Duranton, M. | bioRxiv Science

bioRxiv2021

Interactions between natural selection and recombination shape the genomic landscape of introgression

Hybridization between lineages that have not reached complete reproductive isolation appears more and more like a common phenomenon. Indeed, speciation genomics studies have now extensively shown that many species genomes have hybrid ancestry. However, genomic patterns of introgression are often heterogeneous across the genome. In many organisms, a positive correlation between introgression levels and recombination rate has been observed. It is usually explained by the purging of deleterious introgressed material due to incompatibilities. However, the opposite relationship was observed in a North American population of Drosophila melanogaster with admixed European and African ancestry. In order to explore how directional and epistatic selection can impact the relationship between introgression and recombination, we performed forward simulations of whole D. melanogaster genomes reflecting the North American populations history. Our results revealed that the simplest models of positive selection often yield negative correlations between introgression and recombination such as the one observed in D. melanogaster. We also confirmed that incompatibilities tend to produce positive introgression-recombination correlations. And yet, we identify parameter space under each model where the predicted correlation is reversed. These findings deepen our understanding of the evolutionary forces that may shape patterns of ancestry across genomes, and they strengthen the foundation for future studies aimed at estimating genome-wide parameters of selection in admixed populations.

evolutionary biology↗

bioRxiv2019

The contribution of ancient admixture to reproductive isolation between European sea bass lineages

Understanding how new species arise through the progressive establishment of reproductive isolation barriers between diverging populations is a major goal in Evolutionary Biology. One important result of speciation genomics studies is that the genomic regions involved in reproductive isolation frequently harbor anciently diverged haplotypes that predate the reconstructed history of species divergence. The possible origins of these old alleles remain highly debated, since they relate to contrasted mechanisms of speciation that are not fully understood yet. In the European sea bass (Dicentrarchus labrax), the genomic regions involved in reproductive isolation between Atlantic and Mediterranean lineages are enriched for anciently diverged alleles of unknown origin. Here, we used haplotype-resolved whole-genome sequences to test whether divergent haplotypes could have originated from a closely related species, the spotted sea bass (Dicentrarchus punctatus). We found that an ancient admixture event between D. labrax and D. punctatus is responsible for the presence of shared derived alleles that segregate at low frequencies in both lineages of D. labrax. An exception to this was found within regions involved in reproductive isolation between the two D. labrax lineages. In those regions, archaic tracts originating from D. punctatus locally reached high frequencies or even fixation in Atlantic genomes but were almost absent in the Mediterranean. We showed that the ancient admixture event most likely occurred between D. punctatus and the D. labrax Atlantic lineage, while Atlantic and Mediterranean D. labrax lineages were experiencing allopatric isolation. Our results suggest that local adaptive introgression and/or the resolution of genomic conflicts provoked by ancient admixture have probably participated to the establishment of reproductive isolation between the two D. labrax lineages.\n\nAuthor summarySpeciation is often viewed as a progressive accumulation of reproductive isolation barriers between two diverging lineages through the time. When initiated, the speciation process may however take different routes, sometimes leading to the erosion of an established species barrier or to the acquisition of new speciation genes transferred from another species boundary. Here, we describe such a case in the European sea bass. This marine fish species has split 300,000 years ago into an Atlantic and a Mediterranean lineage, which remained partially reproductively isolated after experiencing postglacial secondary contact. For unknown reasons, genomic regions involved in reproductive isolation between lineages have started to diverge well before the split. We here show that diverged alleles were acquired by the Atlantic lineage from an ancient event of admixture with a parapatric sister species about 80,000 years ago. Introgressed foreign alleles that were locally driven to high frequencies in the Atlantic have subsequently resisted to introgression within the Mediterranean during the postglacial secondary contact, thus contributing to increased reproductive isolation between two sea bass lineages. These results support the view that reproductive isolation barriers can evolve via reticulate gene flow across multiple species boundaries.

evolutionary biology↗

bioRxiv2017

The origin and remolding of genomic islands of differentiation in the European sea bass

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 unlinked to speciation can interfere. Here, we used haplotype-resolved whole-genome sequences to identify the mechanisms responsible for the formation of genomic islands between Atlantic and Mediterranean sea bass lineages. We show that genomic islands first emerged in allopatry through the effect of linked selection acting on a heterogeneous recombination landscape. Upon secondary contact, preexisting islands were strongly remolded by differential introgression, revealing variable fitness effects among regions involved in reproductive isolation. Interestingly, we found that divergent regions containing ancient polymorphisms conferred the strongest resistance to introgression.

evolutionary biology↗