Differential timing of gene expression regulation between leptocephali of the two Anguilla eel species in the Sargasso Sea

The unique life-history characteristics of North Atlantic catadromous eels have long intrigued evolutionary biologists, especially with respect to mechanisms that could explain their persistence as two ecologically very similar but reproductively and geographically distinct species. Differential developmental schedules during young larval stages have commonly been hypothesized to represent such a key mechanism. We performed a comparative analysis of gene expression by means of microarray experiments with American and European eel leptocephali collected in the Sargasso Sea in order to test the alternative hypotheses of (1) differential timing of gene expression regulation during early development versus (2) species-specific differences in expression of particular genes. Our results provide much stronger support for the former hypothesis since no gene showed consistent significant differences in expression levels between the two species. In contrast, 146 genes showed differential timings of expression between species, although the observed expression level differences between the species were generally small. Consequently, species-specific gene expression regulation seems to play a minor role in species differentiation. Overall, these results show that the basis of the early developmental divergence between the American and European eel is probably influenced by differences in the timing of gene expression regulation for genes involved in a large array of biological functions.     

Qualitative assessment of the diet of European eel larvae in the Sargasso Sea resolved by DNA barcoding

European eels (Anguilla anguilla) undertake spawning migrations of more than 5000 km from continental Europe and North Africa to frontal zones in the Sargasso Sea. Subsequently, the larval offspring are advected by large-scale eastward ocean currents towards continental waters. However, the Sargasso Sea is oligotrophic, with generally low plankton biomass, and the feeding biology of eel larvae has so far remained a mystery, hampering understanding of this peculiar life history. DNA barcoding of gut contents of 61 genetically identified A. anguilla larvae caught in the Sargasso Sea showed that even the smallest larvae feed on a striking variety of plankton organisms, and that gelatinous zooplankton is of fundamental dietary importance. Hence, the specific plankton composition seems essential for eel larval feeding and growth, suggesting a linkage between eel survival and regional plankton productivity. These novel insights into the prey of Atlantic eels may furthermore facilitate eel larval rearing in aquaculture, which ultimately may replace the unsustainable use of wild-caught glass eels.     

Differential effects of origin and salinity rearing conditions on growth of glass eels of the American eel Anguilla rostrata: implications for stocking programmes

In this study, growth patterns were monitored in controlled fresh and brackish water (BW) conditions for 7 months during Anguilla rostrata glass eel and elver stages. Null hypotheses tested were that there is no significant difference in growth between glass eels (1) collected from two geographic regions typified by different sex ratios, (2) reared in fresh and BW and (3) due to origin × salinity interactions. It was found that young A. rostrata from Mira River (MR, Cape Breton, Nova Scotia, Canada, an area where both males and females occur) grew faster than those from Grande-Rivière-Blanche (Québec, Canada, an area where population are highly skewed towards females; 99–100%). Anguilla rostrata from both origins also grew faster in BW, although there was a trend for origin × salinity interactions whereby this effect was more pronounced for fish from the MR. The results support the hypothesis that salinity can influence growth patterns, as possibly can quantitative genetic differences between A. rostrata glass eels from different origins. Possible explanations for these patterns and potential consequences for sex determination and translocation programmes are discussed.     

Individual assignment test reveals differential restriction to dispersal between two salmonids despite no increase of genetic differences with distance

In many species genes move over limited distances, such that genetic differences among populations or individuals are expected to increase as a function of geographical distance. In other species, however, genes may move any distance over a single generation time, such that no increase of genetic differences is expected to occur with distance. Patterns of gene dispersal have been assessed typically using this theoretical property. In this study, this classical approach based on a Mantel test was compared to a new method using individual assignment to reveal contrasts in dispersal patterns between 15 populations of brook charr Salvelinus fontinalis and 10 populations of Atlantic salmon Salmo salar sampled in eastern Canada, where both species co-occur naturally. Based on the Mantel test, we found evidence for neither an increase of genetic differences with distance in either species nor a significant contrast between them. The individual-based method, in contrast, revealed that individual assignment in both species was non random, being significantly biased toward geographically proximate locations. Furthermore, brook charr were on average assigned to a closer river than were salmon, according to a priori expectations based on the dispersal behaviour of the two species. We thus propose that individual assignment methods might be a promising and more powerful alternative to Mantel tests when isolation by distance cannot be postulated a priori.     

