Skip to main content

Advertisement

SpringerLink
Log in

Within- and trans-generational responses to combined global changes are highly divergent in two congeneric species of marine annelids

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Trans-generational plasticity (TGP) represents a primary mechanism for guaranteeing species persistence under rapid global changes. To date, no study on TGP responses of marine organisms to global change scenarios in the ocean has been conducted on phylogenetically closely related species, and we thus lack a true appreciation for TGP inter-species variation. Consequently, we examined the tolerance and TGP of life-history and physiological traits in two annelid species within the genus Ophryotrocha: one rare (O. robusta) and one common (O. japonica). Both species were exposed over two generations to ocean acidification (OA) and warming (OW) in isolation and in combination (OAW). Warming scenarios led to a decrease in energy production together with an increase in energy requirements, which was lethal for O. robusta before viable offspring could be produced by the F1. Under OA conditions, O. robusta was able to reach the second generation, despite showing lower survival and reproductive performance when compared to control conditions. This was accompanied by a marked increase in fecundity and egg volume in F2 females, suggesting high capacity for TGP under OA. In contrast, O. japonica thrived under all scenarios across both generations, maintaining its fitness levels via adjusting its metabolomic profile. Overall, the two species investigated show a great deal of difference in their ability to tolerate and respond via TGP to future global changes. We emphasize the potential implications this can have for the determination of extinction risk, and consequently, the conservation of phylogenetically closely related species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request and are available on the PANGAEA data library.

References

  • Angiletta MJ (2009) Thermal Adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford

    Google Scholar 

  • Bouquet J-M, Troedsson C, Novac A, Reeve M, Lechtenbörger AK, Massart W et al (2018) Increased fitness of a key appendicularian zooplankton species under warmer, acidified seawater conditions. PLoS ONE 13(1):e0190625

    PubMed  PubMed Central  Google Scholar 

  • Bozinovic F, Calosi P, Spicer JI (2011) Physiological correlates of geographic range in animals. Annu Rev Ecol Evol Syst 42:155–179

    Google Scholar 

  • Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365

    CAS  PubMed  Google Scholar 

  • Calosi P, Bilton DT, Spicer JI (2008) Thermal tolerance, acclimatory capacity and 531 vulnerability to global climate change. Biol Lett 4:99–102

    PubMed  Google Scholar 

  • Calosi P, Bilton DT, Spicer JI, Votier SC, Atfield A (2010) What determines a species’ geographical range? Thermal biology and latitudinal range size relationships in European diving beetles (Coleoptera: Dytiscidae). J Anim Ecol 79:194–204

    PubMed  Google Scholar 

  • Calosi P, De Wit P, Thor P, Dupont S (2016) Will life find a way? Evolution of marine species under global change. Evol Appl 9:1035–1042

    PubMed  PubMed Central  Google Scholar 

  • Calosi P, Putnam HM, Twitchett RJ, Vermandele F (2019) Marine metazoan modern mass extinction: improving predictions by integrating fossil, modern, and physiological data. Annu Rev Mar Sci 11:369–390

    Google Scholar 

  • Chakravarti LJ, Jarrold M, 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 9:113–1146

    Google Scholar 

  • Chevin LM, Collins S, Lefèvre F (2013) Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field. Funct Ecol 27:967–979

    Google Scholar 

  • Christie MR, Marine ML, French RA, Blouin MS (2012) Genetic adaptation to captivity can occur in a single generation. Proc Natl Acad Sci USA 109:238–242

    CAS  PubMed  Google Scholar 

  • Dickson AG (1990) Standard potential of the (AgCl (s) + ½ H2 (g) = Ag (s) + HCl (aq)) cell and the dissociation constant of bisulfate ion in synthetic sea water from 273.15 to 318.15 K. J Chem Thermodyn 215:29–43

    Google Scholar 

  • Côté IM, Darling ES, Brown CJ (2016) Interactions among ecosystem stressors and their importance in conservation. Proc R Soc B Biol Sci 283:20152592

    Google Scholar 

  • Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part 1. Oceanogr Res Pap 34:1733–1743

