Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The maternal effects of dietary restriction on Dnmt expression and reproduction in two clones of Daphnia pulex

Heredity (2022)Cite this article

Subjects

Abstract

The inheritance of epigenetic marks induced by environmental variation in a previous generation is broadly accepted as a mediator of phenotypic plasticity. Transgenerational effects linking maternal experiences to changes in morphology, gene expression, and life history of successive generations are known across many taxa. While the number of studies linking epigenetic variation to ecological maternal effects is increasing rapidly, few if any attempts have been made to investigate molecular mechanisms governing epigenetic functions in the context of ecologically relevant maternal effects. Daphnia make an ideal model for investigating molecular epigenetic mechanisms and ecological maternal effects because they will reproduce asexually in the lab. Daphnia are also known to have strong maternal effects, involving a variety of traits and environmental variables. Using two clones of Daphnia pulex, we investigated the plasticity of life history and DNA methyltransferase (Dnmt) gene expression with respect to food limitation within and across generations. We found strong evidence of genotypic variation of responses of life history and Dnmt expression to low food diets, both within and across generations. In general, effects of offspring diet were larger than either the direct maternal effect or offspring-maternal environment interactions, but the direction of the maternal effect was usually in the opposite direction of the within-generation effect. For both life history and Dnmt expression, we also found that when offspring had low food, effects of the maternal environment were stronger than when offspring had high food.

This is a preview of subscription content, access via your institution

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

Buy

All prices are NET prices.

Fig. 1: Experimental design setup.
Fig. 2: Box plots of the effects of diet and maternal diet on the age at maturation in the clones Tro-3 and Morg-5, for both generations.
Fig. 3: Waffle plot representation of diet effect on reproduction type in G0 where each square represents one individual.
Fig. 4: Waffle plot representation of the effect of diet on reproduction type in G1.
Fig. 5: Normalized relative fold expression and standard error for DNA methyltransferases 1, 2, and 3 in the D. pulex clones Tro-3 and Morg-5.

Data availability

Data can be accessed at Dryad: https://doi.org/10.5061/dryad.1c59zw3zz.

References

  • Aagaard-Tillery KM, Grove K, Bishop J, Ke X, Fu Q, McKnight R et al. (2008) Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 41:91–102

    Article  CAS  Google Scholar 

  • Alekseev V, Lampert W (2001) Maternal control of resting – egg production in Daphnia. Nature 414:899–901

    Article  CAS  Google Scholar 

  • Anderson OS, Sant KE, Dolinoy DC (2012) Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. J Nutritional Biochem 23:853–859

    Article  CAS  Google Scholar 

  • Agrawal AA, Laforsch C, Tollrian R (1999) Transgenerational induction of defenses in animals and plants. Nature 401:60–63

    Article  CAS  Google Scholar 

  • Asselman J, De Coninck DIM, Vandegehuchte MB, Jansen M, Decaestecker E, De Meester L, Busshe JV, Vanhaecke L, Janssen CR, De Schamphelaere KAC (2015) Global cytosine methylation in Daphnia magna depends on genotype, environment, and their interaction. Environ Toxicol 34:5

    Google Scholar 

  • Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36:83–105

    Article  Google Scholar 

  • Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412

    Article  CAS  Google Scholar 

  • Bewick AJ, Vogel KJ, Moore AJ, Schmitz RJ (2017) Evolution of DNA methylation across insects. Mol Biol Evol 34:654–665

    CAS  Google Scholar 

  • Bird A (2007) Perceptions of epigenetics. Nature 447:396–398

    Article  CAS  Google Scholar 

  • Boersma M (1995) The allocation of resources to reproduction in Daphnia galeata: against the odds? Ecology 76(4):121–1261

    Article  Google Scholar 

  • Boersma M (1997) Offspring size in Daphnia: does it pay to be overweight? Hydrobiologia 360:79–88

    Article  Google Scholar 

  • Boycott AE, Diver C (1923) On the inheritance of the sinistrality in Limnea peregra. Proc R Soc Lond B 95:207–213

