Christophe Eizaguirre

Infection can substantially reduce host fitness and influence population dynamics, yet it is often difficult to detect and quantify in wild animal populations. Molecular tools offer a valuable means of identifying cryptic infection in natural systems. Using whole-genome bisulfite sequencing, we examined whether infection with the parasitic leech Ozobranchus margoi is associated with DNA methylation variation in loggerhead sea turtles ( Caretta caretta ), while also assessing the potential value of this variation as a biomarker of parasite infection. In nesting females, we identified infection-associated differentially methylated CpG sites associated with genes implicated in immune signalling and cellular regulation. Offspring of infected females also showed infection-associated methylation patterns, despite not being directly exposed to the parasite themselves. Differential methylation analyses identified genes involved in immunity, neurodevelopment and metabolic activity, with limited overlap in associated genes and no overlap in differentially methylated sites between generations. Maternal and offspring genome-wide methylation levels showed a non-linear association that differed subtly with maternal infection status, indicating that infection modifies intergenerational methylation associations. Finally, methylation profiles showed strong discriminatory power for maternal infection status in both maternal and hatchling samples using machine learning models, supporting their potential as candidate biomarkers of cryptic infection. Together, these results show that parasite infection is associated with distinct, generation-specific DNA methylation signatures, and highlight the potential value of epigenetic data for monitoring cryptic infection states in conservation-relevant systems.

Linking animal movements to environmental drivers is essential for understanding ecological processes and anticipating species responses to climate change. We investigated habitat-specific movements in a globally significant aggregation of loggerhead turtles ( Caretta caretta ) nesting in Cabo Verde. Satellite tags on 15 adults (12 females, 3 males) provided multi-year tracks spanning breeding, migration, and foraging habitats. Movements and phenology differed by habitat. During the breeding season, females used either coastal areas, remaining within ∼20 m depth, or undertook long looping forays up to 360 km. Males showed two strategies: two remained resident in Cabo Verde waters, including Fra, the largest male tracked (Curved carapace length of 105 cm compared with a male mean of 90.7 ± 10.3 cm), while the third migrated annually to distant foraging grounds and returned ahead of the subsequent breeding season. In foraging habitats, turtles adopted neritic or oceanic strategies: neritic turtles remained localised in warm, productive waters, whereas oceanic turtles ranged widely in deeper, less productive areas. Time- and space-shift analyses showed that oceanic foragers used intermediate sea surface temperature and chlorophyll-a conditions relative to nearby or temporally shifted alternatives, consistent with movement within a thermal–trophic trade-off. Together, these results show how sex, body size, and energy balance drive habitat-specific movement dynamics in a changing ocean.

Climate warming can alter reproductive timing of species, yet the capacity for phenological adjustment in long-lived species, particularly marine ones, remains elusive. Using 17 years of monitoring data from one of the largest loggerhead turtle (Caretta caretta) populations, we investigated the environmental drivers of reproductive phenology and output. We found that warmer sea surface temperatures (SST) in both the feeding ground and the nesting ground advanced the start, peak, and end of the nesting season. We provide evidence for waves of arrival at the nesting ground, suggesting more turtles produce fewer clutches than previously thought. Inter-nesting intervals were shorter during episodes of higher SST, particularly in larger females, likely underpinned by metabolic scaling variation in reproductive pacing. Conversely, remigration intervals lengthened over time in all size classes, reflecting the detected continuous decrease in productivity in the feeding ground. As a result of reduced ocean productivity, both clutch size and clutch frequency also declined over the study period. Moreover, the declining trend in body size further reduces reproductive output, as smaller females produce smaller clutch sizes. Overall, we show that sea turtle population dynamics correlate with environmental parameters. The sustained decline in reproductive output underscores the need to mitigate the impacts of climate warming on the foraging area to safeguard this population, which, given its size, holds global significance.

