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Abstract
Speciation is a complex process that leads to the progressive establishment of reproductive isolation barriers between diverging populations. Genome-wide comparisons between closely related species have revealed the existence of heterogeneous divergence patterns, dominated by genomic islands of increased divergence supposed to contain reproductive isolation loci. However, this divergence landscape only provides a static picture of the dynamic process of speciation, during which confounding mechanisms unrelated to speciation can interfere. Here we use haplotype-resolved whole-genome sequences to identify the mechanisms responsible for the formation of genomic islands between Atlantic and Mediterranean sea bass lineages. Local ancestry patterns show that genomic islands first emerged in allopatry through linked selection acting on a heterogeneous recombination landscape. Then, upon secondary contact, preexisting islands were strongly remolded by differential introgression, revealing variable fitness effects among regions involved in reproductive isolation. Interestingly, we find that divergent regions containing ancient polymorphisms conferred the strongest resistance to introgression.
Highlights
The identification of genomic regions that are truly resistant to introgression remains a challenging task, especially because the aforementioned mechanisms are influenced by the recombination landscape and tend to affect similar regions of the genome[27,28,29]
Our results show that genomic regions experiencing stronger linked selection due to low recombination diverge faster during allopatric episodes and better resist introgression in the presence of gene flow
The genetic relationships of the newly sequenced genomes with respect to the range-wide population structure of the European sea bass were evaluated with a Principal Component (PC) Analysis including 112 additional individuals genotyped at 13,094 common single nucleotide polymorphisms (SNPs; Fig. 1a, b and Supplementary Note 2)
Summary
The identification of genomic regions that are truly resistant to introgression remains a challenging task, especially because the aforementioned mechanisms are influenced by the recombination landscape and tend to affect similar regions of the genome[27,28,29]. Historical demographic inferences revealed that the two lineages have started to diverge in allopatry around 300,000 years before present (BP) and experienced a post-glacial secondary contact generating varying rates of introgression across the genome[31] This evolutionary history mirrors the distributional range shifts that occurred across many taxa during glacial periods especially in the Atlantic–Mediterranean region[33], which are recognized as an important source of species diversification[34,35]. Our results show that genomic regions experiencing stronger linked selection due to low recombination diverge faster during allopatric episodes and better resist introgression in the presence of gene flow These findings support that multiple loci affect RI in sea bass, with the most divergent having the strongest effects
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