Ecological Epigenetics

Epigenetics and Climate Change

The implications of epigenetics in species living in coastal regions, particularly in the context of adaptation and resilience to climate change, are profound and multifaceted. Coastal ecosystems are among the most dynamic and vulnerable environments, often facing challenges such as rising sea levels, increased storm frequency, and changing salinity. Epigenetics plays a crucial role in how these species adapt and survive under such rapidly changing conditions.

  1. Rapid Adaptation to Environmental Changes: Unlike genetic mutations, epigenetic modifications can occur relatively quickly in response to environmental changes. This rapid epigenetic response can allow species in coastal regions to adjust to shifts in temperature, salinity, or other stress factors associated with climate change, without waiting for long-term evolutionary changes through natural selection.

  2. Transgenerational Adaptation: Some epigenetic changes can be passed from one generation to the next. This means that if a population is exposed to a certain stressor (like increased salinity), the offspring may inherit some of the adaptations that help them survive in that environment, even if they are not exposed to the stressor themselves. This transgenerational epigenetic inheritance can be crucial for the survival of species in rapidly changing environments.

  3. Developmental Plasticity: Epigenetics contributes to developmental plasticity, where organisms can modify their development in response to environmental cues. This can result in changes in physical characteristics or behaviors that are better suited to the new environment, enhancing survival and reproduction.

  4. Resilience to Extreme Events: Coastal regions are often subject to extreme weather events like hurricanes or floods. Epigenetic mechanisms can contribute to the resilience of species by enabling rapid stress responses and recovery, ensuring survival and continuity.

  5. Community Dynamics and Ecosystem Functioning: The epigenetic responses of individual species can influence broader community dynamics and ecosystem functioning. For example, if a key species develops an epigenetic adaptation that alters its role in the ecosystem, it can have cascading effects on other species and overall ecosystem health.

  6. Potential for Conservation and Management Strategies: Understanding the epigenetic mechanisms underlying adaptation in coastal species can inform conservation efforts. It can lead to strategies that support the natural adaptive capacity of these species, thereby enhancing ecosystem resilience to climate change.

Coastal ecosystems are characterized by dynamic environmental variations and anthropogenic impacts, making the role of epigenetic mechanisms in adaptation and resilience paramount (Mounger et al., 2021). Epigenetic variation has been found to be high in coastal foundation species, indicating its importance in enabling species to cope with diverse and challenging coastal environments (Mounger et al., 2020). This is further supported by the fact that individuals with similar genetic profiles exhibit divergent epigenetic profiles, suggesting that epigenetic changes may be associated with environmental heterogeneity (Lira et al., 2010). Additionally, rapid phenotypic alterations mediated by epigenetic mechanisms are particularly important for the persistence of species in dynamic ecosystems, such as those in coastal regions (Mounger et al., 2021). Furthermore, the capacity of species to cope with disturbances and adapt while maintaining essential functions, as defined by coastal resilience, is influenced by epigenetic mechanisms (Raub et al., 2021). It has been suggested that genotypic diversity can replace the role of species diversity in species-poor coastal ecosystems, buffering against extreme climatic events (Reusch et al., 2005). This is significant in the context of climate change, as coastal areas are increasingly at risk from both natural and human-induced hazards (Almutairi et al., 2020). Moreover, the sensitivity of coastal species to ocean acidification highlights the need to understand the epigenetic effects of environmental stressors on coastal species (Pousse et al., 2022). In conclusion, epigenetics has profound implications for species living in coastal regions, particularly in the context of adaptation and resilience in the face of climate change. The high epigenetic variation observed in coastal species, coupled with the capacity of epigenetic mechanisms to enable rapid phenotypic alterations, underscores the importance of epigenetics in facilitating species’ ability to cope with diverse and challenging coastal environments.

