Hybridization and adaptive introgression in a marine invasive species in native habitats.

Hybridization of distinct populations or species is an important evolutionary driving force. For invasive species, hybridization can enhance their competitive advantage as a source of adaptive novelty by introgression of selectively favored alleles. Using single-nucleotide polymorphism (SNP) microarrays we assess genetic diversity and population structure in the invasive ctenophore Mnemiopsis leidyi in native habitats. Hybrids are present at the distribution border of two lineages, especially in highly fluctuating environments including very low salinities, while hybrids occur at lower frequency in stable high-saline habitats. Analyses of hybridization status suggest that hybrids thriving in variable environments are selected for, while they are selected against in stable habitats. Translocation of hybrids might accelerate invasion success in non-native habitats. This could be especially relevant for M. leidyi as low salinity limits its invasion range in western Eurasia. Although hybridization status is currently disregarded, it could determine high-risk areas where ballast water exchange should be prevented.

The formation of the Indo-Pacific montane avifauna.

The processes generating the earth's montane biodiversity remain a matter of debate. Two contrasting hypotheses have been advanced to explain how montane populations form: via direct colonization from other mountains, or, alternatively, via upslope range shifts from adjacent lowland areas. We seek to reconcile these apparently conflicting hypotheses by asking whether a species' ancestral geographic origin determines its mode of mountain colonization. Island-dwelling passerine birds at the faunal crossroads between Eurasia and Australo-Papua provide an ideal study system. We recover the phylogenetic relationships of the region's montane species and reconstruct their ancestral geographic ranges, elevational ranges, and migratory behavior. We also perform genomic population studies of three super-dispersive montane species/clades with broad island distributions. Eurasian-origin species populated archipelagos via direct colonization between mountains. This mode of colonization appears related to ancestral adaptations to cold and seasonal climates, specifically short-distance migration. Australo-Papuan-origin mountain populations, by contrast, evolved from lowland ancestors, and highland distribution mostly precludes their further colonization of island mountains. Our study explains much of the distributional variation within a complex biological system, and provides a synthesis of two seemingly discordant hypotheses for montane community formation.

Population genomics of the island thrush elucidates one of earth's great archipelagic radiations.

Tropical islands are renowned as natural laboratories for evolutionary study. Lineage radiations across tropical archipelagos are ideal systems for investigating how colonization, speciation, and extinction processes shape biodiversity patterns. The expansion of the island thrush across the Indo-Pacific represents one of the largest yet most perplexing island radiations of any songbird species. The island thrush exhibits a complex mosaic of pronounced plumage variation across its range and is arguably the world's most polytypic bird. It is a sedentary species largely restricted to mountain forests, yet it has colonized a vast island region spanning a quarter of the globe. We conducted a comprehensive sampling of island thrush populations and obtained genome-wide SNP data, which we used to reconstruct its phylogeny, population structure, gene flow, and demographic history. The island thrush evolved from migratory Palearctic ancestors and radiated explosively across the Indo-Pacific during the Pleistocene, with numerous instances of gene flow between populations. Its bewildering plumage variation masks a biogeographically intuitive stepping stone colonization path from the Philippines through the Greater Sundas, Wallacea, and New Guinea to Polynesia. The island thrush's success in colonizing Indo-Pacific mountains can be understood in light of its ancestral mobility and adaptation to cool climates; however, shifts in elevational range, degree of plumage variation and apparent dispersal rates in the eastern part of its range raise further intriguing questions about its biology.

Gelatinous macrozooplankton diversity and distribution dataset for the North Sea and Skagerrak/Kattegat during January-February 2021.

