Laura Meyer

The formation of ecotypes is driven by evolutionary mechanisms that reduce gene flow through complex interactions among ecological, historical and genomic factors. In the European anchovy ( Engraulis encrasicolus ), marine and coastal ecotypes have been identified in the northeast Atlantic and the Mediterranean Sea, yet the genomic basis of their divergence remains unclear. Here, we present the first genome-scale analysis of this species complex, integrating whole-genome sequencing (WGS) and RAD-seq data from populations spanning its distribution range. In addition to the known marine and coastal ecotypes, we identify a previously undetected lineage extending from southern Morocco, through the Canary Islands, to South Africa. This southern Atlantic lineage exhibits a gradient of admixture with northern populations near the Atlantic–Mediterranean transition zone. Genomic differentiation landscapes reveal large regions of high linkage disequilibrium, probably corresponding to 13 structural variants (SVs) segregating within or between lineages. Notably, three of the six SVs contributing to the gene flow barrier between northern ecotypes originated in the southern lineage, supporting a partially shared evolutionary history between the coastal ecotype and the southern lineage. This study highlights how SVs that arose in geographically isolated lineages can act as key genetic elements in ecotype formation, reinforcing reproductive isolation through distinct evolutionary pathways.

The formation of ecotypes is shaped by mechanisms that reduce gene flow through complex interactions between ecological, historical, and genomic factors. In the European anchovy ( Engraulis encrasicolus ), marine and coastal ecotypes have been identified in the North-East Atlantic and Mediterranean Sea, yet the genomic basis of their divergence remains unclear. Here, we present the first genome-scale analysis of this species complex, integrating whole-genome sequencing (WGS) and RAD-seq data from populations across its distribution range. In addition to the marine and coastal ecotypes, we identify a previously undetected lineage which is present in southern Morocco, the Canary Islands and even in South Africa. This southern Atlantic lineage exhibits a gradient of admixture with northern populations near the Atlantic-Mediterranean transition zone. Genomic differentiation landscapes reveal large regions of high linkage disequilibrium, likely corresponding to thirteen structural variants (SVs) segregating within or between the lineages. Notably, three of the six SVs contributing to the gene flow barrier between northern ecotypes originated in the southern lineage, supporting a partially shared evolutionary history between the coastal ecotype and the southern lineage. Our findings suggest that anchovy ecotype divergence has been shaped by a combination of ancient structural variation, admixture, and local adaptation. This study highlights how SVs that arose between geographically isolated lineages can act as key genetic elements in ecotype formation, reinforcing reproductive isolation through distinct evolutionary pathways.

Chromosomal inversions can play an important role in divergence and reproductive isolation by building and maintaining distinct allelic combinations between evolutionary lineages. Alternatively, they can take the form of balanced polymorphisms that segregate within populations until one arrangement becomes fixed. Many questions remain about how inversion polymorphisms arise, how they are maintained over the long term, and ultimately, whether and how they contribute to speciation. The long‐snouted seahorse (Hippocampus guttulatus) is genetically subdivided into geographic lineages and marine‐lagoon ecotypes, with shared structural variation underlying lineage and ecotype divergence. Here, we aim to characterize structural variants and to reconstruct their history and suspected role in ecotype formation. We generated a near chromosome‐level genome assembly and described genome‐wide patterns of diversity and divergence through the analysis of 112 whole‐genome sequences from Atlantic, Mediterranean, and Black Sea populations. By also analysing linked‐read sequencing data, we found evidence for two chromosomal inversions that were several megabases in length and showed contrasting allele frequency patterns between lineages and ecotypes across the species range. We reveal that these inversions represent ancient intraspecific polymorphisms, one likely being maintained by divergent selection and the other by pseudo‐overdominance. A possible selective coupling between the two inversions was further supported by the absence of specific haplotype combinations and a putative functional interaction between the two inversions in reproduction. Lastly, we detected gene flux eroding divergence between inverted alleles at varying levels for the two inversions, with a likely impact on their dynamics and contribution to divergence and speciation.

Chromosomal inversions can play an important role in divergence and reproductive isolation by building and maintaining distinct allelic combinations between evolutionary lineages. Alternatively, they can take the form of balanced polymorphisms that segregate within populations over time until one arrangement becomes fixed. Many questions remain about how these different inversion polymorphisms arise, how the mechanisms responsible for their long-term maintenance interact, and ultimately how they contribute to speciation. The long-snouted seahorse ( Hippocampus guttulatus ) is known to be subdivided into partially isolated lineages and marine-lagoon ecotypes differentiated by structural variation. Here, we aim to characterise these differences along the entire genome, and to reconstruct their history and role in ecotype formation. We generated a near chromosome-level reference genome assembly and described genome-wide patterns of diversity and divergence through the analysis of 112 whole-genome sequences from Atlantic, Mediterranean, and Black Sea populations. Combined with linked-read sequencing data, we found evidence for two megabase-scale chromosomal inversions showing contrasted allele frequency patterns across the species range. We reveal that these inversions represent ancient intraspecific polymorphisms, one being likely maintained by divergent selection, and the other by associative overdominance. Haplotype combinations characterising Mediterranean ecotypes also suggest the existence of potential interactions between the two inversions, possibly driven by environment-dependent fitness effects. Lastly, we detected gene flux eroding divergence between inverted alleles at varying levels between the two inversions, with a likely impact on their long-term dynamics.

Reports of morphological differences between European anchovy (Engraulis cf. encrasicolus) from coastal and marine habitats have long existed in the ichthyologic literature, and have given rise to a long-standing debate on their taxonomic status. More recently, molecular studies have confirmed the existence of genetic differentiation between the two anchovy ecotypes. Using ancestry-informative markers, we show that coastal anchovies throughout the Mediterranean share a common ancestry, and that substantial genetic differentiation persists in different pairs of coastal/marine populations despite the presence of limited gene flow. On the basis of genetic and ecological arguments, we propose that coastal anchovies deserve a species status of their own (E. maeoticus) and argue that a unified taxonomical framework is critical for future research and management.