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Eizaguirre, C.

Publications and source records attributed to Eizaguirre, C..

15 recordsLinked to original sources

Epigenetic signatures of infection within and across generations in the endangered Loggerhead sea turtle

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.

genetics↗

Habitat-specific environmental characteristics are associated with the movement of male and female loggerhead sea turtles

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.

zoology↗

Warming-induced sex bias fuels deceptive conservation success in sea turtles

Global warming threatens species with temperature-dependent sex determination (TSD) by risking extreme offspring sex-ratio bias. In sea turtles, warmer incubation conditions produce more females. Such biases can transiently inflate apparent population growth before male scarcity undermines reproduction, possibly leading to population extinction. Here, we combine 15 years of field monitoring, drone-based sex-ratio surveys, Argos telemetry, and eco-physiological modelling to test whether rising temperatures underpin the rapid increase in loggerhead (Caretta caretta) nesting in Cabo Verde, one of the worlds largest populations. Historical air temperature, lagged by one generation, predicts current nest counts, consistent with a climate-driven, female-biased population. Drone surveys reveal an approximately 9:1 female-to-male breeding sex ratio across two consecutive breeding seasons, and simulations reproduce observed nesting trajectories under historical warming but not under null (no-warming) scenarios. Extending the analysis to 28 global loggerhead populations reveals consistent links between temperatures, latitude, and nesting trends. Our results identify warming-induced sex ratio bias as a key, yet deceptive, driver of apparent recovery, highlighting the need to reassess conservation success through the lens of demography of TSD species.

ecology↗

DNA methylation reveals evolved buffering responses to climate-driven sex ratio skew in sea turtles

Species with temperature-dependent sex determination (TSD), including all sea turtles which produce females at warmer temperatures, face projections of demographic collapse under climate-driven sex ratio skews. However, the accuracy of such predictions remains uncertain, as current models rely heavily on indirect sex ratio proxies due to the lack of a scalable, non-invasive method for sexing hatchlings. Through whole methylome sequencing, we identified 777 sex-associated DNA methylation markers from blood samples of sex-verified loggerhead turtle (Caretta caretta) hatchlings incubated at three controlled temperatures. Applying these markers to a large-scale field experiment showed that classic nest temperature-based models overestimated female production by an average of up to 60.2%, suggesting the presence of evolved buffering mechanisms against thermal effects on sex determination. Our findings highlight the need to revise climate-driven sex ratio forecasts with empirical field data, such as methylation-based assessments, to better understand and safeguard the hidden resilience of vulnerable TSD species.

zoology↗

The migration of an expanding sea turtle population alters the structure of marine megafauna communities

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 seasons 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 seasons 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.

ecology↗

Chromosome-level genome assembly and methylome profile enables insights for the conservation of endangered loggerhead sea turtles

BackgroundCharacterising genetic and epigenetic diversity is crucial for assessing the adaptive potential of populations and species. Slow-reproducing and already threatened species, including endangered sea turtles, are particularly at risk. Those species with temperature-dependent sex determination (TSD) have heightened climate vulnerability, with sea turtle populations facing feminisation and extinction under future climate change. High- quality genomic and epigenomic resources will therefore support conservation efforts for these flagship species with such plastic traits. FindingsWe 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, 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 29,883 annotated genes. We then extracted the ONT-derived methylome and validated it via whole genome bisulfite sequencing of ten loggerheads from the same population. Applying our novel resources, we reconstructed population size fluctuations and matched them with major climatic events and niche availability. We identified microchromosomes as key regions for monitoring genetic diversity and epigenetic flexibility. Isolating 191 TSD-linked genes, we further built the largest network of functional associations and methylation patterns for sea turtles to date. ConclusionsWe present a high-quality loggerhead sea turtle genome and methylome from the globally significant East Atlantic population. By leveraging ONT sequencing to create genomic and epigenomic resources simultaneously, we showcase this dual strategy for driving conservation insights into endangered sea turtles.

genomics↗

Complex life cycles and parasite-mediated trophic cascades drive species coexistence and the maintenance of genetic diversity

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.

ecology↗

DNA methylation carries signatures of sublethal effects under thermal stress in loggerhead sea turtles