    CAS  Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Spec Publ 3:1–191

    Google Scholar 

  • Donelson JM, Munday PL, McCormick MI, Pitcher CR (2012) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Change 2:30–32

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Donelson JM, Salinas S, Munday PL, Shama LN (2018) Transgenerational plasticity and climate change experiments: Where do we go from here? Glob Change Biol 24:13–34

    Google Scholar 

  • Donelson JM, Sunday JM, Figueira WF, Gaitan-Espitia JD, Hobday AJ, Johnson CR et al (2019) Understanding interactions between plasticity, adaptation and range shifts in response to marine environmental change. Philos Trans R Soc B 374:20180186

    Google Scholar 

  • Duncan EJ, Gluckman PD, Dearden PK (2014) Epigenetics, plasticity, and evolution: How do we link epigenetic change to phenotype? J Exp Zool B Mol Dev Evol 322:208–220

    CAS  PubMed  Google Scholar 

  • Eirin-Lopez J, Putnam M (2019) Marine environmental epigenetics. Ann Rev Mar Sci 11:335–368

    PubMed  Google Scholar 

  • Fox RJ, Donelson JM, Schunter C, Ravasi T, Gaitan-Espitia JD (2019) Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos Trans R Soc B 374:20180174

    Google Scholar 

  • Garland T Jr, Adolph SC (1994) Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool 67:797–828

    Google Scholar 

  • Ghalambor CK, McKay J, Carroll S, Reznick D (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407

    Google Scholar 

  • Ghalambor CK, Hoke KL, Ruell EW, Fischer EK, Reznick DN, Hughes KA (2015) Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525:372

    CAS  PubMed  Google Scholar 

  • Gibbin EM, Massamba N’Siala G, Chakravarti LJ, Jarrold MD, Calosi P (2017a) The evolution of phenotypic plasticity under global change. Sci Rep 7:17253

    PubMed  PubMed Central  Google Scholar 

  • Gibbin EM, Chakravarti LJ, Jarrold MD, Christen F, Turpin V, Massamba N’Siala G, Blier PU, Calosi P (2017b) Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life-history and physiology in a marine metazoan? J Exp Biol 220:551–563

    PubMed  Google Scholar 

  • Gibson R, Atkinson R, Gordon J, Smith I, Hughes D (2012) 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 Annu Rev Annu Rev 49:1–42

    Google Scholar 

  • Griffith AW, Gobler CJ (2017) Transgenerational exposure of North Atlantic bivalves to ocean acidification renders offspring more vulnerable to low pH and additional stressors. Sci Rep 7:11394

    PubMed  PubMed Central  Google Scholar 

  • Hall POJ, Aller RC (1992) Rapid, small-volume, flow injection analysis for ΣCO2 and NH4+ in marine and freshwaters. Limnol Oceanogr 37:1113–1119

    CAS  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation, mechanisms and processes in physiological evolution. Oxford University Press, Oxford

    Google Scholar 

  • Hofmann GE (2017) Ecological epigenetics in marine metazoans. Front Mar Sci 4:4

    Google Scholar 

  • Hoshijima U, Hofmann GE (2019) Variability of seawater chemistry in a kelp forest environment is linked to in situ transgenerational effects in the purple sea urchin, Strongylocentrotus purpuratus. Front Mar Sci 6:62

    Google Scholar 

  • Husson F, Lê S, Pagès J (2017) Exploratory multivariate analysis by example using R. Chapman and Hall, London

    Google Scholar 

  • Hutchinson GE (1978) An Introduction to Population Ecology. Yale University Press, New Haven

    Google Scholar 

  • IPCC (2014) Climate Change 2014: 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

    Google Scholar 

  • Jarrold MD, Chakravarti LJ, Gibbin EM, Christen F, Massamba-N'Siala G, Blier PU, Calosi P (2019) Life-history trade-offs and limitations associated with phenotypic adaptation under future ocean warming and elevated salinity. Philos Trans R Soc B 374:20180428

    Google Scholar 

  • Karelitz S, Lamare MD, Mos B, De Bari H, Dworjanyn SA, Byrne M (2019) 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