Magnetic particles associated with the lateral line of the European eel Anguilla anguilla

Magnetization measurements of the European eel Anguilla anguilla demonstrated the presence of magnetic material concentrated in the region of the mandibular canals of the lateral line system. The data suggest that the material is magnetite, has a size suitable for magnetoreception and is of biogenic origin. The presence of magnetic particles in the lateral line system is discussed in relation to their possible role in allowing the fish to orientate with respect to the geomagnetic field during their extensive oceanic spawning migrations.     

Genetic differentiation between populations of the European rose hip fly Rhagoletis alternata

We tested for genetic differentiation between populations of Rhagoletis alternata Fall. (Diptera: Tephritidae) on three different host species. We collected larvae from three rose species of the section Caninae ( Rosa canina L., Rosa corymbifera Borkh . , and Rosa rubiginosa L.) from 15 sites across Germany, where the three roses occurred together. Additionally, we sampled three sites in Switzerland. Roses differ in morphology (e.g. leaf glands) as well as phenology. We were able to score nine allozyme loci (five polymorphic). Populations from the three hosts did not differ in genetic variability. We found significant genetic differentiation between populations from different host species. However, the differentiation was very low (0.9%). Hence, we found no indication for host races. Furthermore, surprisingly little geographical structure of genetic differentiation was found between populations of this fruit fly across central Europe. We offer three mutually non-exclusive explanations for these findings. First, gene flow between populations of Rh. alternata is high. Second, the pattern of genetic differentiation is based on a recent expansion of the distributional range . Third, the ongoing gene flow between roses of the section Caninae acts as a hybrid bridge.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 619–625.     

Environmental factors affecting migration of the European eel in the Rivers Severn and Avon, England

Studies were conducted during 1991–1993 on environmental factors affecting the upstream migration of eels in the Rivers Severn and Avon, England. Migrants (> 156 000 pigmented elvers and > 189 000 juveniles) were trapped as they attempted to ascend weir or sluice barriers. Multiple regression models were developed to compare catches per trap per night (C) with data for various key environmental parameters at seven sites, from the tidal limit to a maximum of 42.5 km upstream. The key stimulus for migration of both elvers and juveniles at the tidal limit was water temperature, with some weaker monthly influences related to seasonal temperature increases. Smaller annual influences probably related to earlier glass eel recruitment into the lower estuary. A weak early tidal effect was demonstrated only once, in 1993 in the Severn. Temperature also exerted significant effects on C of juvenile eels at the tidal limit and in the non-tidal rivers, although effects weakened with distance upstream. Year, month, river flows and whether traps were mounted on weirs or sluices made only small contributions at a few sites. Distance between traps also contributed to combined data for upper Severn sites. The threshold temperature in all cases was 14–16°C, with low to zero catches below 10–11°C, catch maxima being achieved above 18–20°C. The implications of strong temperature-dependence of migration in relation to stock recruitment and management are discussed. Special reference is made to recent decreases in recruitment of eels to Europe and N. America and possible long-term effects of global warming.     

Genome‐wide single‐generation signatures of local selection in the panmictic European eel

Next‐generation sequencing and the collection of genome‐wide data allow identifying adaptive variation and footprints of directional selection. Using a large SNP data set from 259 RAD‐sequenced European eel individuals (glass eels) from eight locations between 34 and 64^oN, we examined the patterns of genome‐wide genetic diversity across locations. We tested for local selection by searching for increased population differentiation using F_ST‐based outlier tests and by testing for significant associations between allele frequencies and environmental variables. The overall low genetic differentiation found (F_ST = 0.0007) indicates that most of the genome is homogenized by gene flow, providing further evidence for genomic panmixia in the European eel. The lack of genetic substructuring was consistent at both nuclear and mitochondrial SNPs. Using an extensive number of diagnostic SNPs, results showed a low occurrence of hybrids between European and American eel, mainly limited to Iceland (5.9%), although individuals with signatures of introgression several generations back in time were found in mainland Europe. Despite panmixia, a small set of SNPs showed high genetic differentiation consistent with single‐generation signatures of spatially varying selection acting on glass eels. After screening 50 354 SNPs, a total of 754 potentially locally selected SNPs were identified. Candidate genes for local selection constituted a wide array of functions, including calcium signalling, neuroactive ligand–receptor interaction and circadian rhythm. Remarkably, one of the candidate genes identified is PERIOD, possibly related to differences in local photoperiod associated with the >30° difference in latitude between locations. Genes under selection were spread across the genome, and there were no large regions of increased differentiation as expected when selection occurs within just a single generation due to panmixia. This supports the conclusion that most of the genome is homogenized by gene flow that removes any effects of diversifying selection from each new generation.     

Evidence for isolation by time in the European eel (Anguilla anguilla L.)

