European eels (Anguilla anguilla) undertake a approximately 5000-kilometer (km) spawning migration from Europe to the Sargasso Sea. The larvae are transported back to European waters by the Gulf Stream and North Atlantic Drift. However, details of the spawning migration remain unknown because tracking eels in the Atlantic Ocean has, so far, eluded study. Recent advances in satellite tracking enable investigation of migratory behavior of large ocean-dwelling animals. However, sizes of available tags have precluded tracking smaller animals like European eels. Here, we present information about the swimming direction, depth, and migratory behavior of European eels during spawning migration, based on a miniaturized pop-up satellite archival transmitter. Although the tagging experiment fell short of revealing the full migration to the Sargasso Sea, the data covered the first 1300 km and provided unique insights.

European eels (Anguilla anguilla) spawn in the remote Sargasso Sea in partial sympatry with American eels (Anguilla rostrata), and juveniles are transported more than 5000 km back to the European and North African coasts. The two species have been regarded as classic textbook examples of panmixia, each comprising a single, randomly mating population. However, several recent studies based on continental samples have found subtle, but significant, genetic differentiation, interpreted as geographical or temporal heterogeneity between samples. Moreover, European and American eels can hybridize, but hybrids have been observed almost exclusively in Iceland, suggesting hybridization in a specific region of the Sargasso Sea and subsequent nonrandom dispersal of larvae. Here, we report the first molecular population genetics study based on analysis of 21 microsatellite loci in larvae of both Atlantic eel species sampled directly in the spawning area, supplemented by analysis of European glass eel samples. Despite a clear East-West gradient in the overlapping distribution of the two species in the Sargasso Sea, we only observed a single putative hybrid, providing evidence against the hypothesis of a wide marine hybrid zone. Analyses of genetic differentiation, isolation by distance, isolation by time and assignment tests provided strong evidence for panmixia in both the Sargasso Sea and across all continental samples of European eel after accounting for the presence of sibs among newly hatched larvae. European eel has declined catastrophically, and our findings call for management of the species as a single unit, necessitating coordinated international conservation efforts.

The spawning areas of the Atlantic freshwater eels were discovered about a century ago by the Danish scientist Johannes Schmidt who after years of searching found newly hatched larvae of the European eel, Anguilla anguilla, and the American eel, Anguilla rostrata, in the southern Sargasso Sea. The discovery showed that anguillid eels migrate thousands of kilometers to offshore spawning areas for reproduction, and that their larvae, called leptocephali, are transported equally long distances by ocean currents to their continental recruitment areas. The spawning sites were found to be related to oceanographic conditions several decades later by German and American surveys from 1979 to 1989 and by a Danish survey in 2007 and a German survey in 2011. All these later surveys showed that spawning occurred within a restricted latitudinal range, between temperature fronts within the Subtropical Convergence Zone of the Sargasso Sea. New data and re-examinations of Schmidt's data confirmed his original conclusions about the two species having some overlap in spawning areas. Although there have been additional collections of leptocephali in various parts of the North Atlantic, and both otolith research and transport modelling studies have subsequently been carried out, there is still a range of unresolved questions about the routes of larval transport and durations of migration. This paper reviews the history and basic findings of surveys for anguillid leptocephali in the North Atlantic and analyses a new comprehensive database that includes 22612 A. anguilla and 9634 A. rostrata leptocephali, which provides a detailed view of the spatial and temporal distributions and size of the larvae across the Atlantic basin and in the Mediterranean Sea. The differences in distributions, maximum sizes, and growth rates of the two species of larvae are likely linked to the contrasting migration distances to their recruitment areas on each side of the basin. Anguilla rostrata leptocephali originate from a more western spawning area, grow faster, and metamorphose at smaller sizes of <70 mm than the larvae of A. anguilla, which mostly are spawned further east and can reach sizes of almost 90 mm. The larvae of A. rostrata spread west and northwest from the spawning area as they grow larger, with some being present in the western Caribbean and eastern Gulf of Mexico. Larvae of A. anguilla appear to be able to reach Europe by entering the Gulf Stream system or by being entrained into frontal countercurrents that transport them directly northeastward. The larval duration of A. anguilla is suggested to be quite variable, but gaps in sampling effort prevent firm conclusions. Although knowledge about larval behaviour is lacking, some influences of directional swimming are implicated by the temporal distributions of the largest larvae. Ocean-atmosphere changes have been hypothesized to affect the survival of the larvae and cause reduced recruitment, so even after about a century following the discovery of their spawning areas, mysteries still rema...

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The two primary ways that species respond to heterogeneous environments is through local adaptation and phenotypic plasticity. The American eel (Anguilla rostrata) presents a paradox; despite inhabiting drastically different environments [1], the species is panmictic [2, 3]. Spawning takes place only in the southern Sargasso Sea in the Atlantic Ocean [1]. Then, the planktonic larvae (leptocephali) disperse to rearing locations from Cuba to Greenland, and juveniles colonize either freshwater or brackish/saltwater habitats, where they spend 3-25 years before returning to the Sargasso Sea to spawn as a panmictic species. Depending on rearing habitat, individuals exhibit drastically different ecotypes [4-6]. In particular, individuals rearing in freshwater tend to grow slowly and mature older and are more likely to be female in comparison to individuals that rear in brackish/saltwater [4, 6]. The hypothesis that phenotypic plasticity alone can account for all of the differences was not supported by three independent controlled experiments [7-10]. Here, we present a genome-wide association study that demonstrates a polygenic basis that discriminates these habitat-specific ecotypes belonging to the same panmictic population. We found that 331 co-varying loci out of 42,424 initially considered were associated with the divergent ecotypes, allowing a reclassification of 89.6%. These 331 SNPs are associated with 101 genes that represent vascular and morphological development, calcium ion regulation, growth and transcription factors, and olfactory receptors. Our results are consistent with divergent natural selection of phenotypes and/or genotype-dependent habitat choice by individuals that results in these genetic differences between habitats, occurring every generation anew in this panmictic species.