Epigenética y Cambio Climático

Las implicaciones de la epigenética en las especies que viven en regiones costeras, particularmente en el contexto de la adaptación y resiliencia al cambio climático, son profundas y multifacéticas. Los ecosistemas costeros están entre los ambientes más dinámicos y vulnerables, enfrentando desafíos como el aumento del nivel del mar, la mayor frecuencia de tormentas y el cambio en la salinidad. La epigenética juega un papel crucial en cómo estas especies se adaptan y sobreviven bajo condiciones que cambian rápidamente.

Adaptación Rápida a Cambios Ambientales: A diferencia de las mutaciones genéticas, las modificaciones epigenéticas pueden ocurrir relativamente rápido en respuesta a cambios ambientales. Esta rápida respuesta epigenética puede permitir que las especies en regiones costeras se ajusten a cambios en la temperatura, la salinidad u otros factores de estrés asociados con el cambio climático, sin esperar cambios evolutivos a largo plazo a través de la selección natural.

Adaptación Transgeneracional: Algunos cambios epigenéticos pueden transmitirse de una generación a otra. Esto significa que si una población está expuesta a un cierto factor de estrés (como el aumento de la salinidad), la descendencia puede heredar algunas de las adaptaciones que les ayudan a sobrevivir en ese ambiente, incluso si no están expuestos al factor de estrés ellos mismos. Esta herencia epigenética transgeneracional puede ser crucial para la supervivencia de especies en ambientes que cambian rápidamente.

Plasticidad del Desarrollo: La epigenética contribuye a la plasticidad del desarrollo, donde los organismos pueden modificar su desarrollo en respuesta a señales ambientales. Esto puede resultar en cambios en características físicas o comportamientos que son más adecuados para el nuevo ambiente, mejorando la supervivencia y reproducción.

Resiliencia a Eventos Extremos: Las regiones costeras a menudo están sujetas a eventos climáticos extremos como huracanes o inundaciones. Los mecanismos epigenéticos pueden contribuir a la resiliencia de las especies al permitir respuestas rápidas al estrés y recuperación, asegurando la supervivencia y continuidad.

Dinámicas de la Comunidad y Funcionamiento del Ecosistema: Las respuestas epigenéticas de especies individuales pueden influir en las dinámicas de la comunidad y el funcionamiento del ecosistema. Por ejemplo, si una especie clave desarrolla una adaptación epigenética que altera su rol en el ecosistema, puede tener efectos en cascada en otras especies y en la salud general del ecosistema.

Potencial para Estrategias de Conservación y Gestión: Comprender los mecanismos epigenéticos subyacentes en la adaptación de especies costeras puede informar los esfuerzos de conservación. Puede conducir a estrategias que apoyen la capacidad adaptativa natural de estas especies, mejorando así la resiliencia del ecosistema al cambio climático.

Los ecosistemas costeros se caracterizan por variaciones ambientales dinámicas e impactos antropogénicos, lo que hace que el papel de los mecanismos epigenéticos en la adaptación y resiliencia sea primordial (Mounger et al., 2021). Se ha encontrado que la variación epigenética es alta en especies fundadoras costeras, indicando su importancia en permitir a las especies hacer frente a ambientes costeros diversos y desafiantes (Mounger et al., 2020). Esto se apoya aún más en el hecho de que individuos con perfiles genéticos similares exhiben perfiles epigenéticos divergentes, lo que sugiere que los cambios epigenéticos pueden estar asociados con la heterogeneidad ambiental (Lira et al., 2010). Además, las alteraciones fenotípicas rápidas mediadas por mecanismos epigenéticos son particularmente importantes para la persistencia de especies en ecosistemas dinámicos, como los de las regiones costeras (Mounger et al., 2021). Además, la capacidad de las especies para hacer frente a perturbaciones y adaptarse mientras mantienen funciones esenciales, como se define por la resiliencia costera, está influenciada por mecanismos epigenéticos (Raub et al., 2021). Se ha sugerido que la diversidad genotípica puede reemplazar el papel de la diversidad de especies en ecosistemas costeros con poca diversidad de especies, amortiguando contra eventos climáticos extremos (Reusch et al., 2005). Esto es significativo en el contexto del cambio climático, ya que las áreas costeras están cada vez más en riesgo tanto por peligros naturales como inducidos por el hombre (Almutairi et al., 2020). Además, la sensibilidad de las especies costeras a la acidificación del océano resalta la necesidad de entender los efectos epigenéticos de los factores de estrés ambientales en las especies costeras (Pousse et al., 2022). En conclusión, la epigenética tiene implicaciones profundas para las especies que viven en regiones costeras, particularmente en el contexto de la adaptación y resiliencia frente al cambio climático. La alta variación epigenética observada en especies costeras, junto con la capacidad de los mecanismos epigenéticos para permitir alteraciones fenotípicas rápidas, subraya la importancia de la epigenética en facilitar la capacidad de las especies para hacer frente a ambientes costeros diversos y desafiantes.

