Population genomics of the nesting and foraging areas of the loggerhead turtle (Caretta caretta) facing climate change

Abstract

[eng] Genomic techniques are increasingly being utilized in conservation biology, providing critical insights into the behavior, reproductive success, and various threats faced by vulnerable species. The loggerhead sea turtle (Caretta caretta) is particularly sensitive to climate change and presents a complex life cycle characterized by long migrations from nesting populations to foraging grounds. The threats and characteristics of the species highlight the importance of understanding its population dynamics for informed management decisions and effective conservation strategies.

In this study, we focused on loggerhead turtles at different life stages. We first established a robust genomic baseline using the 2bRAD technique, analyzing 278 individuals from three regional management units (RMUs): the Mediterranean RMU (MED), represented by individuals from 11 nesting sites; the North West Atlantic RMU (NWA), represented by individuals from two nesting sites; and the North East Atlantic RMU (NEA), represented by individuals from one nesting site. We revealed significant genetic differentiation among the three RMUs and subsequently within the Mediterranean RMU identified three genetically differentiated SubRMUs: Greece (GRE), Levantine (LEV), and Sirte (SIR).

Additionally, we tested our baseline assessing the natal origin of juvenile loggerhead turtles in foraging areas employing a hierarchical approach, moving from a global perspective that included all three RMUs to a regional level that considered the three SubRMUs within the Mediterranean. We genotyped 103 individuals from four Mediterranean foraging areas: the Catalan region (CAT), Lampedusa (LAM), Eastern Aegean Sea (EAS), and Western Aegean Sea (WAS). Only 3 individuals were assigned to

NWA and 1 to NEA, thus indicating that these foraging areas are primarly used by Mediterranean individuals. Among the 99 individuals assigned to the Mediterranean RMU, the individuals assigned to the Lebantine SubRMU were predominant, with some exhibiting mixed assignments, indicating some admixture among subregions.

Finally, to assess the rapid increase in the number of nesting events observed in Spain, we sampled 45 hatchlings from eight nests laid between 2016 and 2019. We found that nests were laid by different females, except for two nests attributed to the same female but within the same season. This suggests that the nesting activity is due to a surge of colonizing individuals rather than a return of females born in the region. We hypothesize that the rising number of colonizers results from successful conserva- tion efforts, a feminization of the originating populations, and earlier sexual maturation among individuals. Using our baseline, we identified in the emerging nesting area, one hybrid nest between an Atlantic female and a Mediterranean male assigned to the Sirte SubRMU, as well as several nests resulting from the genetic admixture among different Mediterranean SubRMUs. Thus, in response to climate change, the expansion into new nesting sites may be promoting genetic mixing between previously isolated populations, with potential implications for the species’ conservation. Our results not only clarify the current status of this colonization, but also highlight the need for ongoing efforts to monitor returning individuals to confirm the establishment of a stable resident population.

In conclusion, the results obtained in this study provide critical information for understanding the ecological and evolutionary processes affecting loggerhead sea turtles. Our findings will contribute to enhancing conservation strategies in long lived species with high and complex dispersal behavior by identifying populations impacted by threats beyond nesting areas and facilitating the study of specific origins in mixed foraging habitats.

[spa] La tortuga boba (Caretta caretta) es la tortuga marina más abundante en el Mar Mediterráneo y presenta un ciclo de vida complejo entre zonas de anidación y de alimentación. Evaluar su estructuración poblacional, identificar el origen natal de los juveniles en zonas de alimentación y analizar la nidificación emergente como resultado del cambio climático permitirá diseñar estrategias de gestión adecuadas. El reciente desarrollo de herramientas genómicas para a especie, como el 2bRAD, permite abordar estas cuestiones a pesar de la complejidad que presenta la especie.

En esta tesis, se utilizó esta técnica genómica para construir un baseline genómico de las tres Unidades de Manejo Regional (RMU) que pueden contribuir con individuos presentes en el Mediterráneo: Atlántico-Noroeste (NWA), Atlántico-Noreste (NEA) y Mediterráneo (MED) Se identificó una diferenciación genética significativa entre las 3 RMUs y dentro del Mediterráneo se detectaron tres SubRMUs: Grecia, Levante y Sirte. El baseline se utilizó para asignar juveniles de las zonas de alimentación tanto a nivel de RMU como SubRMU con alta precisión (>0.7), y se detectaron individuos de origen mixto entre SubRMUs.

Asimismo, se evaluó el aumento de anidaciones en España analizando 45 crías de 8 nidos (2016-2019) con la misma metodología genómica. Se identificaron diferentes hembras nidificantes excepto por dos nidos puestos por la misma hembra durante la misma época de nidificación. Utilizando nuestro baseline, identificamos que uno de los nidos era mixto entre una hembra atlántica y un macho de origen mediterráneo, así como múltiples nidos resultantes de la reproducción entre individuos de diferentes SubRMUs mediterráneas. Los resultados sugieren que la anidación se debe a nuevos

individuos colonizadores y no a tortugas remigrantes. Hipotetizamos que esta colonización se relaciona con esfuerzos exitosos de conservación, feminización de la población y una maduración sexual temprana, y dado el alto porcentaje de crías hembras sugerimos el potencial establecimiento de una población residente en la región. El uso de herramientas genómicas como 2bRAD mejora la comprensión de los procesos evolutivos y ecológicos que afectan a especies vulnerables. Los resultados de esta tesis son clave para decisiones informadas en conservación de esta especie y enfrentar sus desafíos frente al cambio climático y la colonización de nuevas áreas.