Life history traits of highly vagile marine species, such as adult reproductive success and larval dispersal, are strongly determined by oceanographic and climatic forces. Nevertheless, marine organisms may show restricted dispersal in time and space. Patterns of isolation by distance (IBD) have been repeatedly observed in marine species. If spawning time is a function of geographical location, temporal and spatial isolation, can easily be confounded or misinterpreted. In this study, we aimed at discriminating between various forces shaping the genetic composition of recruiting juveniles of the European eel (Anguilla anguilla L.). By controlling for geographical variation, we assessed temporal variation and tested for possible isolation by time (IBT) between recruitment waves within and between years. Using 12 polymorphic allozyme and six variable microsatellite loci, we show that genetic differentiation was low (F(ST) = 0.01-0.002) and significant between temporal samples. Regression analysis between genetic and temporal distance, was consistent with a subtle interannual pattern of IBT. Our data suggest that the population dynamics of the European eel may be governed by a double pattern of temporal variance in genetic composition: (i) a broad-scale IBT of spawning cohorts, possibly as a consequence of the large migration loop in anguillids and strong variance in annual adult reproductive contribution; and (ii) a smaller-scale variance in reproductive success (genetic patchiness) within cohorts among seasonally separated spawning groups, most likely originating from fluctuating oceanic and climatic forces. The consistency of both mechanisms remains to be verified with fine-scale analyses of both spawning/migrating aged adults and their offspring to confirm the stochastic/deterministic nature of the IBT pattern in eel.     

Maturation patterns in female European eel: age and size at the silver eel stage

The maturation pattern in the female European eel Anguilla anguilla was studied by investigating age and size patterns of silver eels in different aquatic environments in Sweden, covering limnic, brackish and marine waters. The results neither supported the hypothesis that there is a critical size or age when eels enter the silvery stage, nor that size and age at maturity are positively related. Age at maturity, however, was observed to be negatively related to growth rate in all localities, i.e. the female reproductive tactic apparently is to become sexually mature at the earliest possible opportunity. Furthermore, it was recognized that a significant amount of variation was due to habitat differences, since the female eel maturation pattern deviated systematically between sampling sites, as it did also when the effect of growth rate was eliminated. Thus, the ability of the female eel to adjust maturation to an optimal size and age can be questioned, because the panmictic nature of the eel means local adaptations are unlikely Growth rate dependent differences suggest that variations in maturation patterns between eel environments are linked more to the opportunity for nutrient accumulation than to other aspects of growth.     

Distribution of individual inbreeding coefficients, relatedness and influence of stocking on native anadromous brown trout (Salmo trutta) population structure

We examined polymorphism at seven microsatellite loci in 4023 brown trout (Salmo trutta) collected from 32 tributaries to the Limfjord, Denmark (approximately 200 km) and from two hatcheries used for stocking. Populations differ in their estimated sizes and stocking histories. Mean individual inbreeding coefficients do not differ among locations within rivers. Relatedness varies between sites within rivers indicating varied local dynamics at a very small geographical scale. Relatedness is sometimes lower than expected among an equal number of simulated individuals with randomized genotypes, suggesting structure within locations. Five per cent of the genetic variance is distributed among rivers (F(ST) = 0.049), but in the western, less heavily stocked, area of the Limfjord a higher proportion of the genetic variance is distributed among rivers than among locations within rivers. The reverse is true of the eastern, more heavily stocked, area of the Limfjord. Here, a higher proportion of the genetic variance is distributed among locations within rivers than among rivers. Assignment tests reveal that the majority of trout (mean 77% of all fish) are more probably of local origin than hatchery origin but this proportion varies regionally, with rivers in the western area of the Limfjord showing a relatively high (mean 88%) and those in the eastern area showing a relatively low (mean 72%) proportion of locally assigned trout. These results can be interpreted as reflecting stocking impact. Also, the proportion of locally assigned trout correlates with the populations' stocking histories, with rivers presently subjected to stocking (hatchery trout) showing low (mean approximately 0.73), and rivers where stocking was discontinued showing high (mean approximately 0.84) proportions of local fish, probably reflecting lower survival of hatchery than of wild trout. There is evidence for isolation by distance at a large geographical scale when individual river populations are pooled into nine geographical regions but not at a small geographical scale when populations are considered individually. We reject the null hypothesis that stocking has had no impact on population structure but the relatively high proportion of locally assigned trout in populations where stocking with domestic fish no longer takes place suggests limited long-term success of stocking.     