This data article includes a qualitative and quantitative description of the gelatinous macrozooplankton community of the North Sea during January-February 2021. Sampling was conducted during the 1st quarter International Bottom Trawl Survey (IBTS) on board the Danish R/V DANA (DTU Aqua Denmark) and the Swedish R/V Svea (SLU Sweden), as part of the ichthyoplankton investigation during night-time. A total of 147 stations were investigated in the western, central and eastern North Sea as well as the Skagerrak and Kattegat. Sampling was conducted with a 13 m long Midwater Ring Net (MIK net, Ø 2 m, mesh size 1.6 mm, cod end with smaller mesh size of 500 µm), equipped with a flow meter. The MIK net was deployed in double oblique hauls from the surface to c. 5 m above the sea floor [1,2]. Samples were visually analysed unpreserved on a light table and/or with a stereomicroscope or magnifying lamp within 2 hours after catch. A total of 13,510 individuals were counted/sized. Twelve gelatinous macrozooplankton species or genera were encountered, namely the hydrozoan Aequorea vitrina, Aglantha digitale, Clytia spp., Leuckartiara octona, Tima bairdii, Muggiaea atlantica; the scyphozoans Cyanea capillata and Cyanea lamarckii and the ctenophores Beroe spp., Bolinopsis infundibulum, Mnemiopsis leidyi, Pleurobrachia pileus. Abundance data are presented on a volume specific (m-3) and area specific (m-2) basis. Size data have been used to estimate wet weights based on published length-weight regressions (see Table 1). For the groups i) hydrozoan jellyfish, ii) scyphozoan jellyfish, iii) ctenophores, as well as iv) grouped gelatinous macrozooplankton, spatial weight specific distribution patterns are presented. This unpublished dataset contributes baseline information about the gelatinous macrozooplankton diversity and its specific distribution patterns in the extended North Sea area during winter (January-February) 2021. These data can be an important contribution to address global change impacts on marine systems, especially considering gelatinous macrozooplankton abundance changes in relation to anthropogenic stressors.

Genome-wide methylation in the panmictic European eel (Anguilla anguilla).

The role of methylation in adaptive, developmental and speciation processes has attracted considerable interest, but interpretation of results is complicated by diffuse boundaries between genetic and non-genetic variation. We studied whole genome genetic and methylation variation in the European eel, distributed from subarctic to subtropical environments, but with panmixia precluding genetically based local adaptation beyond single-generation responses. Overall methylation was 70.9%, with hypomethylation predominantly found in promoters and first exons. Redundancy analyses involving juvenile glass eels showed 0.06% and 0.03% of the variance at SNPs to be explained by localities and environmental variables, respectively, with GO terms of genes associated with outliers primarily involving neural system functioning. For CpGs 2.98% and 1.36% of variance was explained by localities and environmental variables. Differentially methylated regions particularly included genes involved in developmental processes, with Hox clusters featuring prominently. Life stage (adult versus glass eels) was the most important source of inter-individual variation in methylation, probably reflecting both ageing and developmental processes. Demethylation of transposable elements relative to pure European eel was observed in European X American eel hybrids, possibly representing postzygotic barriers in this system characterized by prolonged speciation and ongoing gene flow. Whereas the genetic data are consistent with a role of single-generation selective responses, the methylation results underpin the importance of epigenetics in the life cycle of eels and suggest interactions between local environments, development and phenotypic variation mediated by methylation variation. Eels are remarkable by having retained eight Hox clusters, and the results suggest important roles of methylation at Hox genes for adaptive processes.

Comparative genomics and signatures of selection in North Atlantic eels.

Comparative genomic approaches can identify putative private and shared signatures of selection. We performed a comparative genomic study of North Atlantic eels, European eel (Anguilla Anguilla) and American eel (A. rostrata). The two sister species are nearly undistinguishable at the phenotypic level and despite a wide non-overlapping continental distribution, they spawn in partial sympatry in the Sargasso Sea. Taking advantage of the newly assembled and annotated genome, we used genome wide RAD sequencing data of 359 individuals retrieved from Sequence Nucleotide Archive and state-of-the-art statistic tests to identify putative genomic signatures of selection in North Atlantic eels. First, using the FST and XP-EHH methods, we detected apparent islands of divergence on a total of 7 chromosomes, particularly on chromosomes 6 and 10. Gene ontology analyses suggested candidate genes mainly related to energy production, development and regulation, which could reflect strong selection on traits related to eel migration and larval duration time. Gene effect prediction using SNPeff showed a high number of SNPs in noncoding regions, pointing to a possible regulatory role. Second, using the iHS method we detected shared regions under selection on a total of 11 chromosomes. Several hypotheses might account for the detection of shared islands of selection in North Atlantic eels, including parallel evolution due to adaptation to similar environments and introgression. Future comparative genomic studies will be needed to further clarify the causes and consequences of introgression, including the directionality of these introgression events.

The formation of avian montane diversity across barriers and along elevational gradients.

