Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization.

In contrast to the large amount of ecological information supporting the role of natural selection as a main cause of population divergence and speciation, an understanding of the genomic basis underlying those processes is in its infancy. In this paper, we review the main findings of a long-term research programme that we have been conducting on the ecological genomics of sympatric forms of whitefish (Coregonus spp.) engaged in the process of speciation. We present this system as an example of how applying a combination of approaches under the conceptual framework of the theory of adaptive radiation has yielded substantial insight into evolutionary processes in a non-model species. We also discuss how the joint use of recent biotechnological developments will provide a powerful means to address issues raised by observations made to date. Namely, we present data illustrating the potential offered by combining next generation sequencing technologies with other genomic approaches to reveal the genomic bases of adaptive divergence and reproductive isolation. Given increasing access to these new genomic tools, we argue that non-model species studied in their ecological context such as whitefish will play an increasingly important role in generalizing knowledge of speciation.

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Fish abundance surveys in the Rhine system have shown in the past two decades that there is a rapid upriver invasion of a freshwater sculpin of the genus Cottus. These fish are found in habitats that are atypical for the known species Cottus gobio, which is confined to small cold streams within the Rhine drainage. Phylogeographic analysis based on mitochondrial haplotypes and diagnostic single nucleotide polymorphisms indicates that the invasive sculpins are hybrids between two old lineages from the River Scheldt drainage and the River Rhine drainage, although it is morphologically more similar to the Scheldt sculpins. Most importantly, however, the invasive population possesses a unique ecological potential that does not occur in either of the source populations from the Rhine or the Scheldt, which allows the colonization of new habitats that have previously been free of sculpins. Microsatellite analysis shows that the new lineage is genetically intermediate between the old lineages and that it forms a distinct genetic group across its whole expansion range. We conclude that hybridization between long separated groups has lead to the fast emergence of a new, adaptationally distinct sculpin lineage.