Recruitment mechanism of the eel, Anguilla japonica, to the Japanese coast

A total of 149 Anguilla japonica elvers collected at 10 locations along the Japanese coast were aged according to otolith daily increments. The interrelationships among age, birth date, body size, pigmentation stage, sampling location and the timing of recruitment were examined in order to determine the recruitment mechanism of elvers to coastal waters.
First catches of eels were earlier in the locations at lower latitudes. Age at recruitment was roughly constant, 218 ± 29 (mean ± s.d.) days old, disregarding the localities, but a weak positive correlation was obtained between age and sampling date or timing of recruitment. Body length at recruitment was also constant, 56.3 ± 2.3 mm s.l., and showed no significant correlation with either locality or recruitment timing. Estimated birth date ranged from April to November, the mean ± s.d. being 22 July 1982 ± 42 days, suggesting a peak season spawning in summer. Birth date was closely related with both the latitude of location and sampling time. Pigmentation developed more at lower latitude. Recruitment mechanism of the Japanese eel was summarized as follows: the earlier-born individual recruits earlier at lower latitude and at younger age, but at a constant body size.     

Intraseasonal characterization of glass eel migration in the River Tiber: space and time dynamics

Glass eel ( Anguilla anguilla ) upstream migration was studied in the River Tiber estuary to obtain a better understanding of spatial and temporal migration dynamics within the season of ascent. Using data from glass eel fisheries, time series analysis of daily catches per unit of effort revealed a fortnightly cycle that can be related to invasion waves possibly corresponding to tidal currents. The amplitude of these waves appeared to correspond to the tidal area of the estuary. Furthermore, glass eels apparently had a delay in this area before resuming upstream migration.     

Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea

A main goal of population geneticists is to study patterns of gene flow to gain a better understanding of the population structure in a given organism. To date most efforts have been focused on studying gene flow at either broad scales to identify barriers to gene flow and isolation by distance or at fine spatial scales in order to gain inferences regarding reproduction and local dispersal. Few studies have measured connectivity at multiple spatial scales and have utilized novel tools to test the influence of both environment and geography on shaping gene flow in an organism. Here a seascape genetics approach was used to gain insight regarding geographic and ecological barriers to gene flow of a common reef sponge, Stylissa carteri in the Red Sea. Furthermore, a small‐scale (<1 km) analysis was also conducted to infer reproductive potential in this organism. At the broad scale, we found that sponge connectivity is not structured by geography alone, but rather, genetic isolation in the southern Red Sea correlates strongly with environmental heterogeneity. At the scale of a 50‐m transect, spatial autocorrelation analyses and estimates of full‐siblings revealed that there is no deviation from random mating. However, at slightly larger scales (100–200 m) encompassing multiple transects at a given site, a greater proportion of full‐siblings was found within sites versus among sites in a given location suggesting that mating and/or dispersal are constrained to some extent at this spatial scale. This study adds to the growing body of literature suggesting that environmental and ecological variables play a major role in the genetic structure of marine invertebrate populations.     

Timing and pattern of annual silver eel migration in two European watersheds are determined by similar cues

Many animals perform long‐distance migrations in order to maximize lifetime reproductive success. The European eel migrates several thousand kilometers between their feeding habitats in continental waters (fresh‐, brackish, and sea water) and their spawning area in the Sargasso Sea. Eels residing in freshwaters usually initiate their spawning migration as silver eels during autumn, triggered by diverse environmental cues. We analyzed the time series of silver eel downstream migration in Burrishoole, Ireland (1971–2015), and Imsa, Norway (1975–2015), to examine factors regulating the silver eel migration from freshwater to the sea. The migration season (90% of the run) generally lasted from 1 August to 30 November. Environmental factors acting in the months before migration impacted timing and duration of migration, likely through influencing the internal processes preparing the fish for migration. Once the migration had started, environmental factors impacted the day‐to‐day variation in number of migrants, apparently stimulating migration among those eels ready for migration. Both the day‐to‐day variation in the number of migrants and the onset of migration were described by nearly identical models in the two rivers. Variables explaining day‐to‐day variation were all associated with conditions that may minimize predation risk; number of migrants was reduced under a strong moon and short nights and increased during high and increasing water levels. Presence of other migrants stimulated migration, which further indicates that silver eel migration has evolved to minimize predation risk. The onset of migration was explained mainly by water levels in August. The models for duration of the migration season were less similar between the sites. Thus, the overall migration season seems governed by the need to reach the spawning areas in a synchronized manner, while during the actual seaward migration, antipredator behavior seems of overriding importance.     