Tropical mountains harbor exceptional concentrations of Earth's biodiversity. In topographically complex landscapes, montane species typically inhabit multiple mountainous regions, but are absent in intervening lowland environments. Here we report a comparative analysis of genome-wide DNA polymorphism data for population pairs from eighteen Indo-Pacific bird species from the Moluccan islands of Buru and Seram and from across the island of New Guinea. We test how barrier strength and relative elevational distribution predict population differentiation, rates of historical gene flow, and changes in effective population sizes through time. We find population differentiation to be consistently and positively correlated with barrier strength and a species' altitudinal floor. Additionally, we find that Pleistocene climate oscillations have had a dramatic influence on the demographics of all species but were most pronounced in regions of smaller geographic area. Surprisingly, even the most divergent taxon pairs at the highest elevations experience gene flow across barriers, implying that dispersal between montane regions is important for the formation of montane assemblages.

Invasion genomics uncover contrasting scenarios of genetic diversity in a widespread marine invader.

Invasion rates have increased in the past 100 y irrespective of international conventions. What characterizes a successful invasion event? And how does genetic diversity translate into invasion success? Employing a whole-genome perspective using one of the most successful marine invasive species world-wide as a model, we resolve temporal invasion dynamics during independent invasion events in Eurasia. We reveal complex regionally independent invasion histories including cases of recurrent translocations, time-limited translocations, and stepping-stone range expansions with severe bottlenecks within the same species. Irrespective of these different invasion dynamics, which lead to contrasting patterns of genetic diversity, all nonindigenous populations are similarly successful. This illustrates that genetic diversity, per se, is not necessarily the driving force behind invasion success. Other factors such as propagule pressure and repeated introductions are an important contribution to facilitate successful invasions. This calls into question the dominant paradigm of the genetic paradox of invasions, i.e., the successful establishment of nonindigenous populations with low levels of genetic diversity.

Transcriptomic profiling of male European eel (Anguilla anguilla) livers at sexual maturity.

The European eel Anguilla anguilla has a complex life cycle that includes freshwater, seawater and morphologically distinct stages as well as two extreme long distance migrations. Eels do not feed as they migrate across the Atlantic to the Sargasso Sea but nevertheless reach sexual maturity before spawning. It is not yet clear how existing energy stores are used to reach the appropriate developmental state for reproduction. Since the liver is involved in energy metabolism, protein biosynthesis and endocrine regulation it is expected to play a key role in the regulation of reproductive development. We therefore used microarrays to identify genes that may be involved in this process. Using this approach, we identified 231 genes that were expressed at higher and 111 genes that were expressed at lower levels in sexually mature compared with immature males. The up-regulated set includes genes involved in lipid metabolism, fatty acid synthesis and transport, mitochondrial function, steroid transport and bile acid metabolism. Several genes with putative enzyme functions were also expressed at higher levels at sexual maturity while genes involved in immune system processes and protein biosynthesis tended to be down-regulated at this stage. By using a high-throughput approach, we have identified a subset of genes that may be linked with the mobilization of energy stores for sexual maturation and migration. These results contribute to an improved understanding of eel reproductive biology and provide insight into the role of the liver in other teleosts with a long distance spawning migrations.

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

Mitochondrial genes are part of the oxidative phosphorylation pathway and important for energy production. Although evidence for positive selection at the mitochondrial level exists, few studies have investigated the link between amino acid changes and phenotype. Here we test the hypothesis that differences in two life-history related traits, migratory distance between spawning and foraging areas and larval phase duration, are associated with divergent selection within the mitochondrial ATP6 gene in anguillid eels. We compare amino acid changes among 18 species with the sequence of the putative ancestral species, believed to have shown short migratory distance and larval phase duration. We find positive correlations between both life-history related traits and (i) the number of amino acid changes and (ii) the strength of the combined physico-chemical and structural changes at positions previously identified as candidates for positive selection. This supports a link between genotype and phenotype driven by positive selection at ATP6.

Genomic resources notes accepted 1 October 2014-30 November 2014.

This article documents the public availability of (i) RAD sequencing data and validated SNPs for the American mink Neovison vison and (ii) Transcriptome resources for two nonmodel freshwater crustacean species, the copepod Eucyclops serrulatus and the amphipod Echinogammarus veneris.