    Article  Google Scholar 

  • Brett MT (1993) Resource quality effects on Daphnia longispina offspring fitness. J Plankton Res 15(4):403–412

    Article  Google Scholar 

  • Burns CW (1995) Effects of crowding and different food levels on growth and reproductive investment of Daphnia. Oecologia 101:234–244

    Article  Google Scholar 

  • Cameron NM, Shahrokh D, Del Corpo A, Dhir SK, Szyf M, Champagne FA, Meaney MJ (2008) Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J Neuroendocrinol 20:795–801

    Article  CAS  Google Scholar 

  • Champagne FA (2012) Epigenetics and developmental plasticity across species. Dev Psychobiol 55:33–41

    Article  Google Scholar 

  • Chan SY, Vasilopoulou E, Kilby MD (2009) The role of the placenta in thyroid hormone delivery to the fetus. Nat Clin Pract Endocrinol Metab 5:45–54

    Article  CAS  Google Scholar 

  • Chong S, Whitelaw E (2004) Epigenetic germline inheritance. Curr Opin Genet Dev 14(6):692–696

    Article  CAS  Google Scholar 

  • Clark J, Garbutt JS, McNally L, Little TJ (2017) Disease spread in age structured populations with maternal age effects. Ecol Lett 20:445–451

    Article  Google Scholar 

  • Colbourne JK, Herbert PDN, Taylor DJ (1997) Evolutionary origins of phenotypic diversity. In: Givnish TJ, Systma KJ (eds) Daphnia in molecular evolution and adaptive radiation. Cambridge University Press. p 163–188

  • Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH et al. (2011) The ecoresponsive genome of Daphnia pulex. Science 331(6017):555–561

    Article  CAS  Google Scholar 

  • Desmarais KH (1997) Keeping Daphnia out of the surface film with cetyl alcohol. J Plankton Res 19(1):149–154

    Article  Google Scholar 

  • Dorts J, Falisse E, Schoofs E, Flamion E, Kestermont P, Silvestre F (2016) DNA methyltransferases and stress-related genes expression in zebrafish larvae after exposure to heat and copper during reprogramming of DNA methylation. Sci Rep 6:34254

    Article  CAS  Google Scholar 

  • Ducker GS, Rabinowitz JD (2016) One-carbon metabolism in health and disease. Cell Metab 25:27–42. https://doi.org/10.1016/j.cmet.2016.08

  • Dudycha JL, Brandon CS, Deitz KC (2012) Population genomics of resource exploitation: insights from gene expression profiles of two Daphnia ecotypes fed alternate resources. Ecol Evol 2:329–340

  • Dzialowski EM, Reed WL, Sotherland PR (2009) Effects of egg size on double-crested cormorant (Phalacrocorax auritus) egg composition and hatchling phenotype. Comp Biochem Physiol A Mol Integr Physiol 152:262–267

    Article  Google Scholar 

  • Frost PC, Ebert D, Larson JH, Marcus MA, Wagner ND, Zalewski A (2010) Transgenerational effects of poor elemental food quality on Daphnia magna. Oecologia 162(4):865–872

    Article  Google Scholar 

  • Gabsi F, Glazier DS, Hammers-Wirtz M, Ratte HT, Preuss TG (2014) How to interactive maternal traits and environmental factors determine offspring size in Daphnia magna?. Ann Limnol 50:9–18

    Article  Google Scholar 

  • Garbutt JS, Little TJ (2016) Bigger is better: changes in body size explain a maternal effect of food on offspring disease resistance. Ecol Evolution 7:1403–1409

    Article  Google Scholar 

  • Gibney ER, Nolan CM (2010) Epigenetics and gene expression. Heredity 105:4–13

    Article  CAS  Google Scholar 

  • Gillis MK, Walsh MR (2019) Individual variation in plasticity dulls transgenerational responses to stress. Funct Ecol 33:1993–2002

  • Glazier DS (1992) Effects of food, genotype, and maternal size and age on offspring investment in Daphnia magna. Ecology 73(3):910–926