    Google Scholar 

  • Koenigstein S, Mark FC, Gößling-Reisemann S, Reuter H, Pörtner HO (2016) Modelling climate change impacts on marine fish populations: process-based integration of ocean warming, acidification and other environmental drivers. Fish Fish 17:972–1004

    Google Scholar 

  • Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Durate CM, Gattuso JP (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19:1884–1896

    Google Scholar 

  • Lewis E, Wallace D (1998) CO2SYS program. Carbon Dioxyde Information Analysis Center, Oak Ridge National Laboratory Environmental Sciences Division, Oak Ridge

    Google Scholar 

  • Lu W, Kimball E, Rabinowitz JD (2006) A high-performance liquid chromatography-tandem mass spectrometry method for quantitation of nitrogen-containing intracellular metabolites. J Am Soc Mass Spectrom 17:37–50

    CAS  PubMed  Google Scholar 

  • Lyons KG, Brigham CA, Traut BH, Schwartz MW (2005) Rare species and ecosystem functioning. Conserv Biol 19:1019–1024

    Google Scholar 

  • Marshall DJ (2008) Transgenerational plasticity in the sea: Context-dependent maternal effects across the life history. Ecology 89:418–427

    PubMed  Google Scholar 

  • Marshall DJ, Keough MJ (2008) The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol 53:1–60

    Google Scholar 

  • Massamba-N'Siala G, Simonini R, Cossu P, Prevedelli D (2011) Life-history and demographic spatial variation in Mediterranean populations of the opportunistic polychaete Ophryotrocha labronica (Polychaeta, Dorvilleidae). Mar Biol 158:1523–1535

    Google Scholar 

  • Massamba-N'Siala G, Calosi P, Bilton DT, Prevedelli D, Simonini R (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). J Exp Mar Biol Ecol 438:109–117

    Google Scholar 

  • Mehrbach C, Culberson CH, Hawley JE, Pytkowicx RM (1973) Measurement of the apparent dissociation constant of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    CAS  Google Scholar 

  • Melatunan S, Calosi P, Rundle SD, Widdicombe S, Moody AJ (2013) Effects of ocean acidification and elevated temperature on shell plasticity and its energetic basis in an intertidal gastropod. Mar Ecol Prog Ser 472:155–168

    CAS  Google Scholar 

  • Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M, Thorndyke MC, Bleich M, Pörtner HO (2009) Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeoscoences 6:2313–2331

    CAS  Google Scholar 

  • Miller GM, Watson SA, McCormick MI, Munday PL (2013) Increased CO2 stimulates reproduction in coral reef fish. Glob Change Biol 19:3037–3045

    Google Scholar 

  • Mouillot D, Bellwood DR, Baraloto C, Chave J, Galzin R et al (2013) Rare species support vulnerable functions in high-diversity ecosystems. PLoS Biol 11:e1001569

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    CAS  PubMed  Google Scholar 

  • Munday PL, McCormick MI, Nilsson GE (2012) Impact of global warming and rising CO2 levels on coral reef fishes: what hope for the future? J Exp Biol 215:3865–3873

    CAS  PubMed  Google Scholar 

  • Parker LM, Ross PM, O'Connor WA, Borysko L, Raftos DA, Pörtner HO (2012) Adult exposure influence offspring response to ocean acidification in oysters. Glob Change Biol 18:82–92

    Google Scholar 

  • Paxton H, Åkesson B (2010) The Ophryotrocha labronica group (Annelida: Dorvilleidae)—with the description of seven new species. Zootaxa 2713:1–24

    Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. JHU Press, Baltimore

    Google Scholar 

  • Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367

    PubMed  Google Scholar 

  • Pistevos JC, Calosi P, Widdicombe S, Bishop JD (2011) Will variation among genetic individuals influence species responses to global climate change? Oikos 120:675–689

    Google Scholar 

  • Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217

    Google Scholar 

  • Pörtner HO, Gutt J (2016) Impacts of climate variability and change on (Marine) animals: physiological underpinnings and evolutionary consequences. Integr Comp Biol 56:31–44