Rising global temperatures are a major threat to biodiversity. Whilst research generally focuses on thermal tolerance and mortality, sublethal effects may alter population dynamics and subsequently the adaptive potential of species. However, detecting such effects in the wild can be challenging, particularly for endangered and long-lived species with cryptic life histories. This necessitates the development of molecular tools to identify their signatures. In a split-clutch design experiment, we relocated clutches of wild, nesting loggerhead sea turtles (Caretta caretta) to a protected, in-situ hatchery. Eggs were then split into two sub-clutches incubated under shallow (35cm) or deep (55cm) conditions, with those in the shallow treatment experiencing significantly higher temperatures. Whilst no difference in hatching success was observed between treatments, hatchlings that emerged from the shallow, warmer treatment had altered length-mass relationships, and were weaker at fitness tests of locomotion capacity than their siblings incubated in the deep, cooler treatment. To characterise the molecular signatures of these thermal effects, we performed whole genome bisulfite sequencing on blood samples collected upon emergence. This identified 714 differentially methylated sites between treatments, including on genes with neuronal development, cytoskeleton, and sex determination functions. Taken together, our results show that higher incubation temperatures can induce sublethal effects in hatchlings, which are reflected in their DNA methylation status at identified sites. Such sites could be used as biomarkers of thermal stress, especially if they are retained across life stages. Overall, this study suggests that global warming may have population-level consequences for loggerhead sea turtles, by reducing hatchling quality, dispersal capacity and the adaptive potential of this species. Conservation efforts for climate-threatened taxa like endangered sea turtles will therefore benefit from strategies that monitor and mitigate exposure to incubation temperatures that lead to sublethal effects.

genomics↗

Parasite-mediated predation determines the infection in a complex predator-prey 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.

ecology↗

Productive foraging sites enhance maternal health and impact offspring fitness in a capital breeding species

Feeding ecology is an essential component of an organisms life, but foraging comes with risks and energetic costs. Species in which populations exhibit more than one feeding strategy, such as sea turtles, are good systems for investigating how feeding ecology impacts life-history traits, reproduction and carried over effects across generations. Here, we investigated how the feeding ecology of loggerhead sea turtles (Caretta caretta) nesting at the Cabo Verde archipelago correlates with reproductive outputs and offspring fitness. We determined the feeding ecology of female turtles before and during the breeding season from stable isotope analysis of carbon and nitrogen, and correlated isotopic ratio with female and hatchling fitness traits. We found that female turtles feeding at higher trophic positions produced larger clutches. We also found that females with less depleted {delta}13C values, typical of productive foraging areas, had greater fat reserves, were less likely to be infected by leech parasites, and produced heavier offspring. The offspring of infected mothers with less depleted {delta}13C values performed best in crawling and self-righting trials than those of non-infected mothers with less depleted {delta}13C values. Overall, our study shows adult female loggerheads that exploit productive areas build capital reserves that impact their reproductive success and offspring fitness. Together, we uphold the suggestion that not all foraging habitats are equal, and can alter the fitness of populations.

ecology↗

Origin Matters: Using a Local Reference Genome Improves Measures in Population Genomics

Genome-level sequencing enables us to ask fundamental questions about the genetic basis of adaptation, population structure, and epigenetic mechanisms, but usually requires a suitable reference genome for mapping population-level re-sequencing data. In some model systems, multiple reference genomes are available, giving researchers the challenging task of determining which reference genome best suits their data. Here we compare the use of two different reference genomes for the three-spined stickleback (Gasterosteus aculeatus), one novel genome derived from a European gynogenetic individual and the published reference genome of a North American individual. Specifically, we investigate the impact of using a local reference versus one generated from a distinct lineage on several common population genomics analyses. Through mapping genome resequencing data of 60 sticklebacks from across Europe and North America, we demonstrate that genetic distance among samples and the reference impacts downstream analyses. Using a local reference genome increased mapping efficiency and genotyping accuracy, effectively retaining more and better data. Despite comparable distributions of the metrics generated across the genome using SNP data (i.e., {pi}, Tajimas D, and FST), window-based statistics using different references resulted in different outlier genes and enriched gene functions. A marker-based analysis of DNA methylation distributions had a comparably high overlap in outlier genes and functions, yet with distinct differences depending on the reference genome. Overall, our results highlight how using a local reference genome decreases reference bias to increase confidence in downstream analyses of the data. Such results have significant implications in all reference-genome-based population genomic analyses.

bioinformatics↗

Genetics survey reveals colonization and philopatry of the loggerhead sea turtles across geographic scales