References:

Almutairi, A., Mourshed, M., & Ameen, R. (2020). Coastal community resilience frameworks for disaster risk management. Natural Hazards, 101(2), 595-630. https://doi.org/10.1007/s11069-020-03875-3

Lira, C., Parisod, C., Fernandes, R., Mata, C., Cardoso, M., & Ferreira, P. (2010). Epigenetic variation in mangrove plants occurring in contrasting natural environment. Plos One, 5(4), e10326. https://doi.org/10.1371/journal.pone.0010326

Mounger, J., Boquete, M., Schmid, M., Granado, R., Robertson, M., Voors, S., … & Richards, C. (2020). Inheritance of DNA methylation differences in the mangrove Rhizophora mangle. https://doi.org/10.1101/2020.10.24.353482

Mounger, J., Boquete, M., Schmid, M., Granado, R., Robertson, M., Voors, S., … & Richards, C. (2021). Inheritance of DNA methylation differences in the mangrove Rhizophora mangle. Evolution & Development, 23(4), 351-374. https://doi.org/10.1111/ede.12388

Pousse, E., Munroe, D., Hart, D., Hennen, D., Cameron, L., Rheuban, J., … & Meseck, S. (2022). Dynamic energy budget modeling of Atlantic surfclam, Spisula solidissima, under future ocean acidification and warming. Marine Environmental Research, 177, 105602. https://doi.org/10.1016/j.marenvres.2022.105602

Raub, K., Stepenuck, K., Panikkar, B., & Stephens, J. (2021). An analysis of resilience planning at the nexus of food, energy, water, and transportation in coastal US cities. Sustainability, 13(11), 6316. https://doi.org/10.3390/su13116316

Reusch, T., Ehlers, A., Hämmerli, A., & Worm, B. (2005). Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences, 102(8), 2826-2831. https://doi.org/10.1073/pnas.0500008102

Epigenetics in Ecological and Evolutionary Processes

Epigenetics plays a crucial role in the ecological and evolutionary processes of various organisms, particularly plants and animals. The interaction between epigenetics and the environment has been a subject of increasing interest (Feil & Fraga, 2012). Studies have shown that epigenetic mechanisms, such as DNA methylation and chromatin modifications, mediate responses to environmental cues and play a significant role in the adaptation of species to changing environmental conditions (Consuegra & López, 2016).

Furthermore, epigenetic diversity has been found to enhance the productivity and stability of plant populations, indicating its ecological implications (Latzel et al., 2013). Additionally, evidence from pyrosequencing suggests that natural variation in animal personality is associated with DNA methylation, highlighting the relevance of epigenetics in understanding behavioral consistency and its ecological and evolutionary implications (Verhulst et al., 2016).

The significance of epigenetics for plant ecology has been emphasized, with a call for increased transfer of knowledge and methods from model species research to genomes of evolutionarily divergent species, as well as the examination of responses to complex natural environments at a more mechanistic level (Richards et al., 2017). Furthermore, the opportunities and limitations of reduced representation bisulfite sequencing in plant ecological epigenomics have been explored, aiming to understand the unique contributions of epigenetic mechanisms to ecological and evolutionary processes (Paun et al., 2018).

Marine environmental epigenetics has also been studied, providing insights applicable to critical issues such as aquaculture, biomonitoring, and biological invasions, thereby improving the understanding and prediction of marine taxa responses to global climate change (Eirín‐López & Putnam, 2019).

In conclusion, epigenetics has emerged as a crucial factor in ecological and evolutionary processes, influencing the adaptation, productivity, and stability of plant populations, as well as the behavioral consistency of animals. The interaction between epigenetics and the environment has significant implications for understanding and predicting the responses of various organisms to environmental changes.

Epigenética en Procesos Ecológicos y Evolutivos

La epigenética juega un papel crucial en los procesos ecológicos y evolutivos de diversos organismos, particularmente plantas y animales. La interacción entre la epigenética y el ambiente ha sido un tema de creciente interés (Feil & Fraga, 2012). Estudios han mostrado que mecanismos epigenéticos, como la metilación del ADN y las modificaciones de la cromatina, median respuestas a señales ambientales y juegan un papel significativo en la adaptación de especies a condiciones ambientales cambiantes (Consuegra & López, 2016).

Además, se ha encontrado que la diversidad epigenética aumenta la productividad y estabilidad de poblaciones de plantas, indicando sus implicaciones ecológicas (Latzel et al., 2013). Igualmente, evidencia proveniente de pirosecuenciación sugiere que la variación natural en la personalidad animal está asociada con la metilación del ADN, resaltando la relevancia de la epigenética en la comprensión de la consistencia del comportamiento y sus implicaciones ecológicas y evolutivas (Verhulst et al., 2016).

La importancia de la epigenética para la ecología de las plantas ha sido enfatizada, con un llamado a un mayor traslado de conocimiento y métodos desde la investigación de especies modelo a genomas de especies evolutivamente divergentes, así como la examinación de respuestas a ambientes naturales complejos a un nivel más mecanicista (Richards et al., 2017). Además, se han explorado las oportunidades y limitaciones de la secuenciación bisulfito de representación reducida en epigenómica ecológica de plantas, con el objetivo de entender las contribuciones únicas de mecanismos epigenéticos a procesos ecológicos y evolutivos (Paun et al., 2018).

La epigenética ambiental marina también ha sido estudiada, proporcionando percepciones aplicables a temas críticos como la acuicultura, el biomonitoring y las invasiones biológicas, mejorando así la comprensión y predicción de respuestas de taxones marinos al cambio climático global (Eirín‐López & Putnam, 2019).

En conclusión, la epigenética ha emergido como un factor crucial en procesos ecológicos y evolutivos, influyendo en la adaptación, productividad y estabilidad de poblaciones de plantas, así como en la consistencia del comportamiento de los animales. La interacción entre la epigenética y el ambiente tiene implicaciones significativas para la comprensión y predicción de las respuestas de diversos organismos a cambios ambientales.

References:

  • Consuegra, S. and López, C. (2016). Epigenetic‐induced alterations in sex‐ratios in response to climate change: an epigenetic trap?. Bioessays, 38(10), 950-958. https://doi.org/10.1002/bies.201600058
  • Eirín‐López, J. and Putnam, H. (2019). Marine environmental epigenetics. Annual Review of Marine Science, 11(1), 335-368. https://doi.org/10.1146/annurev-marine-010318-095114
  • Feil, R. and Fraga, M. (2012). Epigenetics and the environment: emerging patterns and implications. Nature Reviews Genetics, 13(2), 97-109. https://doi.org/10.1038/nrg3142
  • Latzel, V., Allan, E., Silveira, A., Colot, V., Fischer, M., & Bossdorf, O. (2013). Epigenetic diversity increases the productivity and stability of plant populations. Nature Communications, 4(1). https://doi.org/10.1038/ncomms3875
  • Paun, O., Verhoeven, K., & Richards, C. (2018). Opportunities and limitations of reduced representation bisulfite sequencing in plant ecological epigenomics. New Phytologist, 221(2), 738-742. https://doi.org/10.1111/nph.15388
  • Richards, C., Alonso, C., Becker, C., Bossdorf, O., Bucher, E., Colomé-Tatché, M., … & Verhoeven, K. (2017). Ecological plant epigenetics: evidence from model and non‐model species, and the way forward. Ecology Letters, 20(12), 1576-1590. https://doi.org/10.1111/ele.12858
  • Verhulst, E., Mateman, A., Zwier, M., Samuel, P., Verhoeven, K., & Oers, K. (2016). Evidence from pyrosequencing indicates that natural variation in animal personality is associated with drd4 dna methylation. Molecular Ecology, 25(8), 1801-1811. https://doi.org/10.1111/mec.13519

Invasive Species

Epigenetics plays a significant role in the expansion of invasive species, contributing to their adaptability and success in new environments. The rapid adaptation of invasive species, particularly in response to selection pressures generated by novel environments, involves epigenetic modulation as an adaptive strategy (Carneiro & Lyko, 2020). Epigenetic mechanisms, such as DNA methylation, have been suggested to compensate for losses in genetic variability and contribute to adaptive phenotypic plasticity in invasive species (Bock et al., 2015). Furthermore, epigenetic diversity has been proposed to facilitate the expansion of invasive species by acting as an alternative source of variation in areas with low genetic diversity (Sheldon et al., 2018). This plasticity acquired through epigenetic changes explains the ability of invasive species to expand and colonize new ecosystems, particularly in the presence of reduced genetic diversity due to founder effects (Ardura et al., 2017). Studies have also indicated that epigenetic mechanisms impact several phenotypic traits and may be important for the ecology and evolution of invasive species (Schrey et al., 2012). Additionally, epigenetic variation has been suggested to compensate for decreased genetic variation during introductions, highlighting its potential role in facilitating the success of invasive species in new environments (Schrey et al., 2012). The expansion of invasive species challenges our understanding of the process of adaptation, and epigenetic mechanisms are increasingly recognized as integral to the adaptation of species facing environmental changes (Chisholm et al., 2016). In conclusion, epigenetic mechanisms play a crucial role in the expansion of invasive species by facilitating rapid adaptation, compensating for genetic variability, and contributing to phenotypic plasticity. The plasticity acquired through epigenetic changes enables invasive species to thrive in new environments and colonize new ecosystems, ultimately contributing to their success as invasive species.

Especies Invasoras

La epigenética juega un papel significativo en la expansión de especies invasoras, contribuyendo a su adaptabilidad y éxito en nuevos entornos. La rápida adaptación de las especies invasoras, particularmente en respuesta a las presiones de selección generadas por entornos novedosos, implica la modulación epigenética como una estrategia adaptativa (Carneiro & Lyko, 2020). Mecanismos epigenéticos, como la metilación del ADN, se han sugerido para compensar las pérdidas en variabilidad genética y contribuir a la plasticidad fenotípica adaptativa en especies invasoras (Bock et al., 2015). Además, se ha propuesto que la diversidad epigenética facilita la expansión de las especies invasoras al actuar como una fuente alternativa de variación en áreas con baja diversidad genética (Sheldon et al., 2018). Esta plasticidad adquirida a través de cambios epigenéticos explica la capacidad de las especies invasoras para expandirse y colonizar nuevos ecosistemas, particularmente en presencia de una diversidad genética reducida debido a efectos fundadores (Ardura et al., 2017). Estudios también han indicado que los mecanismos epigenéticos impactan varios rasgos fenotípicos y pueden ser importantes para la ecología y evolución de las especies invasoras (Schrey et al., 2012). Adicionalmente, se ha sugerido que la variación epigenética puede compensar la disminución de la variación genética durante las introducciones, resaltando su potencial rol en facilitar el éxito de las especies invasoras en nuevos entornos (Schrey et al., 2012). La expansión de las especies invasoras desafía nuestra comprensión del proceso de adaptación, y los mecanismos epigenéticos son cada vez más reconocidos como integrales para la adaptación de especies frente a cambios ambientales (Chisholm et al., 2016). En conclusión, los mecanismos epigenéticos juegan un papel crucial en la expansión de las especies invasoras facilitando la rápida adaptación, compensando la variabilidad genética y contribuyendo a la plasticidad fenotípica. La plasticidad adquirida a través de cambios epigenéticos permite a las especies invasoras prosperar en nuevos entornos y colonizar nuevos ecosistemas, contribuyendo en última instancia a su éxito como especies invasoras.