    PubMed  Google Scholar 

  • Prevedelli D, Massamba-N'Siala G, Simonini R (2005) The seasonal dynamics of six species of Dorvilleidae (Polychaeta) in the harbour of La Spezia (Italy). Mar Ecol 26:286–293

    Google Scholar 

  • Prevedelli D, Massamba-N’Siala G, Simonini R (2006) Gonochorism vs. hermaphroditism: relationship between life history and fitness in three species of Ophryotrocha (Polychaeta: Dorvilleidae) with different forms of sexuality. J Anim Ecol 75:203–2012

    PubMed  Google Scholar 

  • Quintero I, Wiens JJ (2013) Rates of projected climate change dramatically exceed past rates of climatic niche evolution among vertebrate species. Ecol Lett 16:1095–1103

    PubMed  Google Scholar 

  • Reusch TB (2014) Climate change in the oceans: evolutionary versus phenotypically plastic responses. Evol Appl 7:104–122

    PubMed  Google Scholar 

  • Rodriguez-Romero A, Jarrold MD, Massamba-N'Siala G, Spicer JI, Calosi P (2016) Multi-generational responses of a marine polycheate to a rapid change in seawater pCO2. Evol Appl 9:1082–1095

    CAS  PubMed  Google Scholar 

  • RStudio Team (2015) RStudio: Integrated Development for R. RStudio, Inc., Boston, https://www.rstudio.com/

  • Ruzicka J, Hansen EH (1988) Flow injection analysis, 2nd edn. Wiley, Hoboken

    Google Scholar 

  • Salinas S, Munch SB (2012) Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol Lett 15:159–163

    PubMed  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shama LNS, Wegner KM (2014) Grandparental effects in marine sticklebacks: transgenerational plasticity across multiple generations. J Evol Biol 27:2297–2307

    CAS  PubMed  Google Scholar 

  • Shama LNS, Strobel A, Mark FC, Wegner KM (2014) Transgenerational plasticity in marine stickleback: maternal effects mediate impacts of a warming ocean. Funct Ecol 28:1482–1493

    Google Scholar 

  • Shama LN, Mark FC, Strobel A, Lokmer A, John U, Wegner KM (2016) Transgenerational effects persist down the maternal line in marine sticklebacks: gene expression matches physiology in a warming ocean. Evol Appl 9:1096–1111

    CAS  PubMed  PubMed Central  Google Scholar 

  • Simonini R (2002) Distribution and ecology of the genus Ophryotrocha (Polychaeta: Dorvilleidae) in Italian harbors and lagoons. Vie et Milieu 52:59–65

    Google Scholar 

  • Simonini R, Prevedelli D (2003) Life history and demography of three populations of Ophryotrocha japonica (Polychaeta: Dorvilleidae). Mar Ecol Prog Ser 171:171–180

    Google Scholar 

  • Simonini R, Massamba-N’Siala G, Grandi V, Prevedelli D (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

    Google Scholar 

  • Simonini R, Grandi V, Massamba-N'Siala G, Martino MP, Castelli A, Prevedelli D (2010) Diversity, habitat affinities and diet of Ophryotrocha species (Polychaeta, Dorvilleidae) living in Mediterranean harbour habitats. Vie et Milieu 60:27–38

    Google Scholar 

  • Small DP (2013) The effects of elevated temperature and pCO2 on the developmental eco-physiology of the European lobster, Homarus gammarus (L.). PhD thesis, Plymouth University Press

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Stumpp M, Hu MY, Melzner F, Gutowska MA, Dorey N, Himmerkus N, Holtmann WC, Dupont ST, Thorndyke MC, Bleich M (2012) Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proc Natl Acad Sci 9:18192–18197

    Google Scholar 

  • Sunday JM, Calosi P, Dupont S, Munday PL, Stillman JH, Reusch TB (2014) Evolution in an acidifying ocean. Trends Ecol Evol 29:117–125

    PubMed  Google Scholar 

  • Thor P, Dupont S (2015) Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob Change Biol 21:432–438

    Google Scholar 

  • Thornhill DJ, Dahlgren TG, Halanych KM (2009) Evolution and ecology of Ophryotrocha (Dorvilleidae, Eunicida). In: Shain DH (ed) Annelids in Modern Biology. Wiley-Blackwell, New Jersey, pp 242–256