Population genomics of marine fishes: next-generation prospects and challenges.

Over the past few years, technological advances have facilitated giant leaps forward in our ability to generate genome-wide molecular data, offering exciting opportunities for gaining new insights into the ecology and evolution of species where genomic information is still limited. Marine fishes are valuable organisms for advancing our understanding of evolution on historical and contemporary time scales, and here we highlight areas in which research on these species is likely to be particularly important in the near future. These include possibilities for gaining insights into processes on ecological time scales, identifying genomic signatures associated with population divergence under gene flow, and determining the genetic basis of phenotypic traits. We also consider future challenges pertaining to the implementation of genome-wide coverage through next-generation sequencing and genotyping methods in marine fishes. Complications associated with fast decay of linkage disequilibrium, as expected for species with large effective population sizes, and the possibility that adaptation is associated with both soft selective sweeps and polygenic selection, leaving complex genomic signatures in natural populations, are likely to challenge future studies. However, the combination of high genome coverage and new statistical developments offers promising solutions. Thus, the next generation of studies is likely to truly facilitate the transition from population genetics to population genomics in marine fishes. This transition will advance our understanding of basic evolutionary processes and will offer new possibilities for conservation and management of valuable marine resources.

Captive breeding programs based on family groups in polyploid sturgeons.

In species with long life cycles and discontinuous availability of individuals to reproduction, implementing a long-term captive breeding program can be difficult or impossible. In such cases, managing diversity among familiar groups instead of individuals could become a suitable approach to avoid inbreeding and increase the possibility to accomplish a breeding scheme. This is the case of several sturgeon species including the Adriatic sturgeon, whose recovery depends on the management of a few captive stocks directly descended from the same group of wild parents. In the present study, relatedness among 445 potential breeders was inferred with a novel software for pedigree reconstruction in tetraploids ("BreedingSturgeons"). This information was used to plan a breeding scheme considering familiar groups as breeding units and identifying mating priorities. A two-step strategy is proposed: a short-term breeding program, relying on the 13 remaining F0 individuals of certain wild origin; and a long-term plan based on F1 families. Simulations to evaluate the loss of alleles in the F2 generation under different pairing strategies and assess the number of individuals to breed, costs and logistical aquaculture constraints were performed. The strategy proposed is transferable to the several other tetraploid sturgeon species on the brink of extinction.

Changes in the gene expression profiles of the brains of male European eels (Anguilla anguilla) during sexual maturation.

BACKGROUND: The vertebrate brain plays a critical role in the regulation of sexual maturation and reproduction by integrating environmental information with developmental and endocrine status. The European eel Anguilla anguilla is an important species in which to better understand the neuroendocrine factors that control reproduction because it is an endangered species, has a complex life cycle that includes two extreme long distance migrations with both freshwater and seawater stages and because it occupies a key position within the teleost phylogeny. At present, mature eels have never been caught in the wild and little is known about most aspects of reproduction in A. anguilla. The goal of this study was to identify genes that may be involved in sexual maturation in experimentally matured eels. For this, we used microarrays to compare the gene expression profiles of sexually mature to immature males. RESULTS: Using a false discovery rate of 0.05, a total of 1,497 differentially expressed genes were identified. Of this set, 991 were expressed at higher levels in brains (forebrain and midbrain) of mature males while 506 were expressed at lower levels relative to brains of immature males. The set of up-regulated genes includes genes involved in neuroendocrine processes, cell-cell signaling, neurogenesis and development. Interestingly, while genes involved in immune system function were down-regulated in the brains of mature males, changes in the expression levels of several receptors and channels were observed suggesting that some rewiring is occurring in the brain at sexual maturity. CONCLUSIONS: This study shows that the brains of eels undergo major changes at the molecular level at sexual maturity that may include re-organization at the cellular level. Here, we have defined a set of genes that help to understand the molecular mechanisms controlling reproduction in eels. Some of these genes have previously described functions while many others have roles that have yet to be characterized in a reproductive context. Since most of the genes examined here have orthologs in other vertebrates, the results of this study will contribute to the body of knowledge concerning reproduction in vertebrates as well as to an improved understanding of eel biology.

Genomic footprints of speciation in Atlantic eels (Anguilla anguilla and A. rostrata).