    Article  Google Scholar 

  • Gliwicz ZM, Guisande C (1992) Family planning in Daphnia: resistance to starvation in offspring born to mothers grown at different food levels. Oceologia 91:463–467

    Article  Google Scholar 

  • Goos JM, Swain CJ, Munch SB, Walsh MR (2018) Maternal diet and age alter direct and indirect relationships between lifer-history traits across multiple generations. Funct Ecol 33:491–502

    Article  Google Scholar 

  • Goulden CE, Horning LL (1980) Population oscillations and energy reserves in planktonic cladocera and their consequences to competition. Proc Natl Acad Sci USA 77:1716–1720

    Article  CAS  Google Scholar 

  • Groothuis TG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos Trans R Soc Lond B Biol Sci 363:1647–1661

    Article  CAS  Google Scholar 

  • Guisande C, Gliwicz ZM (1992) Egg size and clutch size in two Daphnia species at different food levels. J Plankton Res 14(7):997–1007

    Article  Google Scholar 

  • Hearn J, Chow FW-N, Barton H, Tung M, Wilson P, Blaxter M et al. (2018) Daphnia magna microRNAs respond to nutritional stress and ageing but are not transgenerational. Mol Ecol 27:1402–1412

    Article  CAS  Google Scholar 

  • Hearn J, Pearson M, Blaxter M, Wilson PJ, Little TJ (2019) Genome-wide methylation is modified by caloric restriction in Daphnia magna. BCM Genetics 20:197

  • Hearn J, Plenderleith F, Little TJ (2021) DNA methylation differs extensively between strains of the same geographical origin and changes with age in Daphnia magna. Epigenetics Chromatin 14:4. https://doi.org/10.1186/s13072-020-00379-z

  • Head JA (2014) Patterns of DNA methylation in animals: an ecotoxicological perspective. Integr Comp Biol 54:77–86

    Article  CAS  Google Scholar 

  • Hebert PDN (1981) Obligate asexuality in Daphnia. Am Nate 117:784–789

    Article  Google Scholar 

  • Herman JJ, Sultan SE (2016) DNA methylation mediates genetic variation for adaptive transgenerational plasticity. Proc Biol Sci 283(1838):20160988. https://doi.org/10.1098/rspb.2016.0988

    Article  CAS  Google Scholar 

  • Hiruta C, Nishida C, Tochinai S (2010) Abortive meiosis in the oogenesis of parthenogenetic Daphnia pulex. Chromosome Res 18:833–840

    Article  CAS  Google Scholar 

  • Ho DH, Burggren WW (2010) Epigenetics and transgenerational transfer: a physiological perspective. J Exp Biol 213:3–16

    Article  CAS  Google Scholar 

  • Ho DH (2008) Morphological and physiological developmental consequences of parental effects in the chicken embryo (Gallus gallus domesticus) and the zebrafish larva (Danio rerio). Diss: University of North Texas

  • Innes DJ, Fox CJ, Winsor GL (2000) Avoiding the cost of males in obligately asexual Daphnia pulex (Leydig). Proc: Biol Sci 267(1447):991–997

    CAS  Google Scholar 

  • Jeremias G, Barbosa J, Marques SM, De Schamphelaere KAC, Van Nieuwerburgh F, Deforce D, Gonçalves FJM, Pereira JL, Asselman J (2018) Transgenerational inheritance of dna hypomethylation in Daphnia magna in response to salinity stress. Environ Sci Technol 52(17):10114–10123

    Article  CAS  Google Scholar 

  • Jian X, Yang W, Zhao S, Liang H, Zhao Y, Chen L et al. (2013) Maternal effects of inducible tolerance against the toxic cyanobacterium Microcystis aeruginosa in the grazer Daphnia carinata. Environ Pollut 178:142–146

    Article  Google Scholar 

  • Keating KI (1985) The influence of vitamin-B12 deficiency on the reproduction of Daphnia-Pulex Leydig (Cladocera). J Crustacean Biol 5:30–136

