The Fate of a Polygenic Phenotype Within the Genomic Landscapes of Introgression in the European Seabass Hybrid Zone

Abstract

Unraveling the evolutionary mechanisms and consequences of hybridization is a major concern in biology. Many studies have documented the interplay between recombination and selection in modulating the genomic landscape of introgression, but few have considered how associations with phenotype may affect this landscape. Here, we use the European seabass (Dicentrarchus labrax), a key species in marine aquaculture that undergoes natural hybridization, to determine how selection on phenotype modulates the introgression landscape between Atlantic and Mediterranean lineages. We use a high-density single nucleotide polymorphism array to assess individual local ancestry along the genome and improve the mapping of muscle fat content, a polygenic trait that is divergent between lineages. Taking into account variation in recombination rates, we reveal a purging of Atlantic ancestry in the admixed Mediterranean populations. While Atlantic individuals had higher muscle fat content, we observed that genomic regions associated with this trait in Mediterranean populations displayed reduced introgression of Atlantic ancestry. These results emphasize how selection against maladapted alleles shapes the genomic landscape of introgression.

Keywords: European seabass; hybridization; introgression; phenotype; recombination; selection.

Fig. 1.

Violin plot of the muscular fat content residuals for the three populations Atlantic (ATL) and both west and east Mediterranean populations (WEM and EST). Letters represent the significance of Tukey's test (P-adj < 0.01), average with no significant differences are shown with the same letter.

Fig. 2.

Atlantic (ATL) ancestry tracts for both WEM and EST populations. a) Boxplot of the ATL ancestry tracts length in Mbp within each population. b) Boxplot of the number of ATL ancestry within each population. F indicates the significance of the models and DF the degree of freedom followed by the P-value.

Fig. 3.

Mean recombination rate estimates (in cM/Mb) between males and females of the EST line along the 24 chromosomes of the European seabass.

Fig. 4.

a) Whole-genome relationship between local Atlantic ancestry rate and local recombination rate (cM/Mb) for both WEM (green) and EST (orange) populations. The colored plain curve is the mean population response of local Atlantic ancestry rate to local recombination rate predicted by the quasi-binomial mixed logistic regressions with penalized quasi-likelihood (GlmmPQL). The slope coefficient was 0.46 and 0.42 for the WEM (green) and EST (orange) with both significant P-value < 0.001. Dashed-colored curves represent the confidence interval (CI 95%) of the predicted response. b) Slope of the response of local Atlantic ancestry rate to local recombination rate estimated for each of the 24 European seabass chromosomes introduced as random effects in the GlmmPQL for both EST (orange) and WEM (green) populations. Symbols’ shape represents the significance of each separated logistic regression model (GLMs) per chromosome with circles and crosses representing P-values < 0.001 and P > 0.001, respectively.

Fig. 5.

a) Manhattan plot displaying the significance of each “ancestry” variant association with muscle fat content. Each dot represents an SNP carrying the ancestry information distributed along the 24 European seabass chromosomes. The y axis represents the strength of the association as −log 10 of the P values. The dashed horizontal line represents the significance threshold computed with a Bonferroni correction. Blue vertical line represents the position of QTLs associated with population structure. Pink vertical line represents genomic regions with less than 5% of ATL ancestry. b) Violin and box plots of the fat residuals as a function of the ancestry (homozygous ATL, heterozygous ATL/MED, and homozygous MED) for the most significant QTL per LG. The letters indicate the significance of ANOVA and Tukey's test. c) Plots of local Atlantic ancestry rate and local recombination rate (in cM/Mb) of five chromosomes for the WEM populations. Green dots represent the local Atlantic ancestry rate within the WEM population at each SNP position. The red line represents the mean local recombination rate in cM/Mb. The x axis is the position in Mb within each chromosome. Vertical dark orange lines represent the QTLs position retrieved from the GWAS analysis.

Fig. 6.

Negative correlation between the ancestry genomic scores for the 637 QTLs and the fat residuals for each WEM individual represented by green dots (rho_spearman = −0.145, P-value < 0.0001).