The importance of speciation-with-geneflow scenarios is increasingly appreciated. However, the specific processes and the resulting genomic footprints of selection are subject to much discussion. We studied the genomics of speciation between the two panmictic, sympatrically spawning sister species; European (Anguilla anguilla) and American eel (A. rostrata). Divergence is assumed to have initiated more than 3 Ma, and although low gene flow still occurs, strong postzygotic barriers are present. Restriction-site-associated DNA (RAD) sequencing identified 328 300 SNPs for subsequent analysis. However, despite the presence of 3757 strongly differentiated SNPs (FST > 0.8), sliding window analyses of FST showed no larger genomic regions (i.e. hundreds of thousands to millions of bases) of elevated differentiation. Overall FST was 0.041, and linkage disequilibrium was virtually absent for SNPs separated by more than 1000 bp. We suggest this to reflect a case of genomic hitchhiking, where multiple regions are under directional selection between the species. However, low but biologically significant gene flow and high effective population sizes leading to very low genetic drift preclude accumulation of strong background differentiation. Genes containing candidate SNPs for positive selection showed significant enrichment for gene ontology (GO) terms relating to developmental processes and phosphorylation, which seems consistent with assumptions that differences in larval phase duration and migratory distances underlie speciation. Most SNPs under putative selection were found outside coding regions, lending support to emerging views that noncoding regions may be more functionally important than previously assumed. In total, the results demonstrate the necessity of interpreting genomic footprints of selection in the context of demographic parameters and life-history features of the studied species.

Do North Atlantic eels show parallel patterns of spatially varying selection?

BACKGROUND: The two North Atlantic eel species, the European and the American eel, represent an ideal system in which to study parallel selection patterns due to their sister species status and the presence of ongoing gene flow. A panel of 80 coding-gene SNPs previously analyzed in American eel was used to genotype European eel individuals (glass eels) from 8 sampling locations across the species distribution. We tested for single-generation signatures of spatially varying selection in European eel by searching for elevated genetic differentiation using FST-based outlier tests and by testing for significant associations between allele frequencies and environmental variables. RESULTS: We found signatures of possible selection at a total of 11 coding-gene SNPs. Candidate genes for local selection constituted mainly genes with a major role in metabolism as well as defense genes. Contrary to what has been found for American eel, only 2 SNPs in our study correlated with differences in temperature, which suggests that other explanatory variables may play a role. None of the genes found to be associated with explanatory variables in European eel showed any correlations with environmental factors in the previous study in American eel. CONCLUSIONS: The different signatures of selection between species could be due to distinct selective pressures associated with the much longer larval migration for European eel relative to American eel. The lack of parallel selection in North Atlantic eels could also be due to most phenotypic traits being polygenic, thus reducing the likelihood of selection acting on the same genes in both species.

The effects of Medieval dams on genetic divergence and demographic history in brown trout populations.

BACKGROUND: Habitat fragmentation has accelerated within the last century, but may have been ongoing over longer time scales. We analyzed the timing and genetic consequences of fragmentation in two isolated lake-dwelling brown trout populations. They are from the same river system (the Gudenå River, Denmark) and have been isolated from downstream anadromous trout by dams established ca. 600-800 years ago. For reference, we included ten other anadromous populations and two hatchery strains. Based on analysis of 44 microsatellite loci we investigated if the lake populations have been naturally genetically differentiated from anadromous trout for thousands of years, or have diverged recently due to the establishment of dams. RESULTS: Divergence time estimates were based on 1) Approximate Bayesian Computation and 2) a coalescent-based isolation-with-gene-flow model. Both methods suggested divergence times ca. 600-800 years bp, providing strong evidence for establishment of dams in the Medieval as the factor causing divergence. Bayesian cluster analysis showed influence of stocked trout in several reference populations, but not in the focal lake and anadromous populations. Estimates of effective population size using a linkage disequilibrium method ranged from 244 to > 1,000 in all but one anadromous population, but were lower (153 and 252) in the lake populations. CONCLUSIONS: We show that genetic divergence of lake-dwelling trout in two Danish lakes reflects establishment of water mills and impassable dams ca. 600-800 years ago rather than a natural genetic population structure. Although effective population sizes of the two lake populations are not critically low they may ultimately limit response to selection and thereby future adaptation. Our results demonstrate that populations may have been affected by anthropogenic disturbance over longer time scales than normally assumed.