    Article  Google Scholar 

  • Kleiven OT, Larsson P, Hobaek A (1992) Sexual reproduction in Daphnia magna requires three stimulie. Oikos 65:197–206

    Article  Google Scholar 

  • Kusari F, O’Doherty AM, Hodges NJ, Wojewodzic MW (2017) Bi-directional effects of vitamin B12 and methotrexate on Daphnia magna fitness and genomic methylation. Sci Rep 7:11872

    Article  Google Scholar 

  • Kvist J, Athanasio CG, Solari OS, Brown JB, Colbourne JK, Pfrender ME, Mirbahai L (2018) Pattern of DNA methylation in Daphnia: evolutionary perspective. Genome Biol Evolution 10(8):1988–2007

    Article  CAS  Google Scholar 

  • Lamka GF, Harder AM, Sundaram M, Schwartz TS, Christie MR, DeWoody JA, Willoughby JR (2022) Epigenetics in ecology, evolution, and conservation. Front Ecol Evol 10. https://doi.org/10.3389/fevo.2022.871791

  • LaMontagne JM, McCauley E (2001) Maternal effects in Daphnia: what mothers are telling their offspring and do they listen. Ecol Lett 4:64–71

    Article  Google Scholar 

  • Li Q, Jiang X (2014) Offspring tolerance to toxic Microcystis aeruginosa in Daphnia pulex shaped by maternal food availability and age. Fundam Appl Limnol 185:315–319

    Article  Google Scholar 

  • Mastorci F, Vicentini M, Viltart O, Manghi M, Graiani G, Quaini Fet al. (2009) Long-term effects of prenatal stress: changes in adult cardiovascular regulation and sensitivity to stress. Neurosci Biobehav Rev 33:191–203

    Article  Google Scholar 

  • Mkee D, Ebert D (1996) The interactive effects of temperature, food level and maternal phenotype on offspring size in Daphnia magna. Oecologia 107(2):189–196

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nguyen ND, Matsuura T, Kato Y, Watanabe H (2020) Caloric restriction upregulates the expression of DNMT3.1, lacking the conserved catalytic domain, in Daphnia magna. Genesis 58:12

    Article  Google Scholar 

  • Nguyen ND, Matsuura T, Kato Y, Watanabe H (2021) DNMT3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in Daphnia magna. Sci Rep 11:7326

    Article  CAS  Google Scholar 

  • Nusslein-Volhard C, Frohnhofer HG, Lehmann R (1987) Determination of anteroposterior polarity in Drosophila. Science 238:1675–1681

    Article  CAS  Google Scholar 

  • Pieters BJ, Liess M (2006) Maternal nutritional state determines the sensitivity of Daphnia magna offspring to short-term fenvalerate exposure. Aquat Toxicol 76:286–277

    Article  Google Scholar 

  • R Core Team (2021) R: a language and environmental for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Richards EJ (2006) Inherited epigenetic variation – revisiting soft inheritance. Nat Rev Genet 7:395–401

    Article  CAS  Google Scholar 

  • Stollewerk A (2010) The water flea Daphnia – a new model system for ecology and evolution? J Biol 9(2):21

    Article  Google Scholar 

  • Sturtevant AH (1923) Inheritance of direction of coiling in Limnea. Science 58:269

    Article  CAS  Google Scholar 

  • Suter MA, Chen A, Burdine MS, Choudhury M, Harris RA, Lane RH et al. (2012) A maternal high-fat diet modulates fetal SIRT1 histone and protein deacetylase activity in nonhuman primates. FASEB J 26:5106–5114

    Article  CAS  Google Scholar 

  • Tessier AJ, Consolatti NL (1989) Variation in offspring size in Daphnia and consequences for individual fitness. Oikos 56:269–276

    Article  Google Scholar 

  • Tessier AJ, Consolatti NL (1991) Resource quantity and offspring quality in Daphnia. Ecology 72(2):468–478

    Article  Google Scholar 

  • Trerotola M, Relli V, Simeone P, Alberti S (2015) Epigenetic inheritance and the missing heritability. Hum Genomics 9(1):17. https://doi.org/10.1186/s40246-015-0041-3

