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 B3.38 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.

Assessing pre- and post-zygotic barriers between North Atlantic eels (Anguilla anguilla and A. rostrata)

“…30 years (Åström and Dekker, 2007), possibly linked to inland pollution, dams and fisheries (Busch and Braun, 2014;Laporte et al, 2016). This decline suggests possible reduced densities of spawning eels that could lead to a reduced spatial overlap and hybridization (Albert et al, 2006;Jacobsen et al, 2014b). As environmental change within the Sargasso Sea itself may affect eel population sizes (Friedland et al, 2007;Bonhommeau et al, 2008), these two scenarios may not be mutually exclusive and the lack of hybrids could be a consequence of different environmental effects.…”

“…However, little evidence of this exists. In fact, the individual sequenced in this study (LEG29) showing ATP6-ATP5c1 mismatch is, to our knowledge, the only European individual to date that show the American mitogenome (see, for example, Avise et al, 1990;Daemen et al, 2001;Jacobsen et al, 2014b) besides F1 hybrids from Iceland (Avise et al, 1990;Albert et al, 2006;this study). As such, we find the possibility of unidirectional cytonuclear incompatibility unlikely.…”

“…Both species are panmictic (Als et al, 2011;Côté et al, 2013), show high effective population sizes (Côté et al, 2013;Pujolar et al, 2013;Jacobsen et al, 2014b) and spawn in the thermal fronts of the southern Sargasso Sea (McCleave et al, 1987;Tesch, 2003). Their spawning shows extensive overlap in space (Schmidt, 1923;Tesch, 2003;Munk et al, 2010) and time, with peak spawning time in February-April for American and March-June for European eel (McCleave et al, 1987;Tesch, 2003;Miller et al, 2015).…”

Relationship between amino acid changes in mitochondrial ATP6 and life-history variation in anguillid eels

“…Changes within ATP6 have been associated with differences in metabolism and selection linked to energetics [3,4,10]. In freshwater eels, selection may be linked to their migratory loops [8,11]. These involve spawning migration (from freshwater or coastal regions to the ocean) of highly variable distances in different species and consequently also a highly variable larval phase, as larvae rely on ocean currents for advection back to the continental feeding grounds [6,11].…”

“…The genus encompasses several species [6], which furthermore show high effective population sizes (e.g. [7,8]). Thus, selection is likely to be a stronger evolutionary force than genetic drift in these species.…”