Interactions shape community structures, yet the impact of large migratory influxes on communities, particularly marine ones, remains elusive. Using drone surveys, we investigated changes of marine megafauna communities (e.g., sharks, rays), during the mass migration of loggerhead sea turtles ( Caretta caretta ) in Cabo Verde, one of the largest, and growing, rookeries globally and a biodiversity hotspot. In high nesting density areas, with over 6,000 turtles detected in-water at the season’s peak, the community structured with sharks distributing between the turtles and the coastline. In low-density areas (∼500 turtles), no structuring was detected. After the season’s peak, increased shark abundance and shoreward movement suggest they anticipate a nutrient pulse from emerging hatchlings. Our results highlight the role of sea turtle abundance in structuring marine communities, both as a high-quality food resource (hatchlings) and a likely non-consumable species (adults). Overall, we show the significant impact of migratory species on marine megafauna communities.

Background: Characterizing genetic and epigenetic diversity is crucial for assessing the adaptive potential of threatened populations and species in the face of climate change. Sea turtles are particularly vulnerable due to their temperature-dependent sex determination (TSD) system, which heightens the risk of extreme sex ratio bias and extinction under future climate scenarios. High-quality genomic and epigenomic resources will therefore support conservation efforts for these endangered flagship species with such plastic traits. Findings: We generated a chromosome-level genome assembly for the loggerhead sea turtle (Caretta caretta) from the globally important Cabo Verde rookery. Using Oxford Nanopore Technology (ONT) and Illumina reads followed by homology-guided scaffolding to the same species, we achieved a contiguous (N50: 129.7 Mbp) and complete (BUSCO: 97.1%) assembly, with 98.9% of the genome scaffolded into 28 chromosomes and 33,887 annotated genes. We also extracted the blood methylome profile from our ONT reads, which was confirmed to be representative of the reference population via whole-genome bisulfite sequencing of 10 additional loggerheads from the same population. Applying our novel resources, we revealed high conservation of synteny between sea turtle species, reconstructed population size fluctuations in line with major climatic events, and identified microchromosomes as key regions for monitoring genetic diversity and epigenetic flexibility. Isolating 199 TSD-linked genes, we further built a large network of functional protein associations and blood-based methylation patterns. Conclusions: We present a high-quality loggerhead sea turtle genome and methylome from the globally significant East Atlantic population. By leveraging ONT sequencing, we generate genomic and epigenomic resources simultaneously and showcase the potential of this approach for driving molecular insights for conservation of endangered sea turtles.

Duplicated genes provide the opportunity for evolutionary novelty and adaptive divergence. In many cases, having more gene copies increases gene expression, which might facilitate adaptation to stressful or novel environments. Conversely, overexpression or misexpression of duplicated genes can be detrimental and subject to negative selection. In this scenario, newly duplicate genes may evade purifying selection if they are epigenetically silenced, at least temporarily, leading them to persist in populations as copy number variations (CNVs). In animals and plants, younger gene duplicates tend to have higher levels of DNA methylation and lower levels of gene expression, suggesting epigenetic regulation could promote the retention of gene duplications via expression repression or silencing. Here, we test the hypothesis that DNA methylation variation coincides with young duplicate genes that are segregating as CNVs in six populations of the three‐spined stickleback that span a salinity gradient from 4 to 30 PSU. Using reduced‐representation bisulfite sequencing, we found DNA methylation and CNV differentiation outliers rarely overlapped. Whereas lineage‐specific genes and young duplicates were found to be highly methylated, just two gene CNVs showed a significant association between promoter methylation level and copy number, suggesting that DNA methylation might not interact with CNVs in our dataset. If most new duplications are regulated for dosage by epigenetic mechanisms, our results do not support a strong contribution from DNA methylation soon after duplication. Instead, our results are consistent with a preference to duplicate genes that are already highly methylated.

Ongoing climatic shifts and increasing anthropogenic pressures demand an efficient delineation of conservation units and accurate predictions of populations' resilience and adaptive potential. Molecular tools involving DNA sequencing are nowadays routinely used for these purposes. Yet, most of the existing tools focusing on sequence‐level information have shortcomings in detecting signals of short‐term ecological relevance. Epigenetic modifications carry valuable information to better link individuals, populations, and species to their environment. Here, we discuss a series of epigenetic monitoring tools that can be directly applied to various conservation contexts, complementing already existing molecular monitoring frameworks. Focusing on DNA sequence‐based methods (e.g. DNA methylation, for which the applications are readily available), we demonstrate how (a) the identification of epi‐biomarkers associated with age or infection can facilitate the determination of an individual's health status in wild populations; (b) whole epigenome analyses can identify signatures of selection linked to environmental conditions and facilitate estimating the adaptive potential of populations; and (c) epi‐eDNA (epigenetic environmental DNA), an epigenetic‐based conservation tool, presents a non‐invasive sampling method to monitor biological information beyond the mere presence of individuals. Overall, our framework refines conservation strategies, ensuring a comprehensive understanding of species' adaptive potential and persistence on ecologically relevant timescales.

