Genomics and the origin of species

Key Points Speciation is a central and fundamental process in evolution that concerns the origin of reproductive isolation. The latest generation of genomic approaches provide remarkable opportunities to describe speciation and to learn about its underlying mechanisms. Genome scans, which can now be carried out in a truly genome-wide scale and at base-pair resolution, reveal substantial genomic divergence among incipient species even in the face of gene flow and show that there is extensive genomic heterogeneity in the extent of differentiation, especially at early stages of speciation, both in sympatry and in allopatry. The sources of this heterogeneity remain incompletely understood. The combination of genome scans with sophisticated population genetic modelling, quantitative trait locus mapping, admixture analyses and ecology has the potential to distinguish the influence of selection from demographic, historical and structural effects and to link these sources of genomic divergence to phenotypes and to reproductive isolation. Available empirical data suggest that differentiation between parapatric populations can be restricted to few genomic islands, whereas incipient species that coexist in sympatry show differentiation that is widely distributed across the genome. This suggests that genomically widespread selection is required to permit the maintenance and perhaps the build-up of genetic differentiation in sympatry. Recent genomic studies reveal that the genetic basis of reproductive isolation is often complex. The effects of pleiotropy, genetic correlations and patterns of recombination need to be considered alongside effects of ecological and sexual selection as well as genomic conflict. A surprising recent discovery is the re-use of ancient genetic variants in speciation, which are acquired either from standing genetic variation or by introgressive hybridization. In this Review, we propose a 'roadmap' for the development of speciation genomics towards answering classical and emerging questions in speciation research. Genomic approaches are an increasingly important aspect of speciation research. The authors review recent insights from speciation genomics and propose a roadmap for this field, which is aimed at addressing both long-standing and emerging questions about speciation. Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly i