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DISPERSIVE GENOMES: Epigenetic potential as mediator of phenotypic plasticity and natal dispersal

Periodic Reporting for period 1 - GENESPERSIVE (DISPERSIVE GENOMES: Epigenetic potential as mediator of phenotypic plasticity and natal dispersal)

Reporting period: 2022-09-01 to 2024-08-31

Climate change is shaping animal movements at a global scale, affecting species distribution, phenology, and invasion status. Dispersal is the movement from the native habitat to another - either temporarily or for reproduction - and a highly relevant life history trait that will determine fitness prospects, population dynamics and species distributions. Although not all individuals are equally likely to disperse, the causes of the variation in dispersal propensity remain poorly understood. Epigenetic mechanisms – changes in gene expression that do not involve changes in the DNA sequence – enable rapid and plastic responses to environmental changes, and individual genomes may differ in their capacity to respond epigenetically – i.e. epigenetic potential. A high capacity for epigenetically-induced variation in these responses may be a requirement for species to successfully settle in novel environments, and this project predicts that individuals with higher dispersal propensity will show greater epigenetic potential. Using a 40-year dataset from a wild bird population and combining analysis of historical samples, field experiments and cutting-edge epigenetic techniques, GENESPERSIVE addresses this question at broad spatial and temporal scales, including long-term individual data and samples from multiple Eurasian populations to track past colonization and current expansion events. Among other project outcomes, we have developed a bioinformatics pipeline to quantify epigenetic potential from raw genetic sequences, which is publicly available. Our results suggest that, within a population, individuals showing higher dispersal also show higher epigenetic potential. Furtehrmore, we also found higher epigenetic potential in individuals living in that population during the colonization phase, when compared to those from later generations. GENESPERSIVE provides mechanistic insights of dispersal behavior, a key step towards predicting species responses in the face of anthropic changes.
A bioinformatics pipeline to quantify epigenetic potential has been developed by B. Jimeno and M. Ravinet, adapted to the study species (the pied flycatcher) and used to analyse the data included in GENESPERSIVE. The codes associated to this pipeline are available at: https://github.com/markravinet/epigenetic_potential(opens in new window).

The manuscript resulting from the work contemplated in RO1 is currently under review (and available as preprint). Importantly, this publication shows highly relevant and certainly promising results in light of the GENESPERSIVE predictions and objectives, as we found i) higher epigenetic potential in more dispersive individuals within a pied flycatcher (Ficedula hypoleuca) population, ii) higher epigenetic potential in the first generations after patch colonization when compared to individuals living in that same patch decades after colonization, and iii) population-specific differences in epigenetic potential occurring more often in gene regulatory and coding regions, when compared with introns and intergenic regions.

Secondments have been key to develop the bioinformatics pipeline for the within-population (ROI) and among-population (ROIII) results, and the establishment of a fruitful collaboration with the host (Dr. Ravinet). Research line has been very well received and nicely integrated into his lab (currently at the University of Oslo), where B. Jimeno and M. Ravinet currently co-supervise 2 master projects on epigenetic potential.

Regarding dissemination and communication, the researcher attended several courses, including one in Ecological Epigenetics, Risk Assessment in Mountainous areas (by CSIC), and Gender Bias in Research (CSIC). She also received specific training in bioinformatics and genomics during the two secondments performed at Dr. Ravinet´s lab. Furthermore, B. Jimeno attended 3 conferences (2 international, 1 national), in all of them as leading and presenting author, giving an oral presentation. She has also led a special issue proposal on ecological epigenetics (co-edited with Dr. Mark Ravinet, Dr. Jesús Martínez-Padilla and Dr. Kees Van Oers). This proposal has been successfully accepted in the top-ranked journal Philosophical Transactions of the Royal Society B, and is currently in progress (publication expected by the end of 2025-beginning of 2026).Within the communication to non-academic audiences, the researcher has participated in several outreach events, including the International Day for Women and Girl in Science (11 February) and the Pint of Science, both in 2024, targeting high school and broad audiences, respectively. Besides, the researcher has created a project website, where research questions, linked publications and updates will be regularly posted.
GENESPERSIVE provides new insights on the role of epigenetic mechanisms in local adaptation of wild populations under current environmental change. By studying epigenetic potential – a genetic trait that may determine epigenetically-mediated phenotypic plasticity – these results shed new light on the link between epigenetic and genetic inheritance, which is currently one of the most pressing questions in the fields of evolutionary ecology and ecological epigenetics. Furthermore, GENESPERSIVE investigates whether epigenetic potential may be a “pleiotropic source” of phenotypic plasticity at an organismal level, and thus become a proxy for the capacity of individuals to overcome habitat change, with all the impact that entails in the fields of population management and conservation.

Importantly, many outcomes derived from this project are still to come, and several project ideas and collaborations have started as a consequence of additional researchers and labs getting interested in integrating or applying this research line.

The scientific impact, interest and novelty of this new research line is illustrated by the many research works and collaborations derived from the action. The researcher (B. Jimeno) is currently part of several collaborative networks which have started and/or been strengthened during the course of GENESPERSIVE. These include further work and manuscripts ongoing with the host group at IPE-CSIC, participation in the collaborative network led by Dr. Marty Martin, involvement in a collaborative project led by Dr. David Wheatcroft, and the integration into Dr. Ravinet´s lab including MsC supervision.
Predicted association between epigenetic potential and dispersal propensity in the study species
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