The interplay of host–parasite and predator–prey interactions is critical in ecological dynamics because both predators and parasites can regulate communities. But what is the prevalence of infected prey and predators when a parasite is transmitted through trophic interactions considering stochastic demographic changes? Here, we modelled and analysed a complex predator–prey–parasite system, where parasites are transmitted from prey to predators. We varied parasite virulence and infection probabilities to investigate how those evolutionary factors determine species’ coexistence and populations’ composition. Our results show that parasite species go extinct when the infection probabilities of either host are small and that success in infecting the final host is more critical for the survival of the parasite. While our stochastic simulations are consistent with deterministic predictions, stochasticity plays an important role in the border regions between coexistence and extinction. As expected, the proportion of infected individuals increases with the infection probabilities. Interestingly, the relative abundances of infected and uninfected individuals can have opposite orders in the intermediate and final host populations. This counterintuitive observation shows that the interplay of direct and indirect parasite effects is a common driver of the prevalence of infection in a complex system.

Ecological and evolutionary processes shape the dynamics of species interactions, yet the drivers of eco-evolutionary feedback remain elusive. Here, we developed an individual-based model of a coevolving predator-prey-parasite system, in which predators can be infected by trophically transmitted parasites. We combined host-parasite coevolution with prey-predator interactions at an individual level, hence integrating evolutionary and ecological processes. We show that species coexist more when parasite-mediated selection is weak on both the predator and the prey. Population size and genotypic diversity of the parasite are highest at intermediate parasite-mediated selection on the predator and no parasite-mediated selection on the prey. Interestingly, we show that the evolution of super-resistant genotypes, where host genotypes have resistant alleles in all loci, is driven by interspecific interactions rather than by the population size of the host species. Overall, host-parasite coevolution shapes the direction of interspecific ecological interactions which, in turn, determine species coexistence and community diversity in a complex system.

The interplay of host-parasite and predator-prey interactions is critical in ecological dynamics because both predators and parasites play an important role in regulating populations and communities. But what is the prevalence of infected prey and predators when a parasite is transmitted through trophic interactions, particularly when stochastic fluctuations of demographical changes are allowed arising from individual-level dynamics? Here, we analysed the system stability and the frequency of infected and uninfected host subpopulations in a complex predator-prey-parasite system, where infection happens through trophic interactions transmitting parasites from prey to predators. We varied the parasite virulence implemented as reproductive costs imposed on infected hosts and the probabilities of parasites infecting the hosts per encounter, to investigate how those important evolutionary factors will determine the species coexistence and population composition. We further explored the role of stochasticity in our system by comparing our deterministic analysis with stochastic simulations. Our results show that parasites go extinct when the infection probabilities of either host are small. The success in infecting the final host (the predator) is more critical for the survival of the parasite species, as the threshold for infection probability of the predator is higher than that of the prey for three-species coexistence. While our stochastic simulations agree with deterministic predictions well in most parameter regions. However, in the border parameter regions between coexistence and extinction typically with high infection probabilities, while only one possible outcome in deterministic dynamics, both coexistence and extinction can happen in stochastic repeats under the same parameter values. This illustrates the importance of stochasticity and demographic fluctuations in species coexistence. In addition, the proportion of infected individuals increases with the infection probabilities in our deterministic analysis and stochastic simulations as expected. Interestingly, we found that in some parameter space, the relative frequencies of infected and uninfected individuals are different between the intermediate host (prey) and the final host (predator) populations. This counterintuitive observation shows that the interplay of host-parasite and predator-prey interactions lead to more complex dynamics than a simple resource-consumer relationship.