Epigenetics in ecology and evolution

Received: 2 June 2019 | Accepted: 21 November 2019 DOI: 10.1111/1365-2435.13494 EDITORIAL Epigenetics in ecology and evolution Anthony Herrel1 | Dominique Joly2 | Etienne Danchin3 1 Département Adaptations du Vivant, UMR 7179 CNRS/MNHN, Paris Cedex 5, France Abstract 2 1. The discovery of the multidimensional nature of the inherited information carried Laboratoire Evolution, Génomes, Comportement, Ecologie, UMR9191 CNRS/ IRD/Université Paris-Saclay, Gif-sur-Yvette, France 3 Laboratoire Évolution & Diversité Biologique (EDB), UMR5174, CNRS, Université Fédérale de Toulouse, IRD, Toulouse Cedex 9, France Correspondence Anthony Herrel Email: [email protected] Funding information CNRS; Laboratoires d'Excellences (LABEX) TULIP, Grant/Award Number: ANR-10LABX-41; Laboratoires d'Excellences (LABEX) BCDiv, Grant/Award Number: ANR10-LABX-03 Handling Editor: Charles Fox by the epigenome and the characterization of its intra- and intergenerational dynamics have profoundly changed our understanding of the functioning of biological organisms and the origins of phenotypic diversity. 2. This has raised considerable interest in the study of epigenetics which is emerging as a ‘missing link’ between environmental and phenotypic variation. 3. Recent discoveries have provided important insights into the mechanisms of phenotypic plasticity, inheritance and adaptation; key concepts at the crossroads of individual-centred approaches (that mostly study proximate mechanisms); and supra-individual ones (that mostly study ultimate processes). 4. In this context, epigenetics emerges as a major source of inquiry for the study of ecological and evolutionary dynamics. This special feature provides an overview of the role of epigenetics in ecology and evolution. KEYWORDS ecology, epigenetics, evolution Over the past two decades, the study of epigenetics has emerged as biological variation in all its complexity (Maher, 2008). This resulted an important discipline for the understanding of biological evolution in the debate about missing heritability and revealed the existence (for reviews, see, for instance: Bossdorf, Richards, & Pigliucci, 2008; of other forms of information transmission across generations Danchin et al., 2011; Danchin, Pocheville, Rey, Pujol, & Blanchet, (Danchin, 2013). 2020; Jablonka & Raz, 2009; Rando & Verstrepen, 2007; Richards, The discovery of epigenetics (any modification other than 2006; Skinner, Manikkam, & Guerrero-Bosagna, 2010; Wang, Liu, & changes in DNA sequences affecting gene expression, whether Sun, 2017). From the turn of the third millennium onwards, major those modifications have been shown to be stable or not) profoundly advances have been generated by exceptional technological ad- changed our understanding of the functioning of biological organ- vances in high-throughput sequencing that now allow the simul- isms and generated considerable interest in its role as a ‘missing link’ taneous analysis of genomes, epigenomes and transcriptomes in between environmental and phenotypic variation. In particular, re- all their complexity. These approaches, initially developed by mo- cent discoveries have fostered a full revision of the mechanisms of lecular biologists, are becoming accessible to researchers in other phenotypic plasticity (Bonduriansky & Day, 2018; Herman, Spencer, subdisciplines of biology working on both model and non-model Donohue, & Sultan, 2014; Jablonka, 2013; Pigliucci, Murren, & species. Consequently, these approaches have provided a new impe- Schlichting, 2006; Reed, Waples, Schindler, Hard, & Kinnison, 2010; tus to studies of the relationships between genes, environment and Sentis et al., 2018; Sultan, 2011; Zhang, Fischer, Colot, & Bossdorf, phenotypes in an eco-evolutionary context. A particularly surpris- 2012), inheritance (Bonduriansky, 2012; Bonduriansky & Day, 2018; ing outcome of the use of recent high-throughput molecular tech- Danchin, 2013; Day & Sweatt, 2011) and adaptation (Danchin et al., nologies was the discovery that the information encoded into the 2011, 2018, 2019; Pocheville & Danchin, 2015, 2017). These three DNA nucleotide sequence by itself is often insufficient to explain major lines of research in evolutionary biology are at the crossroads Functional Ecology. 2020;34:381–384. wileyonlinelibrary.com/journal/fec © 2020 British Ecological Society | 381 382 | Functional Ecology EDITORIAL between individual-centred approaches (that mostly study prox- Schweitzer, 2013; Galloway, 2005). Yet, little is known about how imate mechanisms) and supra-individual approaches (that mostly paternal transmission occurs. Champagne (2020) describes the cur- study ultimate processes) and are all impacted by our understand- rent state of knowledge regarding paternal epigenetic effects, the ing of epigenetics (Danchin & Pocheville, 2014; Jablonka & Lamb, interplay between maternal and paternal influences, and the im- 2005; Pocheville & Danchin, 2015). Epigenetics has emerged as a portance of considering the complex nature of reproduction when key discipline in the study of ecological and evolutionary dynamics, predicting the transmission of phenotypes across generations. The and this special feature contributes to highlighting the importance paper reviews experimental evidence on how sperm can drive the of this discipline. paternal transmission of epigenetic marks by a diversity of environ- As most disciplines in molecular biology, the study of epi- mental effects, such as nutritional or toxicological effects, and may genetics initially benefited considerably from the use of model shape offspring characteristics. The review also emphasizes how organisms. Today, however, the time is ripe to transfer discoveries the environmental exposure history of males may alter female mate from model organisms to non-model organisms, rendering these preference through sexual selection processes. It hence argues for a approaches more ecologically relevant. The transfer of knowledge better integration of behaviour in the transgenerational transmission to non-model organisms and more complex naturalistic settings of epigenetic variation. may then allow us to study the molecular basis of the complex in- Biological invasions are a global scourge and a major issue in teractions among organisms within communities and ecosystems. the current context of globalization and the world-wide and rapid As such, the study of epigenetic inheritance may provide novel transport of organisms outside of their native range. However, for insights into previously unexplained aspects of complex ecolog- an invader to be successful it needs to be able to rapidly respond ical interactions. With this special feature on the impact of epi- to and cope with different environmental conditions. Marin et al. genetics in the field of ecology, and particularly that of functional (2020) examine the possible link between stress, epigenetic ecology, we want to stimulate ecologists to embrace epigenetics changes and transposable element activity in generating pheno- as a major source of information allowing the study of the inter- typic and genetic variation in invasive populations. They argue actions among organisms and their biotic and abiotic environment that these mechanisms can contribute to the success of biolog- with the hope of fostering a better understanding of adaptation ical invasions by facilitating plasticity as well as rapid adaptive and evolution. evolution. Indeed, whereas epigenetic variation and transposable The potential role of epigenetics in answering important ecolog- elements are generally well regulated and thus not expressed ical and evolutionary questions is illustrated in this special feature. in natural populations, these mechanisms may be released from First, Pimpinelli and Piacentina (2020) discuss how transposons may their regulation in new and stressful environments. As such, contribute to translating phenotypic plasticity into genetic variabil- Marin and collaborators argue that the epigenome needs to be ity through their impact on epigenetic mechanisms. Especially in the studied in greater detail if we want to understand the mecha- context of rapid environmental change, it may be important to be nisms by which populations successfully colonize and adapt to able to translate phenotypic plasticity into variation that is encoded new environments. in the genome, and thus under direct natural selection. Pimpinelli Given the ability of epigenetic mechanisms to allow organisms to and Piacentina argue that modifications induced by transposons respond to rapid changes in their environment, they may also play an would not only impact epigenetic mechanisms but also be stably in- important role in conservation. Indeed, the paper by Rey et al. (2020) herited. Indeed, transposable elements are environment-responsive argues strongly that epigenetic variation and more particularly DNA molecular elements that can rapidly produce phenotypic and geno- methylation represent important components of biodiversity linking typic variants in response to environmental perturbations by caus- genomes to environments. They highlight the importance of DNA ing regulatory changes in the transcription of the genome. As such, methylation in providing biomarkers for past and present environ- transposons may play an important role on the relevant ecological mental stress, the ecological structuring of wild populations, improv- time-scales within which organisms need to respond to the current ing translocations and studying landscape connectivity. As such, and ongoing rapid changes in their environment. At the end of their epigenetic mechanisms appear to be a promising and important tool review, Pimpinelli and Piacentina discuss a few model systems where in conservation biology. transposons are likely to have played a role in the rapid phenotypic Together, these papers not only show the versatility of epigenetic diversification observed and suggest promising avenues for future mechanisms in generating phenotypic variability but more importantly research. show the importance of including epigenetic thinking when address- The characterization of parental transmission of epigenetic vari- ing questions in ecology and evolution. Especially in our current ever ation to offspring is of major importance to understanding how rapid more rapidly changing landscape, understanding how organisms may individual phenotypic changes are passed on through generations respond to change appears a crucial biological endeavour for which and stay heritable over generations. A number of studies have been epigenetic approaches may provide a major contribution. Different devoted to demonstrating how maternal processes shape the physi- aspects would need further theoretical and experimental investiga- cal and social context of offspring development through behavioural tion, including (a) the quantification of epigenetic reversion rate at the and physiological mechanisms (Adkins-Regan, Banerjee, Correa, & individual and transgenerational scales under different environmental Functional Ecology EDITORIAL scenarios; (b) the characterization of the epimutation pattern (random, directed – as for phenotypic plasticity, or dependent or not on environmental conditions), here again at the different biological levels; (c) the study of the genetic control of epimutations in relation to the possible genetic transmission across generations; and (d) the causal relationship between epigenetics, phenotypes and fitness in order to establish the adaptive value of epigenetics. Among these four points, the latter is probably the most crucial to demonstrate the extent of epigenetics in evolution as well as its impact on the heritability and the stability of the genomic compartment. We hope that this special feature will stimulate readers to think about the role of epigenetics in ecology and evolution and that it will spark new studies trying to understand variation in nature and its role in allowing populations to respond to variation in biotic and abiotic factors. AC K N OW L E D G E M E N T S The authors would like to thank the CNRS for funding the RTP and GDR 3E networks that have allowed to stimulate research on epigenetics and evolution in France. We would also like to thank all the members of the scientific committee of the RTP and GDR 3E networks for fruitful discussions. This work was supported by the Laboratoires d'Excellences (LABEX) TULIP (ANR-10-LABX-41) and Laboratoires d'Excellences (LABEX) BCDiv (ANR-10-LABX-03). ORCID Anthony Herrel https://orcid.org/0000-0003-0991-4434 Dominique Joly https://orcid.org/0000-0001-8000-4308 Etienne Danchin https://orcid.org/0000-0002-5013-9612 REFERENCES Adkins-Regan, E., Banerjee, S. B., Correa, S. M., & Schweitzer, C. (2013). Maternal effects in quail and zebra finches: Behavior and hormones. General and Comparative Endocrinology, 190, 34–41. https://doi. org/10.1016/j.ygcen.2013.03.002 Bonduriansky, R. (2012). Rethinking heredity, again. Trends in Ecology & Evolution, 27, 330–336. https://doi.org/10.1016/j.tree.2012.02.003 Bonduriansky, R., & Day, T. (2018). Extended heredity: A new understanding of inheritance and evolution. Princeton, NJ: Princeton University Press. Bossdorf, O., Richards, C. L., & Pigliucci, M. (2008). Epigenetics for ecologists. Ecology Letters, 11, 106–115. Champagne, A. (2020). Interplay between paternal germline and maternal effects in shaping development: The overlooked importance of behavioural ecology. Functional Ecology, 34(2), 401–413. https://doi. org/10.1111/1365-2435.13411 Danchin, É. (2013). Avatars of information: Towards an inclusive evolutionary synthesis. Trends in Ecology & Evolution, 28, 351–358. https:// doi.org/10.1016/j.tree.2013.02.010 Danchin, É., Charmantier, A., Champagne, F. A., Mesoudi, A., Pujol, B., & Blanchet, S. (2011). Beyond DNA: Integrating inclusive inheritance into an extended theory of evolution. Nature Reviews Genetics, 12, 475–486. https://doi.org/10.1038/nrg3028 Danchin, É., Nöbel, S., Pocheville, A., Dagaeff, A. C., Demay, L., Alphand, A., … Isabel, G. (2018). Cultural flies: Conformist social learning in fruit flies predicts long-lasting mate-choice traditions. Science, 362, 1025– 1030. https://doi.org/10.1126/science.aat1590 | 383 Danchin, É., & Pocheville, A. (2014). Inheritance is where physiology meets evolution. Journal of