Unravelling the genomic landscape of divergence between lineages is key to understanding speciation 1 . The naturally hybridizing collared flycatcher and pied flycatcher are important avian speciation models 2-7 that show pre-as well as postzygotic isolation 8,9 . We sequenced and assembled the 1.1-Gb flycatcher genome, physically mapped the assembly to chromosomes using a low-density linkage map 10 and re-sequenced population samples of each species. Here we show that the genomic landscape of species differentiation is highly heterogeneous with approximately 50 'divergence islands' showing up to 50-fold higher sequence divergence than the genomic background. These non-randomly distributed islands, with between one and three regions of elevated divergence per chromosome irrespective of chromosome size, are characterized by reduced levels of nucleotide diversity, skewed allele-frequency spectra, elevated levels of linkage disequilibrium and reduced proportions of shared polymorphisms in both species, indicative of parallel episodes of selection. Proximity of divergence peaks to genomic regions resistant to sequence assembly, potentially including centromeres and telomeres, indicate that complex repeat structures may drive species divergence. A much higher background level of species divergence of the Z chromosome, and a lower proportion of shared polymorphisms, indicate that sex chromosomes and autosomes are at different stages of speciation. This study provides a roadmap to the emerging field of speciation genomics.As lineages diverge, a combination of pre-as well as postzygotic reproductive isolation barriers will eventually arise 1 . Divergence is likely to start from specific loci that may precede and cause the evolution of reproductive incompatibility. Hybridization between diverging lineages may therefore create a genomic mosaic of regions where interspecific gene flow occurs at different rates (the genic view of speciation 11 ), with introgression expected to be weak in genomic regions involved in speciation. Revealing the genomic regions with elevated levels of divergence will eventually deepen our knowledge of the speciation process. However, more than 150 years after the publication of On the Origin of Species 12 , the genetic basis of speciation is still largely unresolved 13,14 . We know little about the identity, number and effect size of loci involved in population divergence, their genomic distribution and the type of mutations involved. Advances in sequencing technology now open a promising avenue for the study of genomic divergence, even for non-model vertebrate species with gigabase (Gb)-sized genomes.The collared flycatcher Ficedula albicollis and the pied flycatcher Ficedula hypoleuca (Fig. 1) are important study organisms for key aspects of evolutionary ecology and biology 2-7 . Diverged less than 2 million years ago, their history has been shaped by repeated cycles of glaciation in Eurasia where periods of allopatric divergence in refugia probably alternated with periods of secondary contact...

Speciation is a continuous process during which genetic changes gradually accumulate in the genomes of diverging species. Recent studies have documented highly heterogeneous differentiation landscapes, with distinct regions of elevated differentiation ("differentiation islands") widespread across genomes. However, it remains unclear which processes drive the evolution of differentiation islands; how the differentiation landscape evolves as speciation advances; and ultimately, how differentiation islands are related to speciation. Here, we addressed these questions based on population genetic analyses of 200 resequenced genomes from 10 populations of four Ficedula flycatcher sister species. We show that a heterogeneous differentiation landscape starts emerging among populations within species, and differentiation islands evolve recurrently in the very same genomic regions among independent lineages. Contrary to expectations from models that interpret differentiation islands as genomic regions involved in reproductive isolation that are shielded from gene flow, patterns of sequence divergence (d xy and relative node depth) do not support a major role of gene flow in the evolution of the differentiation landscape in these species. Instead, as predicted by models of linked selection, genome-wide variation in diversity and differentiation can be explained by variation in recombination rate and the density of targets for selection. We thus conclude that the heterogeneous landscape of differentiation in Ficedula flycatchers evolves mainly as the result of background selection and selective sweeps in genomic regions of low recombination. Our results emphasize the necessity of incorporating linked selection as a null model to identify genome regions involved in adaptation and speciation.[Supplemental material is available for this article.]Uncovering the genetic architecture of reproductive isolation and its evolutionary history are central tasks in evolutionary biology. The identification of genome regions that are highly differentiated between closely related species, and thereby constitute candidate regions involved in reproductive isolation, has recently been a major focus of speciation genetic research. Studies from a broad taxonomic range, involving organisms as diverse as plants (Renaut et al.