AimUnderstanding the processes that underlie the distribution of genetic diversity in endangered species is a goal of modern conservation biology. Specifically, how population structure affects genetic diversity and contributes to a species adaptive potential remain elusive. The loggerhead sea turtle (Caretta caretta) faces multiple conservation challenges due to its migratory nature and philopatric behaviour. LocationsAtlantic Ocean, Cabo Verde, island of Boavista MethodsHere, using 4207 mtDNA sequences, we analysed the colonisation patterns and distribution of genetic diversity within a major ocean basin (the Atlantic), a regional rookery (Cabo Verde Archipelago) and a local island (Island of Boavista, Cabo Verde). ResultsHypothesis-driven population genetic models suggest the colonization of the Atlantic has occurred in two distinct waves, each corresponding to major mtDNA lineages. We propose the oldest lineage entered the basin via the isthmus of Panama and sequentially established aggregations in Brazil, Cabo Verde and in the area of USA and Mexico. The second lineage entered the Atlantic via the Cape of Good Hope, establishing colonies in the Mediterranean Sea, and from then on, re-colonized the already existing rookeries of the Atlantic. At the Cabo Verde level, we reveal an asymmetric gene flow maintaining links across nesting groups despite significant genetic structure amongst nesting groups. This structure stems from female philopatric behaviour which could further be detected by weak but significant structure amongst beaches separated by only a few kilometres on the island of Boavista. Main conclusionTo explore demographic processes at diverse geographic scales improves understanding the complex evolutionary history of highly migratory philopatric species. Unveiling the past facilitates the design of conservation programmes targeting the right management scale to maintain a species adaptive potential and putative response to human-induced selection.

evolutionary biology↗

Maternally derived sex steroid hormones impact sex ratios of loggerhead sea turtles

Global warming could drive species with temperature-dependent sex determination to extinction by persistently skewing offspring sex ratios. Evolved mechanisms that buffer these biases are therefore paramount for their persistence. Here, we tested whether maternally-derived sex steroid hormones affect the sex-determination cascade and provide a physiological mechanism to buffer sex ratio bias in the endangered loggerhead sea turtle (Caretta caretta). We quantified estradiol and testosterone in nesting females and their egg yolks at oviposition, before incubating nests in situ at standardised temperatures. Upon hatchling emergence, we developed a new, non-lethal method to establish the sex of individuals. Despite standardised incubation temperatures, sex ratios varied widely among nests, correlating non-linearly with the estradiol:testosterone ratio in egg yolks. Males were produced at an equal ratio, with females produced either side of this optimum. This result provides evidence that maternal hormone transfer forms a physiological mechanism that impacts sex determination in this endangered species.

physiology↗

DNA methylation facilitates local adaptation and adaptive transgenerational plasticity

While environmentally inducible epigenetic marks are discussed as one mechanism of transgenerational plasticity, environmentally stable epigenetic marks emerge randomly. When resulting in variable phenotypes, stable marks can be targets of natural selection analogous to DNA sequence-based adaptation processes. We studied both postulated pathways in natural populations of three-spined sticklebacks (Gasterosteus aculeatus) and sequenced their methylomes and genomes across a salinity cline. Consistent with local adaptation, populations showed differential methylation (pop-DMS) at genes enriched for osmoregulatory processes. In a two-generation experiment, 62% of these pop-DMS were insensitive to salinity manipulation, suggesting that they could be stable targets for natural selection. Two-thirds of the remaining inducible pop-DMS became more similar to patterns detected in wild populations from the corresponding salinity, and this pattern accentuated over consecutive generations, indicating a mechanism of adaptive transgenerational plasticity. Natural DNA methylation patterns can thus be attributed to two epigenetic pathways underlying the rapid emergence of adaptive phenotypes in the face of environmental change.

evolutionary biology↗

Region-specific magnetic field structure sea turtle populations

Philopatry and long distance migrations are common in the animal kingdom, of which sea turtles are flagship examples. Recent studies have suggested sea turtles use the Earths magnetic field to navigate across ocean basins to return to their natal area, yet the mechanisms underlying this process remain unknown. If true though, the genetic structure at nesting sites should positively correlate with differences in location-specific magnetic vectors within nesting regions. Here, we confirm this working hypothesis but only in certain regions of the world and for all sea turtle species nesting in those regions. Reversely, where no correlations were found between genetic differentiation and geomagnetic vectors, this was the case for all nesting sea turtle species. Our approach hence reveals parallel but not universal use of geomagnetic cues in sea turtles. We describe magneto-sensing regions as characterized by sharp clines of total and vertical field intensity vectors offering the navigation cues that increase philopatric accuracy and promote genetic structuring among sea turtle populations.

evolutionary biology↗