Divergence and introgression among the virilis group of Drosophila

Abstract

Speciation with gene flow is now widely regarded as common. However, the frequency of introgression between recently diverged species and the evolutionary consequences of gene flow are still poorly understood. The virilis group of Drosophila contains 12 species that are geographically widespread and show varying levels of prezygotic and postzygotic isolation. Here, we use de novo genome assemblies and whole-genome sequencing data to resolve phylogenetic relationships and describe patterns of introgression and divergence across the group. We suggest that the virilis group consists of three, rather than the traditional two, subgroups. Some genes undergoing rapid sequence divergence across the group were involved in chemical communication and desiccation tolerance, and may be related to the evolution of sexual isolation and adaptation. We found evidence of pervasive phylogenetic discordance caused by ancient introgression events between distant lineages within the group, and more recent gene flow between closely related species. When assessing patterns of genome-wide divergence in species pairs across the group, we found no consistent genomic evidence of a disproportionate role for the X chromosome as has been found in other systems. Our results show how ancient and recent introgressions confuse phylogenetic reconstruction, but may play an important role during early radiation of a group.

Keywords: Divergence; gene flow; introgression; phylogenomics; reproductive isolation; speciation.

Figure 1

Species tree of the virilis group with estimated divergence times. (a) Species tree reconstruction was performed using ASTRAL and gene trees for 1336 single‐copy orthologs. Divergence times were estimated using the BPP program (see Supplementary material) and randomly sampled, genome‐wide small introns (100 loci consisting of 75–85 bp small introns). Posterior estimates for divergence times were scaled using a single calibration point (denoted by the red dot; see text for details). (b) Principal component analysis (PCA) showing species relationships using randomly sampled SNPs on the X chromosome (3218 SNPs) and autosomes (12,272 SNPs). (c) Map showing putative ranges for species in all three phylads. Created with BioRender.com

Figure 2

Gene flow is extensive between Palearctic and Nearctic members of the montana and littoralis phylads. (a) D‐statistic values shown between species with significant, excess allele sharing. (b) Admixture proportions (f4‐ratio) between species with evidence of significant, excess allele sharing

Figure 3

Genome‐wide introgression facilitates phylad‐specific gene sharing. (a) Schematic showing directionality of gene flow tested by f _dm statistic and pie chart illustrating proportion of introgression between species in each comparison calculated using f _dm. (b) Distributions of introgression across chromosomes for each comparison. Dotted line indicates neutrality (no allele sharing). (c) Genome‐wide introgression shown across chromosomes for each comparison, with solid line indicating neutrality. Here, species names are abbreviated (M: D. montana, La: D. lacicola, B: D. borealis, F: D. flavomontana, E: D. ezoana, Li: D. littoralis, K: D. kanekoi, N: D. novamexicana, Lu: D. lummei; and A: D. americana. Asterisks on topologies represent topologies that are concordant with the species tree.

Figure 4

Absolute divergence calculated for each chromosome across coding and noncoding regions. d _XY was calculated using genome‐wide ∼50‐kb windows between species pairs in the virilis group. (a) d _XY was calculated for coding regions across the four species pairs and (b) for intergenic regions. The species pairs shown here are the following: D. montana and D. lacicola (M–L), D. borealis and D. flavomontana (B–F), D. kanekoi and D. ezoana (K–E), and D. novamexicana and D. americana (N–A). Significance between all chromosomes was tested using an ANOVA and significance between the X chromosome and each of the autosomes was tested using the Tukey test. Stars indicate level of significance: 0 = ***, 0.001 = **, 0.01 = *, 0.05 = ., and >0.05 = ns.