Microsatellite DNA polymorphism confirms reproductive isolation and reveals differences in population genetic structure of cryptic pipistrelle bat species

Previous studies have indicated that the common European pipistrelle bat ( Pipistrellus pipistrellus ) comprises two cryptic species, P. pipistrellus and Pipistrellus pygmaeus , which differ in echolocation call frequency and mitochondrial DNA sequence. However, levels of divergence based on nuclear markers have not been examined, and hence the potential for male-mediated gene flow between the species cannot be discounted. Moreover, little is known about population structure and migration patterns in either species. Here, we describe the use of microsatellites to investigate nuclear DNA differentiation between, and the pattern of population genetic structure within, the two cryptic pipistrelle species. In total, 1300 individuals from 82 maternity colonies were sampled across the British Isles and Continental Europe. We show, using multivariate analyses, that colonies of the same species are generally genetically more similar to each other than to those from the other species regardless of geographical location. Our findings support the hypothesis that the species are reproductively isolated. Significant patterns of genetic isolation by distance were identified in both species, indicating that mating may occur before any long-distance autumnal migration. The presence of a sea channel does not confer higher levels of genetic differentiation among colonies over and above distance alone in either species. Differences in genetic population structure were identified between the species, with P. pipistrellus showing a wider range of levels of genetic differentiation among colonies and a stronger relationship between genetic and geographical distance than P. pygmaeus . Differences in dispersal, mating behaviour, colony size and/or postglacial colonization patterns could contribute to the differences observed.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 539–550.     

Tracking the migratory success of stocked European eels Anguilla anguilla in the Baltic Sea

To investigate the extent to which European silver eels Anguilla anguilla, originating from stocking programmes in the Baltic Sea tributaries, effectively contribute to the spawning stock, two hundred and seventy‐four formerly stocked A. anguilla. emigrating from the Schwentine River near Kiel, Germany, were tagged with T‐Bar anchor tags. A total of 29 Anguilla spp. were recaptured (c. 11%) up to 14 months after release. Stocking history of recaptured A. anguilla. was confirmed by otolith microchemistry. Recapture locations were concentrated around the outlet of the Baltic Sea (Danish Belt Sea) with 62% of all recaptures reported here or in the Kattegat. Recaptured Anguilla spp. showed a reduction in both L_T and mass (mean ± s.d . = ?1·5 ± 0·9 cm and ?125·3 ± 50·1 g) while average total fat content remained in the order of values previously reported as high enough to provide energy resources to allow successful completion of the spawning migration (mean ± s.d . = 28·4 ± 4·4%). The documented mean rate of travel (0·8 km day^?1), however, indicated a delay in the target‐oriented migration that might be interpreted as a delayed initial migration phase of orientation towards the exit of the Baltic Sea.     

Sex differentiation of the European eel in brackish and freshwater environments: a comparative analysis

Body growth parameters, age and total length at sex differentiation were compared in three European eel Anguilla anguilla populations from Mediterranean sites with different salinity. Whilst body growth was faster in brackish than in freshwater environments, the present analysis shows that body size at sex differentiation might be a physiological invariant.     

Environmental gradients predict the genetic population structure of a coral reef fish in the Red Sea

The relatively recent fields of terrestrial landscape and marine seascape genetics seek to identify the influence of biophysical habitat features on the spatial genetic structure of populations or individuals. Over the last few years, there has been accumulating evidence for the effect of environmental heterogeneity on patterns of gene flow and connectivity in marine systems. Here, we investigate the population genetic patterns of an anemonefish, Amphiprion bicinctus, along the Saudi Arabian coast of the Red Sea. We collected nearly one thousand samples from 19 locations, spanning approximately 1500 km, and genotyped them at 38 microsatellite loci. Patterns of gene flow appeared to follow a stepping‐stone model along the northern and central Red Sea, which was disrupted by a distinct genetic break at a latitude of approximately 19°N. The Red Sea is characterized by pronounced environmental gradients along its axis, roughly separating the northern and central from the southern basin. Using mean chlorophyll‐a concentrations as a proxy for this gradient, we ran tests of isolation by distance (IBD, R² = 0.52) and isolation by environment (IBE, R² = 0.64), as well as combined models using partial Mantel tests and multiple matrix regression with randomization (MMRR). We found that genetic structure across our sampling sites may be best explained by a combined model of IBD and IBE (Mantel: R² = 0.71, MMRR: R² = 0.86). Our results highlight the potential key role of environmental patchiness in shaping patterns of gene flow in species with pelagic larval dispersal. We support growing calls for the integration of biophysical habitat characteristics into future studies of population genetic structure.