    Article  CAS  Google Scholar 

  • Trijau M, Asselman J, Armant O, Adam-Guillermin C, De Schamphelaere KAC, Alonzo F (2018) Transgenerational DNA methylation changes in Daphnia magna exposed to chronic γ irradiation. Environ Sci Technol 52(7):4331–4339

    Article  CAS  Google Scholar 

  • Urabe J, Sterner RW (2001) Contrasting effects of different types of resource depletion on life-history traits in Daphnia. Funct Ecol 15:165–174

    Article  Google Scholar 

  • Vandegehuchte MB, Kyndt T, Vanholme B, Haegeman A, Gheysen G, Janssen CR (2009a) Occurrence of DNA methylation in Daphnia magna and influence of multigeneration Cd exposure. Environ Int 35(4):700–706

    Article  CAS  Google Scholar 

  • Vandegehuchte MB, Lemiere F, Janssen CR (2009b) Quantitative DNA-methylation in Daphnia magna and effects of multigeneration Zn exposure. Comp Biochem Physiol C Toxicol Pharmacol 150:343–348

    Article  CAS  Google Scholar 

  • Vandegehuchte MB, Janssen CR (2011) Epigenetics and its implications for ecotoxicology. Ecotoxicology 20:607–624

    Article  CAS  Google Scholar 

  • Vandegehuchte MB, Janssen CR (2014) Epigenetics in an ecotoxicological context. Mutat Res Genet Toxicol Environ Mutagen 764–765:36–45

    Article  Google Scholar 

  • Walsh MR, La Pierre KJ, Post DM (2014) Phytoplankton composition modifies predator-driven life history evolution in Daphnia. Evol Ecol 28:397–411

    Article  Google Scholar 

  • Walsh MR, Cooley F, Biles K, Munch SB (2015) Predator-induced phenotypic plasticity within- and across generations: a challenge for theory? Proc R Soc B Biol Sci 282:20142205

    Article  Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag New York. ISBN 978-3-319-24277-4. https://ggplot2.tidyverse.org

  • Wolf JB, Wade MJ (2009) What are maternal effects (and what are they not)? Philos Trans R Soc Lond B Biol Sci 364(1520):1107–1115

    Article  Google Scholar 

  • Zaffagnini F (1987) Reproduction in Daphnia. Mem Ist Ital Idrobiol 45:245–284

    Google Scholar 

  • Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12(8):1045–1062

    Article  Google Scholar 

Download references

Acknowledgements

Matt Bruner, Heather Bruck, Rachel Schomaker, and Jake Swanson assisted with various tasks during the work. The Morg-5 and Tro-3 clones were kindly provided to us by Mike Lynch. Comments from our anonymous reviewers allowed us to greatly improve the manuscript. Funding for this work was provided by a grant from NSF award DEB-1556645 to JLD.

Author information

Author notes

  1. Julia Altman

    Present address: Department of Biology, Virginia Commonwealth University, Richmond, VA, 23284, USA

Authors and Affiliations

  1. Department of Biological Sciences, University of South Carolina, Columbia, SC, 29208, USA

    Trenton C. Agrelius, Julia Altman & Jeffry L. Dudycha

  2. Department of Biological Sciences, University of Notre Dame, Notre Dame, USA

    Trenton C. Agrelius

Authors
  1. Trenton C. Agrelius
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julia Altman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffry L. Dudycha
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TCA and JLD conceived the ideas and designed the experiments and led the writing of the manuscript. TCA and JA collected the data. TCA analyzed the data. All authors contributed critically to the drafts and gave final approval for publication.

Corresponding author

Correspondence to Trenton C. Agrelius.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Associate editor: Bastiaan Star.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Agrelius, T.C., Altman, J. & Dudycha, J.L. The maternal effects of dietary restriction on Dnmt expression and reproduction in two clones of Daphnia pulex. Heredity (2022). https://doi.org/10.1038/s41437-022-00581-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41437-022-00581-7

Search

Advanced search

Quick links