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New insights into the genetic mechanisms underlying behavioural variation in wild marine fish

Periodic Reporting for period 1 - WildFishGenes (New insights into the genetic mechanisms underlying behavioural variation in wild marine fish)

Período documentado: 2020-04-16 hasta 2022-04-15

Humans depend significantly on the welfare of marine ecosystems, deriving benefits not only from resource harvesting but also from the benefits derived from healthy ecosystems (i.e. natural resources’ quality, biodiversity maintenance, and ecosystem resilience to anthropogenic challenges). Traditionally, marine resource management has focused primarily on morphological traits (e.g. body size) of individuals. However, mounting evidence highlights the critical role of behaviour in biodiversity conservation. Fish behaviour, like other phenotypic traits, is largely determined by genetic factors. Therefore, investigating the genetic mechanisms underlying fish behavioural types is pivotal for fisheries management and biodiversity conservation.
This project uses behavioural data obtained by high-throughput acoustic telemetry to simultaneously measure activity and movement in hundreds of wild individuals. Additionally, behavioural quantification was complemented with studies of the same individuals in captivity, assessing exploration, boldness, activity and aggressiveness. These behavioural traits are linked to fishing vulnerability, as individuals exhibiting specific traits are more susceptible at being captured than others, potentially leading to fisheries-induced selection.
In parallel to the behavioural data, the genomic data from the study individuals was characterized through genotyping by sequencing to identify genetic variants associated with specific behavioural types, and complemented by brain transcriptomics to understand gene expression related to fish behaviour. Moreover, the genomic dataset was expanded by means of the assembly and annotation of the species’ genome and the genotyping of individuals from other populations exposed to varying fishing pressures to broaden the scope of the study and open a follow-up research line.
The multidisciplinary nature of the project, combining novel behavioural data collection with next-generation genomic techniques, offered a comprehensive molecular perspective on behavioural characterization. Notably, an association between the number of amino acid copies in a master gene of the clock system and activity timing in marine fish has been described. Additionally, expression levels on several genes were associated with the activity rhythm in this species. Differential activity preferences among individuals can result in varying exposure to human harvesting, potentially leading to the artificial selection of specific gene variants or regulatory pathways influencing individual activity patterns. Furthermore, the reference genome for the study species has been generated, allowing for a population-level analysis from samples subject to varying fishing pressures. The activities conducted under the scope of this project have opened a new line of research in behavioural molecular ecology unprecedented in marine ecosystems.
Throughout this project, a comprehensive behavioural quantification of the study species has been developed, culminating in four published works detailing the behavioural findings. The research, identified distinct behavioural types exhibited consistently in both laboratory and wild settings. Part of this behavioural analysis included the characterization of chronotypes, individual activity rhythms preferences directly linked to vulnerability at being captured by fishers.
At the genomic level, genetic sequence variants associated with individual chronotypes were detected, suggesting a potential genetic basis for fisheries-induced selection. Additionally, several brain-expressed genes were identified with rhythmic expression patterns, further elucidating the genetic underpinnings of behavioural traits. The project’s impact was enhanced by the development of a de novo genome for the study species, which significantly enhanced the interpretation and reach of the findings. The research project has been actively communicated within the scientific community through the participation to nine scientific events, and one publication in a scientific journal, with four additional manuscripts currently in preparation for publication.
In terms of dissemination, the project’s results have been widely shared with the public through targeted efforts. Two press releases were issued, one of which gathered national attention, resulting in widespread coverage across local, regional and national media channels. This project has been actively disseminated to the general public by the organization and participation in over 13 events. Including social media platforms, the outreach efforts have reached over 500,000 people fostering engagement and awareness of this project within broader audiences.
This project has achieved several significant advancements, with far-reaching impacts on both research and wider societal contexts. Key highlights include the detection of an aminoacidic repeat in the study species previously identified in other vertebrates, which is associated with biological rhythm determination. Furthermore, this genetic variant has been linked to behavioural traits that can potentially influence individual susceptibility at being captured, providing novel insights into the genetic basis of fisheries-induced selection.
Another major advancement has been the development of a high-quality chromosome-level assembly and annotation of the study species’ genome. This outcome has been integrated into the Earth Biogenome Project, a global initiative aimed at sequencing the genomes of all eukaryote species within a decade. This contribution not only enhanced the project's research quality and potential, but also supported a worldwide initiative generating and storing biological information as platform for open scientific research and supporting biodiversity conservation.
Furthermore, collaborative efforts with the Netherlands Institute of Ecology (NIOO-KNAW) have yielded fruitful outcomes, fostering strong connections between European research centres. As a result of this collaboration, a new research line has been developed, translating individual-level genetic findings into population-level insights. This follow-up research is aimed to explore how behavioural differences influencing individual fish vulnerability are translated into genetic differences between populations subject to different fishing pressures.
The described advances not only elevate the researcher’s career trajectory but also imply broader societal implications. By describing the genetic foundations of behaviour and vulnerability to fishing pressure, the project's findings contribute valuable knowledge to sustainable fisheries management and conservation strategies, promoting long-term health and resilience of marine ecosystems.
Female individual of Xyrichtys novacula. Image taken by Eneko Aspillaga