Speciation and demographic history of Atlantic eels (Anguilla anguilla and A. rostrata) revealed by mitogenome sequencing

Abstract

Processes leading to speciation in oceanic environments without obvious physical barriers remain poorly known. European and American eel (Anguilla anguilla and A. rostrata) spawn in partial sympatry in the Sargasso Sea. Larvae are advected by the Gulf Stream and other currents towards the European/North African and North American coasts, respectively. We analyzed 104 mitogenomes from the two species along with mitogenomes of other Anguilla and outgroup species. We estimated divergence time between the two species to identify major events involved in speciation. We also considered two previously stated hypotheses: one where the ancestral species was present in only one continent but was advected across the Atlantic by ocean current changes and another where population declines during Pleistocene glaciations led to increasing vicariance, facilitating speciation. Divergence time was estimated to ∼3.38 Mya, coinciding with the closure of the Panama Gateway that led to reinforcement of the Gulf Stream. This could have advected larvae towards European/North African coasts, in which case American eel would be expected to be the ancestral species. This scenario could, however, not be unequivocally confirmed by analyses of dN/dS, nucleotide diversity and effective population size estimates. Extended bayesian skyline plots showed fluctuations of effective population sizes and declines during glaciations, and thus also lending support to the importance of vicariance during speciation. There was evidence for positive selection at the ATP6 and possibly ND5 genes, indicating a role in speciation. The findings suggest an important role of ocean current changes in speciation of marine organisms.

Figure 1

Sampling locations of European and American eels. See Table 1 for population names and sample sizes.

Figure 2

Neighbour-joining tree of 96 mitogenome haplotypes. Bootstrap support >0.7 is shown above the branching points. The direction of nonsynonymous change is represented by coloured bars for all 13 genes along the respective branches and only given for mutations supported by at least two independent sequences. Numbers within gene boxes are the number of observed supported nonsynonymous changes compared with the total number of nonsynonymous changes. Amino-acid positions are shown next to the respective bar and a ‘*' denotes that the substitution is observed in sequences of independent ancestry. A ‘§' denotes that different amino-acid changes have occurred at this position and ‘#' denotes a back mutation. A ‘/' in the sequence name is used to separate between sampling location where haplotypes are shared between multiple samples. The red shape denotes the clade within the American lineage showing possible selection (see text). See Table 1 for sampling codes for individual sequences.

Figure 3

EBSPs of long-term trends in female effective population size (N_ef). Solid lines represent median N_ef-values, whereas dashed lines represent 95% HPD intervals. (a–c) European eel and (d–f) American eel. X-axes represent time and are scaled using estimates of TMRCA from the species phylogeny. (a, b and d, e) Time scaled by mean TMRCA using either the whole (a+d) or the partitioned mitogenome (b+e). (c and f) time scaled using the 95% HPD from the species analysis for the partitioned mitogenome.

Figure 4

Results of the FUBAR test along the ATP6 gene. (a) Rate of synonymous (dS) and nonsynonymous change (dN), and (b) dN/dS. Position 52 that showed significantly elevated dN/dS is denoted by a square, whereas the five fixed nonsynonymous amino-acid changes between European and American eels are denoted by dots.