References:

  • Ardura, A., Zaiko, A., Morán, P., Planes, S., & García‐Vázquez, E. (2017). Epigenetic signatures of invasive status in populations of marine invertebrates. Scientific Reports, 7(1). https://doi.org/10.1038/srep42193
  • Bock, D., Caseys, C., Cousens, R., Hahn, M., Heredia, S., Hübner, S., … & Rieseberg, L. (2015). What we still don’t know about invasion genetics. Molecular Ecology, 24(9), 2277-2297. https://doi.org/10.1111/mec.13032
  • Carneiro, V. and Lyko, F. (2020). Rapid epigenetic adaptation in animals and its role in invasiveness. Integrative and Comparative Biology, 60(2), 267-274. https://doi.org/10.1093/icb/icaa023
  • Chisholm, R., Lorenzi, T., Desvillettes, L., & Hughes, B. (2016). Evolutionary dynamics of phenotype-structured populations: from individual-level mechanisms to population-level consequences. Zeitschrift Für Angewandte Mathematik Und Physik, 67(4). https://doi.org/10.1007/s00033-016-0690-7
  • Consuegra, S. and López, C. (2016). Epigenetic‐induced alterations in sex‐ratios in response to climate change: an epigenetic trap?. Bioessays, 38(10), 950-958. https://doi.org/10.1002/bies.201600058
  • Eirín‐López, J. and Putnam, H. (2019). Marine environmental epigenetics. Annual Review of Marine Science, 11(1), 335-368. https://doi.org/10.1146/annurev-marine-010318-095114
  • Feil, R. and Fraga, M. (2012). Epigenetics and the environment: emerging patterns and implications. Nature Reviews Genetics, 13(2), 97-109. https://doi.org/10.1038/nrg3142
  • Latzel, V., Allan, E., Silveira, A., Colot, V., Fischer, M., & Bossdorf, O. (2013). Epigenetic diversity increases the productivity and stability of plant populations. Nature Communications, 4(1). https://doi.org/10.1038/ncomms3875
  • Paun, O., Verhoeven, K., & Richards, C. (2018). Opportunities and limitations of reduced representation bisulfite sequencing in plant ecological epigenomics. New Phytologist, 221(2), 738-742. https://doi.org/10.1111/nph.15388
  • Richards, C., Alonso, C., Becker, C., Bossdorf, O., Bucher, E., Colomé-Tatché, M., … & Verhoeven, K. (2017). Ecological plant epigenetics: evidence from model and non‐model species, and the way forward. Ecology Letters, 20(12), 1576-1590. https://doi.org/10.1111/ele.12858
  • Schrey, A., Coon, C., Grispo, M., Awad, M., Imboma, T., McCoy, E., … & Martin, L. (2012). Epigenetic variation may compensate for decreased genetic variation with introductions: a case study using house sparrows (passer domesticus) on two continents. Genetics Research International, 2012, 1-7. https://doi.org/10.1155/2012/979751
  • Sheldon, E., Schrey, A., Andrew, S., Ragsdale, A., & Griffith, S. (2018). Epigenetic and genetic variation among three separate introductions of the house sparrow (passer domesticus) into Australia. Royal Society Open Science, 5(4), 172185. https://doi.org/10.1098/rsos.172185
  • Verhulst, E., Mateman, A., Zwier, M., Samuel, P., Verhoeven, K., & Oers, K. (2016). Evidence from pyrosequencing indicates that natural variation in animal personality is associated with drd4 DNA methylation. Molecular Ecology, 25(8), 1801-1811. https://doi.org/10.1111/mec.13519