Tana1, a new putatively active Tc1-like transposable element in the genome of sturgeons.

We report the discovery of a new putatively active Tc1-like transposable element (Tana1) in the genome of sturgeons, an ancient group of fish considered as living fossils. The complete sequence of Tana1 was first characterized in the 454-sequenced transcriptome of the Adriatic sturgeon (Acipenser naccarii) and then isolated from the genome of the same species and from 12 additional sturgeons including three genera of the Acipenseridae (Acipenser, Huso, Scaphirhynchus). The element has a total length of 1588bp and presents inverted repeats of 210bp, one of which partially overlapping the 3' region of the transposase gene. The spacing of the DDE motif within the catalytic domain in Tana1 is unique (DD38E) and indicates that Tana1 can be considered as the first representative of a new Tc1 subfamily. The integrity of the native form (with no premature termination codons within the transposase), the presence of all expected functional domains and its occurrence in the sturgeon transcriptome suggest a current or recent activity of Tana1. The presence of Tana1 in the genome of the 13 sturgeon species in our study points to an ancient origin of the element that existed before the split of the group 170 million years ago. The dissemination of Tana1 across sturgeon genomes could be interpreted by postulating vertical transmission from an ancestral Tana1 with a particularly slow evolutionary rate Horizontal transmission might have also played a role in the dissemination of Tana1 as evidenced by the presence of a complete copy in the genome of Atlantic salmon. Vertical and horizontal transmission are not mutually exclusive and may have concurred in shaping the evolution of Tana1.

Body size correlates with fertilization success but not gonad size in grass goby territorial males.

In fish species with alternative male mating tactics, sperm competition typically occurs when small males that are unsuccessful in direct contests steal fertilization opportunities from large dominant males. In the grass goby Zosterisessor ophiocephalus, large territorial males defend and court females from nest sites, while small sneaker males obtain matings by sneaking into nests. Parentage assignment of 688 eggs from 8 different nests sampled in the 2003-2004 breeding season revealed a high level of sperm competition. Fertilization success of territorial males was very high but in all nests sneakers also contributed to the progeny. In territorial males, fertilization success correlated positively with male body size. Gonadal investment was explored in a sample of 126 grass gobies collected during the period 1995-1996 in the same area (61 territorial males and 65 sneakers). Correlation between body weight and testis weight was positive and significant for sneaker males, while correlation was virtually equal to zero in territorial males. That body size in territorial males is correlated with fertilization success but not gonad size suggests that males allocate much more energy into growth and relatively little into sperm production once the needed size to become territorial is attained. The increased paternity of larger territorial males might be due to a more effective defense of the nest in comparison with smaller territorial males.

Surviving in a toxic world: transcriptomics and gene expression profiling in response to environmental pollution in the critically endangered European eel.

BACKGROUND: Genomic and transcriptomic approaches have the potential for unveiling the genome-wide response to environmental perturbations. The abundance of the catadromous European eel (Anguilla anguilla) stock has been declining since the 1980s probably due to a combination of anthropogenic and climatic factors. In this paper, we explore the transcriptomic dynamics between individuals from high (river Tiber, Italy) and low pollution (lake Bolsena, Italy) environments, which were measured for 36 PCBs, several organochlorine pesticides and brominated flame retardants and nine metals. RESULTS: To this end, we first (i) updated the European eel transcriptome using deep sequencing data with a total of 640,040 reads assembled into 44,896 contigs (Eeelbase release 2.0), and (ii) developed a transcriptomic platform for global gene expression profiling in the critically endangered European eel of about 15,000 annotated contigs, which was applied to detect differentially expressed genes between polluted sites. Several detoxification genes related to metabolism of pollutants were upregulated in the highly polluted site, including genes that take part in phase I of the xenobiotic metabolism (CYP3A), phase II (glutathione-S-transferase) and oxidative stress (glutathione peroxidase). In addition, key genes in the mitochondrial respiratory chain and oxidative phosphorylation were down-regulated at the Tiber site relative to the Bolsena site. CONCLUSIONS: Together with the induced high expression of detoxification genes, the suggested lowered expression of genes supposedly involved in metabolism suggests that pollution may also be associated with decreased respiratory and energy production.