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

Abstract

Understanding how new species arise through the progressive establishment of reproductive isolation (RI) barriers between diverging populations is a major goal in Evolutionary Biology. An important result of speciation genomics studies is that genomic regions involved in RI frequently harbor anciently diverged haplotypes that predate the reconstructed history of species divergence. The possible origins of these old alleles remain much debated, as they relate to contrasting mechanisms of speciation that are not yet fully understood. In the European sea bass (Dicentrarchus labrax), the genomic regions involved in RI 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 RI 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 contributed to the establishment of RI between the two D. labrax lineages.

Keywords: Ancient admixture; genomic conflicts; introgression; marine fish; reproductive isolation.

Figure 1

Phylogenetic relationships among D. labrax lineages, D. punctatus, and the outgroup species M. saxatilis. (A) Three different topologies rooted by M. saxatilis, representing the species tree (orange) and two discordant topologies grouping D. punctatus with the Atlantic (green) or the Mediterranean (blue) D. labrax lineage. (B) Proportion of each topology in nonoverlapping 50‐Kb windows along the genome. (C) Genome‐wide average pairwise sequence divergence between species/lineages measured by d _xy using one individual per lineage.

Figure 2

Divergence and introgression statistics measured in nonoverlapping 50‐kb windows along chromosome 20. (A) d _XY measured between the Atlantic and Mediterranean (including eastern and western population) D. labrax lineages. (B) f _D statistics measured using (((MED, AT), PUN), SAX) in red, (((AT, WEM), PUN), SAX) in green, and (((ATL, EMED), PUN), SAX) in blue. (C) Fraction of archaic introgressed tracts (F _archaic) inferred in the eastern Mediterranean (orange) and Atlantic (red) populations of D. labrax. (D) RND_min measured between D. punctatus and D. labrax Atlantic (red), western (green), and eastern (blue) Mediterranean populations. (E) Proportions of genealogies grouping D. punctatus with the Atlantic (green) or the Mediterranean (blue) D. labrax lineage in the Twisst analysis. (F) F _ST between the Atlantic and western Mediterranean population of D. labrax divided by the fraction of Atlantic tracts introgressed into the western Mediterranean genomes for each SNP along the chromosome. Purple points show SNPs with significant associations to reproductive isolation after applying FDR correction to the probabilities determined with the HMM approach. Gray rectangles represent genomic regions identified as involved in reproductive isolation with our window‐based HMM approach.

Figure 3

Estimation of the time since admixture between D. punctatus and Atlantic D. labrax. (A) Length distributions of D. punctatus tracts introgressed into Atlantic D. labrax genomes (blue) and Atlantic D. labrax tracts introgressed into western Mediterranean D. labrax genomes (orange). Both distributions were generated using similar sequence lengths (totalizing 65.6 Mb) along the genomes of 14 Atlantic and 14 Mediterranean individuals, so that tract abundances can be compared. (B). Distribution of estimated time since admixture between D. punctatus and D. labrax (T _admix) obtained from estimated transition parameter values of the HMM model over the 24 chromosomes. The maximum of the distribution is represented by the vertical red dashed line and the blue shape represents the 95% credibility envelope of the distribution obtained using 10,000 bootstrap resampling.

Figure 4

One‐ and two‐dimensional Site Frequency Spectra of D. punctatus‐derived alleles segregating in D. labrax. (A) Conditional Site Frequency Spectra (CSFS) of D. punctatus‐derived alleles in AT (red) and MED (black) D. labrax lineages for categories of SNPs that are either not associated or (B) associated to RI islands identified between the two D. labrax lineages. (C) Conditional Joint Site Frequency Spectra (CJSFS) of derived D. punctatus alleles between MED (54 individuals) and AT (14 individuals) lineages based on 618,842 SNPs not involved in RI, and (D) 7372 SNPs involved in RI.