More on Adaptation and Evolution

Lamka, G. F., Harder, A. M., Sundaram, M., Schwartz, T. S., Christie, M. R., DeWoody, J. A., … & Willoughby, J. R. (2022). Epigenetics in ecology, evolution, and conservation. Frontiers in Ecology and Evolution, 10. https://doi.org/10.3389/fevo.2022.871791

Abstract: Epigenetic variation is often characterized by modifications to DNA that do not alter the underlying nucleotide sequence, but can influence behavior, morphology, and physiological phenotypes by affecting gene expression and protein synthesis. In this review, we consider how the emerging field of ecological epigenetics (eco-epi) aims to use epigenetic variation to explain ecologically relevant phenotypic variation and predict evolutionary trajectories that are important in conservation. Here, we focus on how epigenetic data have contributed to our understanding of wild populations, including plants, animals, and fungi. First, we identified published eco-epi literature and found that there was limited taxonomic and ecosystem coverage and that, by necessity of available technology, these studies have most often focused on the summarized epigenome rather than locus- or nucleotide-level epigenome characteristics. We also found that while many studies focused on adaptation and heritability of the epigenome, the field has thematically expanded into topics such as disease ecology and epigenome-based ageing of individuals. In the second part of our synthesis, we discuss key insights that have emerged from the epigenetic field broadly and use these to preview the path toward integration of epigenetics into ecology. Specifically, we suggest moving focus to nucleotide-level differences in the epigenome rather than whole-epigenome data and that we incorporate several facets of epigenome characterization (e.g., methylation, chromatin structure). Finally, we also suggest that incorporation of behavior and stress data will be critical to the process of fully integrating eco-epi data into ecology, conservation, and evolutionary biology.

Venney, C. J., Anastasiadi, D., Wellenreuther, M., & Bernatchez, L. (2023). The evolutionary complexities of dna methylation in animals: from plasticity to genetic evolution. Genome Biology and Evolution, 15(12). https://doi.org/10.1093/gbe/evad216

The importance of DNA methylation in plastic responses to environmental change and evolutionary dynamics is increasingly recognized. Here, we provide a Perspective piece on the diverse roles of DNA methylation on broad evolutionary timescales, including (i) short-term transient acclimation, (ii) stable phenotypic evolution, and (iii) genomic evolution. We show that epigenetic responses vary along a continuum, ranging from short-term acclimatory responses in variable environments within a generation to long-term modifications in populations and species. DNA methylation thus unlocks additional potential for organisms to rapidly acclimate to their environment over short timeframes. If these changes affect fitness, they can circumvent the need for adaptive changes at the genome level. However, methylation has a complex reciprocal relationship with genetic variation as it can be genetically controlled, yet it can also induce point mutations and contribute to genomic evolution. When habitats remain constant over many generations, or populations are separated across habitats, initially plastic phenotypes can become hardwired through epigenetically facilitated mutagenesis. It remains unclear under what circumstances plasticity contributes to evolutionary outcomes, and when plastic changes will become permanently encoded into genotype. We highlight how studies investigating the evolution of epigenetic plasticity need to carefully consider how plasticity in methylation state could evolve among different evolutionary scenarios, the possible phenotypic outcomes, its effects on genomic evolution, and the proximate energetic and ultimate fitness costs of methylation. We argue that accumulating evidence suggests that DNA methylation can contribute toward evolution on various timescales, spanning a continuum from acclimatory plasticity to genomic evolution.