Physiology, 592, 2307–2317. https://doi. org/10.1113/jphysiol.2014.272096 Danchin, É., Pocheville, A., Rey, O., Pujol, B., & Blanchet, S. (2019). Epigenetically-facilitated mutational assimilation: Epigenetics as a hub within the inclusive evolutionary synthesis. Biological Reviews, 94, 259–282. https://doi.org/10.1111/brv.12453 Day, J. J., & Sweatt, D. (2011). Epigenetic mechanisms in cognition. Neuron, 70, 813–829. https://doi.org/10.1016/j.neuron.2011.05.019 Galloway, L. F. (2005). Maternal effects provide phenotypic adaptation to local environmental conditions. The New Phytologist, 166, 93–99. https://doi.org/10.1111/j.1469-8137.2004.01314.x Herman, J. J., Spencer, H. G., Donohue, K., & Sultan, S. E. (2014). How stable 'should' epigenetic modifications be? Insights from adaptive plasticity and bet hedging. Evolution, 68, 632–643. https://doi. org/10.1111/evo.12324 Jablonka, E. (2013). Epigenetic inheritance and plasticity: The responsive germline. Progress in Biophysics and Molecular Biology, 111, 99–107. https://doi.org/10.1016/j.pbiomolbio.2012.08.014 Jablonka, E., & Lamb, M. J. (2005). Evolution in four dimensions. Genetic, epigenetic, behavioural, and symbolic variation in the history of life. Cambridge, MA: MIT Press. Jablonka, E., & Raz, G. (2009). Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution. Quarterly Review of Biology, 84, 131–176. https://doi. org/10.1086/598822 Maher, B. (2008). Personal genomes: The case of the missing heritability. Nature, 456, 18–21. https://doi.org/10.1038/456018a Marin, P., Genitoni, J., Barloy, D., Maury, S., Gibert, P., Ghalambor, C. K., & Vieira, C. (2020). Biological invasion: The influence of the hidden side of the (epi) genome. Functional Ecology, 34(2), 385–400. https:// doi.org/10.1111/1365-2435.13317 Pigliucci, M., Murren, C. J., & Schlichting, C. D. (2006). Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology, 209, 2362–2367. https://doi.org/10.1242/jeb.02070 Pimpinelli, S., & Piacentini, L. (2020). Environmental changes and evolution of genomes: Transposons as translators of the phenotypic plasticity into genotypic variability. Functional Ecology, 34(2), 428–441. https://doi.org/10.1111/1365-2435.13497 Pocheville, A., & Danchin, É. (2015). Physiology and evolution at the crossroads of genetics and epigenetics. Journal of Physiology, 9, 2243–2243. Pocheville, A., & Danchin, É. (2017). Genetic assimilation and the paradox of blind variation. In P. Humeman & D. Walsh (Eds.), Challenging the modern synthesis. Adaptation, development, and inheritance (pp. 111–136). Oxford, UK: Oxford University Press. Rando, O. J., & Verstrepen, K. J. (2007). Timescales of genetic and epigenetic inheritance. Cell, 128, 655–668. https://doi.org/10.1016/j. cell.2007.01.023 Reed, T. E., Waples, R. S., Schindler, D. E., Hard, J. J., & Kinnison, M. T. (2010). Phenotypic plasticity and population viability: The importance of environmental predictability. Proceedings of the Royal Society B-Biological Sciences, 277, 3391–3400. https://doi.org/10.1098/ rspb.2010.0771 Rey, O., Eizaguirre, C., Angers, B., Baltazar-Soares, M., Sagonas, K., Prunier, J., & Blanchet, S. (2020). Linking epigenetics and biological conservation: Toward a conservation epigenetics perspective. Functional Ecology, 34(2), 414–427. https://doi.org/10.1111/1365-2435.13429 Richards, E. J. (2006). Inherited epigenetic variation – Revisiting soft inheritance. Nature Reviews Genetics, 7, 395–401. https://doi.org/ 10.1038/nrg1834 Sentis, A., Bertram, R., Dardenne, N., Ramon-Portugal, F., Espinasse, G., Louit, I., … Danchin, E. (2018). Evolution without standing genetic variation: Change in transgenerational plastic response under persistent predation pressure. Heredity, 121, 266–281. https://doi. org/10.1038/s41437-018-0108-8 384 | Functional Ecology Skinner, M. K., Manikkam, M., & Guerrero-Bosagna, C. (2010). Epigenetic transgenerational actions of environmental factors in disease etiology. Trends in Endocrinology & Metabolism, 21, 214–222. https://doi. org/10.1016/j.tem.2009.12.007 Sultan, S. E. (2011). Evolutionary implications of individual plasticity. In S. B. Gissis & E. Jablonka (Eds.), Transformations of Lamarckism: From subtle fluids to molecular biology. Cambridge, MA: MIT Press. Wang, Y., Liu, H., & Sun, Z. (2017). Lamarck rises from his grave: Parental environment-induced epigenetic inheritance in model organisms and humans. Biological Reviews, 92, 2084–2111. https://doi.org/10.1111/ brv.12322 EDITORIAL Zhang, Y.-Y., Fischer, M., Colot, V., & Bossdorf, O. (2012). Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytologist, 197, 314–322. https://doi.org/10.1111/nph.12010 How to cite this article: Herrel A, Joly D, Danchin E. Epigenetics in ecology and evolution. Funct Ecol. 2020;34:381–384. https://doi.org/10.1111/1365-2435.13494