    Google Scholar 

  • Underwood T (1996) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge

    Google Scholar 

  • Van Oppen MJ, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. Proc Natl Acad Sci 112:2307–2313

    PubMed  PubMed Central  Google Scholar 

  • Vehmaa A, Brutemark A, Engström-Öst J (2012) Maternal effects may act as an adaptation mechanism for copepods facing pH and temperature changes. PLoS ONE 7:e48538

    CAS  PubMed  PubMed Central  Google Scholar 

  • Viant MR (2007) Metabolomics of aquatic organisms: the new ‘omics’ on the block. Mar Ecol Prog Ser 332:301–306

    CAS  Google Scholar 

  • Vidal DE, Horne AJ (2009) Inheritance if mercury tolerance in the aquatic oligochaete Tubifidex tubifidex. Environ Toxicol Chem 22:2130–2135

    Google Scholar 

  • Violle C, Thuiller W, Mouquet N, Munoz F, Kraft NJ, Cadotte MW, Livingstone SW, Mouillot D (2017) Functional rarity: the ecology of outliers. Trends Ecol Evol 32:356–367

    PubMed  PubMed Central  Google Scholar 

  • Walther K, Anger K, Pörtner HO (2010) Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54 vs. 79 N). Mar Ecol Prog Ser 417:159–170

    Google Scholar 

  • Walther K, Sartoris FJ, Pörtner HO (2011) Impacts of temperature and acidification on larval calcium incorporation of the spider crab Hyas araneus from different latitudes (54 vs. 79 N). Mar Biol 158:2043–2053

    CAS  Google Scholar 

  • Welch MJ, Watson SA, Welsh JQ, McCormick MI, Munday PL (2014) Effects of elevated CO 2 on fish behaviour undiminished by transgenerational acclimation. Nat Clim Change 4:1086

    CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Sarah Jacques and Steeven Ouellet for assisting with DIC analyses, and Daniel Small and Nicholas Beaudreau for the attentive linguistic revision of this MS. This work was financed by NSERC Discovery Program grant (RGPIN-2015-06500), Programme Établissement de Nouveaux Chercheurs Universitaires of FRQNT (No. 199173), by the Fond Institutionnel de Recherche of the Université du Québec à Rimouski all awarded to PC, and co-funded by the European Union through the Marie Skłodowska-Curie Post-doctoral Fellowship (Proposal Number: 659359) awarded to GMN. FV and PC are members of Québec-Océan FRQNT-funded research excellence networks. We finally thank the three anonymous reviewers for their insightful comments and suggestions.

Author information

Author notes

  1. Fanny Noisette & Mathieu Babin

    Present address: Institut des Sciences de La Mer, Université du Québec à Rimouski, 310 Allée des Ursulines, Rimouski, QC, G5L 3A1, Canada

Authors and Affiliations

  1. Département de Biologie, Chimie et Géographie, Université du Québec à Rimouski, 300 Allée des Ursulines, Rimouski, QC, G5L 3A1, Canada

    Cynthia Thibault, Gloria Massamba-N’Siala, Fanny Noisette, Fanny Vermandele & Piero Calosi

  2. Centre d’Écologie Fonctionnelle et Évolutive (CEFE- CNRS), UMR 5175, Montpellier Cedex 5, France

    Gloria Massamba-N’Siala

Authors
  1. Cynthia Thibault
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gloria Massamba-N’Siala
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fanny Noisette
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fanny Vermandele
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mathieu Babin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Piero Calosi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Piero Calosi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for sampling, care and experimental use of organisms for the study have been followed and all necessary approvals have been obtained.

Additional information

Responsible Editor: A.E. Todgham.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Reviewed by undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 267 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thibault, C., Massamba-N’Siala, G., Noisette, F. et al. Within- and trans-generational responses to combined global changes are highly divergent in two congeneric species of marine annelids. Mar Biol 167, 41 (2020). https://doi.org/10.1007/s00227-019-3644-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-019-3644-8

Search

Navigation