Adaptive radiations represent some of the most remarkable explosions of diversification across the tree of life. However, the constraints to rapid diversification and how they are sometimes overcome, particularly the relative roles of genetic architecture and hybridization, remain unclear. Here, we address these questions in the Alpine whitefish radiation, using a whole-genome dataset that includes multiple individuals of each of the 22 species belonging to six ecologically distinct ecomorph classes across several lake-systems. We reveal that repeated ecological and morphological diversification along a common environmental axis is associated with both genome-wide allele frequency shifts and a specific, larger effect, locus, associated with the gene edar. Additionally, we highlight the possible role of introgression between species from different lake-systems in facilitating the evolution and persistence of species with unique trait combinations and ecology. These results highlight the importance of both genome architecture and secondary contact with hybridization in fuelling adaptive radiation.

Ecosystem degradation and biodiversity loss are major global challenges. When reproductive isolation between species is contingent upon the interaction of intrinsic lineage traits with features of the environment, environmental change can weaken reproductive isolation and result in extinction through hybridization. By this process called speciation reversal, extinct species can leave traces in genomes of extant species through introgressive hybridization. Using historical and contemporary samples, we sequenced all four species of an Alpine whitefish radiation before and after anthropogenic lake eutrophication and the associated loss of one species through speciation reversal. Despite the extinction of this taxon, substantial fractions of its genome, including regions shaped by positive selection before eutrophication, persist within surviving species as a consequence of introgressive hybridization during eutrophication. Given the prevalence of environmental change, studying speciation reversal and its genomic consequences provides fundamental insights into evolutionary processes and informs biodiversity conservation.

Theory suggests that speciation with gene flow is most likely when both sexual and ecological selection are divergent or disruptive. Divergent sexual and natural selection on the visual system have been demonstrated before in sympatric, morphologically similar sister species of Lake Victoria cichlids, but this does not explain the subtle morphological differences between them. To investigate the significance of natural selection on morphology during speciation, we here ask whether the prevalence of disruptive ecological selection differs between sympatric sister species that are at different stages of speciation. Some of our species pairs do () and others do not () differ distinctively in sexually selected male nuptial coloration. We find that (i) evidence for disruptive selection, and for evolutionary response to it, is prevalent in traits that are differentiated between sister species; (ii) prevalence of both predicts the extent of genetic differentiation; and (iii) genetic differentiation is weaker in species pairs with conserved male nuptial coloration. Our results speak to the existence of two different mechanisms of speciation with gene flow: speciation mainly by sexual selection tightly followed by ecological character displacement in some cases and speciation mainly by divergent ecological selection in others.