Climatic fluctuations during the Quaternary period governed the demography of species and contributed to population differentiation and ultimately speciation. Studies of these past processes have previously been hindered by a lack of means and genetic data to model changes in effective population size (N e) through time. However, based on diploid genome sequences of high quality, the recently developed pairwise sequentially Markovian coalescent (PSMC) can estimate trajectories of changes in N e over considerable time periods. We applied this approach to resequencing data from nearly 200 genomes of four species and several populations of the Ficedula species complex of black‐and‐white flycatchers. N e curves of Atlas, collared, pied and semicollared flycatcher converged 1–2 million years ago (Ma) at an N e of ≈ 200 000, likely reflecting the time when all four species last shared a common ancestor. Subsequent separate N e trajectories are consistent with lineage splitting and speciation. All species showed evidence of population growth up until 100–200 thousand years ago (kya), followed by decline and then start of a new phase of population expansion. However, timing and amplitude of changes in N e differed among species, and for pied flycatcher, the temporal dynamics of N e differed between Spanish birds and central/northern European populations. This cautions against extrapolation of demographic inference between lineages and calls for adequate sampling to provide representative pictures of the coalescence process in different species or populations. We also empirically evaluate criteria for proper inference of demographic histories using PSMC and arrive at recommendations of using sequencing data with a mean genome coverage of ≥18X, a per‐site filter of ≥10 reads and no more than 25% of missing data.

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Identifying genomic regions underlying adaptation in extant lineages is key to understand the trajectories along which biodiversity evolves. However, this task is complicated by evolutionary processes that obscure and mimic footprints of positive selection. Particularly the long-term effects of linked selection remain underappreciated and difficult to account for. Based on patterns emerging from recent research on the evolution of differentiation across the speciation continuum, I illustrate how long-term linked selection affects the distribution of differentiation along genomes. I then argue that a comparative population genomics framework that exploits emergent features of long-term linked selection can help overcome shortcomings of traditional genome scans for adaptive evolution, but needs to account for the temporal dynamics of differentiation landscapes.Since the dawn of high-throughput sequencing, the inference of genomic regions of accentuated differentiation (Box 1) -variously referred to as differentiation islands, divergence islands, or speciations islands (Box 2) -has become a central focus of research on local adaptation and speciation. The past years have seen an unprecedented quest for such regions (Haasl & Payseur 2016) that assumed accentuated differentiation to evolve trough processes related to adaptation or speciation, in particular positive selection of beneficial variants (Maynard Smith & Haigh 1974;Kaplan et al. 1989) or selection against gene flow (Turner et al. 2005) in extant populations or species (in the following referred to as 'extant lineages', see Glossary). However, recent research highlights that accentuated differentiation may evolve through processes other than positive selection (e. g. Bank et al. 2014;Cruickshank & Hahn 2014;Haasl & Payseur 2016).Particularly, several aspects of linked selection may remain underappreciated. First, awareness that purifying selection at linked sites (background selection, BGS) (Charlesworth et al. 1993;Charlesworth 2013) makes important contributions to linked selection and can mimic the footprints of positive selection (Stephan 2010) is still limited. Furthermore, part of the effects of linked selection observed today may have accumulated over extended periods of time and therefore be related to adaptation in ancestral rather than extant lineages (McVicker et al. 2009;Munch et al. 2016;Phung et al. 2016). Approaches that assist disentangling the effects of alternative forms of selection and the timescales at which they acted are called for.Here, I first showcase the impact of linked selection on the long-term evolution of genetic diversity and hence differentiation (Charlesworth 1998). I then discuss how these effects lead to the evolution of temporally dynamic correlations of differentiation landscapes, and how this process may be influenced by demography and the evolution of genome features. I close by . CC-BY-NC-ND 4.0 International license not peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this pr...