Reinhold Hanel

All roads lead to home: panmixia of European eel in the Sargasso Sea

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.

On the origin and trigger of the notothenioid adaptive radiation

Adaptive radiation is usually triggered by ecological opportunity, arising through (i) the colonization of a new habitat by its progenitor; (ii) the extinction of competitors; or (iii) the emergence of an evolutionary key innovation in the ancestral lineage. Support for the key innovation hypothesis is scarce, however, even in textbook examples of adaptive radiation. Antifreeze glycoproteins (AFGPs) have been proposed as putative key innovation for the adaptive radiation of notothenioid fishes in the ice-cold waters of Antarctica. A crucial prerequisite for this assumption is the concurrence of the notothenioid radiation with the onset of Antarctic sea ice conditions. Here, we use a fossil-calibrated multi-marker phylogeny of nothothenioid and related acanthomorph fishes to date AFGP emergence and the notothenioid radiation. All time-constraints are cross-validated to assess their reliability resulting in six powerful calibration points. We find that the notothenioid radiation began near the Oligocene-Miocene transition, which coincides with the increasing presence of Antarctic sea ice. Divergence dates of notothenioids are thus consistent with the key innovation hypothesis of AFGP. Early notothenioid divergences are furthermore congruent with vicariant speciation and the breakup of Gondwana.

Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons

The diversification of the teleost suborder Notothenioidei (Perciformes) in Antarctic waters provides one of the most striking examples of a marine adaptive radiation. Along with a number of adaptations to the cold environment, such as the evolution of antifreeze glycoproteins, notothenioids diversified into eight families and at least 130 species. Here, we investigate the genetic population structure of the humped rockcod (Gobionotothen gibberifrons), a benthic notothenioid fish. Six populations were sampled at different locations around the Scotia Sea, comprising a large part of the species’ distribution range (N = 165). Our analyses based on mitochondrial DNA sequence data (352 bp) and eight microsatellite markers reveal a lack of genetic structuring over large geographic distances (ΦST ≤ 0.058, FST ≤ 0.005, P values nonsignificant). In order to test whether this was due to passive larval dispersal, we used GPS‐tracked drifter trajectories, which approximate movement of passive surface particles with ocean currents. The drifter data indicate that the Antarctic Circumpolar Current (ACC) connects the sampling locations in one direction only (west–east), and that passive transport is possible within the 4‐month larval period of G. gibberifrons. Indeed, when applying the isolation‐with‐migration model in IMA, strong unidirectional west‐east migration rates are detected in the humped rockcod. This leads us to conclude that, in G. gibberifrons, genetic differentiation is prevented by gene flow via larval dispersal with the ACC.

Mitochondrial phylogeography of the European sprat (Sprattus sprattus L., Clupeidae) reveals isolated climatically vulnerable populations in the Mediterranean Sea and range expansion in the northeast Atlantic

We examined the genetic structure of the European sprat (Sprattus sprattus) by means of a 530‐bp sequence of the mitochondrial control region from 210 fish originating from seven sampling localities of its distributional range. Phylogeographical analysis of 128 haplotypes showed a phylogenetic separation into two major clades with the Strait of Sicily acting as a barrier to gene flow between them. While no population differentiation was observed based on analysis of molecular variance and net nucleotide differences between samples of the Baltic Sea, the North Sea and the Bay of Biscay nor between the Black Sea and the Bosporus, a strong population differentiation between these samples and two samples from the Mediterranean Sea was found. Further, the biggest genetic distance was observed within the Mediterranean Sea between the populations of the Gulf of Lyon and the Adriatic Sea, indicating genetic isolation of these regions. Low genetic diversities and star‐like haplotype networks of both Mediterranean Sea populations point towards recent demographic expansion scenarios after low population size, which is further supported by negative FS values and unimodal mismatch distributions with a low mean. Along the northeast Atlantic coast, a northwards range expansion of a large and stable population can be assumed. The history of a diverse but differentiated Black Sea population remains unknown due to uncertainties in the palaeo‐oceanography of this sea. Our genetic data did not confirm the presently used classification into subspecies but are only preliminary in the absence of nuclear genetic analyses.

Brominated flame retardants and dechloranes in eels from German Rivers

The levels of PBDEs, alternate BFRs and dechloranes in European Eel (Anguilla anguilla) samples (elvers, yellow and silver eels) were investigated to compare the contamination of eels from the rivers Elbe and Rhine and to estimate the BFR contamination throughout the eels life cycle. PBDEs were the dominating flame retardants (FRs) in muscle tissues of yellow and silver eels, while the alternate BFR 2,3-dibromopropyl-2,4,6-tribromophenyl ether (DPTE) and the Dechlorane 602 were the dominating FRs in elvers (juvenile eels). Concentrations of FRs in silver eels from river Rhine were generally higher than concentrations in other eels analysed with up to 46 ng g(-1) wet weight (ww) ∑PBDEs. The concentrations in yellow and silver eels from river Elbe were similar with an average of 9.0±5.1 ng g(-1)ww and 8.1±3.7 ng g(-1)ww respectively. PBDE concentrations in elvers were comparably low (0.02 (BDE-100) to 0.1 (BDE-183) ng g(-1)ww), which lead to the conclusion that these contaminants were mostly ingested within the rivers. Among the alternate BFRs and dechloranes, DPTE as well as the Dechlorane 602 and Dechlorane Plus (DP) were found in all life cycle stages and rivers with concentrations between 0.01 ng g(-1)ww and 0.7 ng g(-1)ww. Dechlorane 603 could only be detected in silver eels from river Rhine. Pentabromoethylbenzene (PBEB) was only found in yellow and silver eels and bis(2-ethylhexyl)tetrabromophthalate (BEHTBP) could only be detected in elvers. These are the first reports of Dec-602 and 603 in aquatic organisms from Europe. The results of this study show the lasting relevance of PBDEs as contaminants in rivers and river-dwelling species but also the growing relevance of emerging contaminants such as alternate BFRs and dechloranes.

Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation

Antarctic notothenioid fishes represent a rare example of a marine species flock. They evolved special adaptations to the extreme environment of the Southern Ocean including antifreeze glycoproteins. Although lacking a swim bladder, notothenioids have diversified from their benthic ancestor into a wide array of water column niches, such as epibenthic, semipelagic, cryopelagic and pelagic habitats. Applying stable carbon (C) and nitrogen (N) isotope analyses to gain information on feeding ecology and foraging habitats, we tested whether ecological diversification along the benthic–pelagic axis followed a single directional trend in notothenioids, or whether it evolved independently in several lineages. Population samples of 25 different notothenioid species were collected around the Antarctic Peninsula, the South Orkneys and the South Sandwich Islands. The C and N stable isotope signatures span a broad range (mean δ13C and δ15N values between −25.4‰ and −21.9‰ and between 8.5‰ and 13.8‰, respectively), and pairwise niche overlap between four notothenioid families was highly significant. Analysis of isotopic disparity‐through‐time on the basis of Bayesian inference and maximum‐likelihood phylogenies, performed on a concatenated mitochondrial (cyt b) and nuclear gene (myh6, Ptr and tbr1) data set (3148 bp), showed that ecological diversification into overlapping feeding niches has occurred multiple times in parallel in different notothenioid families. This convergent diversification in habitat and trophic ecology is a sign of interspecific competition and characteristic for adaptive radiations.

Evolution of the immune system influences speciation rates in teleost fishes

Teleost fishes constitute the most species-rich vertebrate clade and exhibit extensive genetic and phenotypic variation, including diverse immune defense strategies. The genomic basis of a particularly aberrant strategy is exemplified by Atlantic cod, in which a loss of major histocompatibility complex (MHC) II functionality coincides with a marked expansion of MHC I genes. Through low-coverage genome sequencing (9–39×), assembly and comparative analyses for 66 teleost species, we show here that MHC II is missing in the entire Gadiformes lineage and thus was lost once in their common ancestor. In contrast, we find that MHC I gene expansions have occurred multiple times, both inside and outside this clade. Moreover, we identify an association between high MHC I copy number and elevated speciation rates using trait-dependent diversification models. Our results extend current understanding of the plasticity of the adaptive immune system and suggest an important role for immune-related genes in animal diversification.

A century of research on the larval distributions of the Atlantic eels: a re-examination of the data

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 Schmidts 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 remain about the marine life histories of the Atlantic eels.

Comparative population genetics of seven notothenioid fish species reveals high levels of gene flow along ocean currents in the southern Scotia Arc, Antarctica

The Antarctic fish fauna is characterized by high endemism and low species diversity with one perciform suborder, the Notothenioidei, dominating the whole species assemblage on the shelves and slopes. Notothenioids diversified in situ through adaptive radiation and show a variety of life history strategies as adults ranging from benthic to pelagic modes. Their larval development is unusually long, lasting from a few months to more than a year, and generally includes a pelagic larval stage. Therefore, the advection of eggs and larvae with ocean currents is a key factor modulating population connectivity. Here, we compare the genetic population structures and gene flow of seven ecologically distinct notothenioid species of the southern Scotia Arc based on nuclear microsatellites and mitochondrial DNA sequences (D-loop/cytochrome b). The seven species belong to the families Nototheniidae (Gobionotothen gibberifrons, Lepidonotothen squamifrons, Trematomus eulepidotus, T. newnesi) and Channichthyidae (Chaenocephalus aceratus, Champsocephalus gunnari, Chionodraco rastrospinosus). Our results show low-population differentiation and high gene flow for all investigated species independent of their adult life history strategies. In addition, gene flow is primarily in congruence with the prevailing ocean current system, highlighting the role of larval dispersal in population structuring of notothenioids.

Diversity and disparity through time in the adaptive radiation of Antarctic notothenioid fishes.

According to theory, adaptive radiation is triggered by ecological opportunity that can arise through the colonization of new habitats, the extinction of antagonists or the origin of key innovations. In the course of an adaptive radiation, diversification and morphological evolution are expected to slow down after an initial phase of rapid adaptation to vacant ecological niches, followed by speciation. Such ‘early bursts’ of diversification are thought to occur because niche space becomes increasingly filled over time. The diversification of Antarctic notothenioid fishes into over 120 species has become one of the prime examples of adaptive radiation in the marine realm and has likely been triggered by an evolutionary key innovation in the form of the emergence of antifreeze glycoproteins. Here, we test, using a novel time‐calibrated phylogeny of 49 species and five traits that characterize notothenioid body size and shape as well as buoyancy adaptations and habitat preferences, whether the notothenioid adaptive radiation is compatible with an early burst scenario. Extensive Bayesian model comparison shows that phylogenetic age estimates are highly dependent on model choice and that models with unlinked gene trees are generally better supported and result in younger age estimates. We find strong evidence for elevated diversification rates in Antarctic notothenioids compared to outgroups, yet no sign of rate heterogeneity in the course of the radiation, except that the notothenioid family Artedidraconidae appears to show secondarily elevated diversification rates. We further observe an early burst in trophic morphology, suggesting that the notothenioid radiation proceeds in stages similar to other prominent examples of adaptive radiation.