Shedding Light on the Grey Zone of Speciation along a Continuum of Genomic Divergence

International audienceSpeciation results from the progressive accumulation of mutations that decrease the probability of mating between parental populations or reduce the fitness of hybrids-the so-called species barriers. The speciation genomic literature, however, is mainly a collection of case studies, each with its own approach and specificities, such that a global view of the gradual process of evolution from one to two species is currently lacking. Of primary importance is the prevalence of gene flow between diverging entities, which is central in most species concepts and has been widely discussed in recent years. Here, we explore the continuum of speciation thanks to a comparative analysis of genomic data from 61 pairs of populations/ species of animals with variable levels of divergence. Gene flow between diverging gene pools is assessed under an approximate Bayesian computation (ABC) framework. We show that the intermediate "grey zone" of speciation, in which taxonomy is often controversial , spans from 0.5% to 2% of net synonymous divergence, irrespective of species life history traits or ecology. Thanks to appropriate modeling of among-locus variation in genetic drift and introgression rate, we clarify the status of the majority of ambiguous cases and uncover a number of cryptic species. Our analysis also reveals the high incidence in animals of semi-isolated species (when some but not all loci are affected by barriers to gene flow) and highlights the intrinsic difficulty, both statistical and conceptual, of delineating species in the grey zone of speciation. Author Summary Isolated populations accumulate genetic differences across their genomes as they diverge, whereas gene flow between populations counteracts divergence and tends to restore genetic homogeneity. Speciation proceeds by the accumulation at specific loci of mutations that reduce the fitness of hybrids, therefore preventing gene flow-the so-called species barriers. Importantly, species barriers are expected to act locally within the genome, leading to the prediction of a mosaic pattern of genetic differentiation between populations at intermediate levels of divergence-the genic view of speciation. At the same time, linked selection also contributes to speed up differentiation in low-recombining and PLOS Biology