Distribution of genetic diversity reveals colonization patterns and philopatry of the loggerhead sea turtles across geographic scales

Abstract

Understanding the processes that underlie the current distribution of genetic diversity in endangered species is a goal of modern conservation biology. Specifically, the role of colonization and dispersal events throughout a species' evolutionary history often remains elusive. The loggerhead sea turtle (Caretta caretta) faces multiple conservation challenges due to its migratory nature and philopatric behaviour. Here, 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 Boa Vista, Cabo Verde). Data analysis using hypothesis-driven population genetic models suggests the colonization of the Atlantic has occurred in two distinct waves, each corresponding to a major mtDNA lineage. 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 island-specific nesting groups, despite significant genetic structure. This structure stems from female philopatric behaviours, which could further be detected by weak but significant differentiation amongst beaches separated by only a few kilometres on the island of Boa Vista. Exploring biogeographic processes at diverse geographic scales improves our understanding of 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' evolutionary potential.

Figure 1

Sample origin across the three geographic regions. Represented are the number of sequences used in this study for each specific geographic scale: Atlantic, regional (Cabo Verde) and local (Island of Boa Vista). These numbers include both the sequences retrieved from the literature as well as those specifically collected for this study.

Figure 2

Results of hypothesis-testing generated scenarios with Approximate Bayesian Computation. In (a), prior distributions of simulated datasets for all the 5 scenarios in relation to the observed dataset (figure produced by the software). In (b), is shown the multinomial logistic regression used to infer the best-fit model considering a gradual increase of simulated datasets, n, ranked by proximity to the observed dataset. Specifically, the x-axis denotes the number of simulated datasets closer to the observed dataset, n = {8000, 16,000, 24,000, 32,000, 40,000}; the y-axis shows the logit regression R² as a function of n. In (c) is given the evolution of R² ´s confidence intervals for the n in (b). The * denotes non-overlapping confidence intervals among scenarios for the same n. The figure was partially produced with DIYABC v2.1.0.

Figure 3

Reconciling the hypotheses of the colononization of the Atlantic Ocean. Visual representation of the colonisation and dispersal model of the haplogroups I-CCA1 and II-CCA2, supporting two colonisation waves, one via the Isthmus of Panama and the other, later, via South Africa. The figure also highlights the role of the central Atlantic Cabo Verdean rookery as a stepping stone for each lineage across the Atlantic Ocean.

Figure 4

Distribution of average pairwise F_ST among the island-specific nesting groups of the archipelago. Linear regression of average pairwise F_ST per island along the East to West axis of the archipelago. A significant increase in average pairwise F_ST can be observed from East to West (R² = 0.275, p < 0.001).