European (Anguilla anguilla) and American eel (A. rostrata) represent a remarkable case of interspecific hybridization. They are both panmictic and spawn in partial sympatry in the Sargasso Sea, occasionally producing viable, fertile hybrids, primarily found in Iceland. We studied introgressive hybridization from American into European eel based on whole-genome sequences of 78 individuals, encompassing European, American and 21 putative hybrid eels. Previous studies using few genetic markers could not resolve whether hybridization involved simple unidirectional backcrossing or a more complex hybrid swarm scenario. However, local ancestry inference along individual chromosomes revealed Icelandic hybrids were primarily F1 hybrids or first-generation backcrosses toward European eel, with a few showing more complex backcrossing histories. All European eels outside Iceland contained short chromosomal blocks from American eel, indicating a porous genome. We found no evidence for previously stated hypotheses about geographical gradients of introgression in European eel outside Iceland. Several chromosomal regions showed high divergence between the species, but haplotype blocks introgressed from American eel were identified both within and outside these regions. There was little correspondence between regions of high relative and high absolute divergence (dXY), and they presumably reflect selective sweeps within species or regions of reduced recombination rather than barrier loci. We identified a single genomic region with evidence of introgression from American into European eel at multiple occasions, under positive selection in both species. Thus, although the two species maintain genetic integrity, their gene pools are not independent and represent a common pool of standing variation for future adaptive responses.

Anthropogenic biological invasions represent major concerns but enable us to investigate rapid evolutionary changes and adaptation to novel environments. The goldfish Carassius auratus with sexual diploids and asexual triploids coexisting in natural waters, is one of the most widespread invasive fishes in Tibet, providing an ideal model to study evolutionary processes during invasion in different reproductive forms from the same vertebrate. Here, using whole-genome resequencing data of 151 C. auratus individuals from invasive and native ranges, we found different patterns of genomic responses between diploid and triploid populations during their invasion to Tibet. For diploids, although invasive individuals derived from two different genetically distinct sources and had a relative higher diversity (π) at the population level, their individual genetic diversity (genome-wide observed heterozygosity) was significantly lower (21.4%) than that of source individuals. Population structure analysis revealed that the invasive individuals formed a specific genetic cluster distinct from the source populations. Runs of homozygosity analysis showed low inbreeding only in invasive individuals, and only the invasive population experienced a recent decline in effective population size reflecting founder events. For triploids, however, invasive populations showed no loss of individual genetic diversity and no genetic differentiation relative to source populations. Regions of putative selective sweeps between invasive and source populations of diploids mainly involved genes associated with mannosidase activity and embryo development. Our results suggest invasive diploids deriving from distinct sources still lost individual genetic diversity resulting from recent inbreeding and founder events and selective sweeps, and invasive triploids experienced no genetic change owing to their reproduction mode of gynogenesis that precludes inbreeding and founder effects and may make them more powerful invaders.

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, likely reflecting both ageing and developmental processes. Demethylation of transposable elements 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 suggests 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.