molluscs and echinoderms to changing ocean conditions. ICES J Mar Sci 73:537–549
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 220:1–14
Salinas S, Brown SC, Mangel M, Munch SB (2013) Non-genetic inheritance and changing environments. Non-Genetic Inherit 1:38–50
Schneider C, Rasband W, Eliceiri K (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Shama L, Wegner K (2014) Grandparental effects in marine sticklebacks: transgenerational plasticity across multiple generations. Evol Biol 27:2297–2307
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 9:1096–1111
Shama LNS, Strobel A, Mark FC, Wegner KM (2014) Transgenerational plasticity in marine sticklebacks: Maternal effects mediate impacts of a warming ocean. Funct Ecol 28:1482–1493
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 5:1–7
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 179:617–628
Strathmann RR (1975) Larval feeding in echinoderms. Am Zool 15:717–730
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 58:161–175
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 84:773–784
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Thor P, Dupont S (2015) Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob Chang Biol 21:2261–2271
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 7:627–636
Utting S, Millican P (1997) Techniques for the hatchery conditioning of bivalve broodstocks and the subsequent effect on egg quality and larval viability. Aquaculture 155:45–55
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 160:1913–1926
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 33:831–845
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 517:65–77
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.
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Karelitz, S., Lamare, M.D., Mos, B. et al. Impact of growing up in a warmer, lower pH future on offspring performance: transgenerational plasticity in a pan-tropical sea urchin. Coral Reefs 38, 1085–1095 (2019). https://doi.org/10.1007/s00338-019-01855-z
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DOI: https://doi.org/10.1007/s00338-019-01855-z