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• W2743705067 abstract "Based on the assumption that locally accentuated differentiation within genomes represents a footprint of positive selection or barriers to gene flow, the last decade's quest for genomic regions involved in adaptation and speciation has led to the description of differentiation landscapes in numerous taxa (e.g. Ellegren et al., 2012; Jones et al., 2012; Renaut et al., 2013; Soria-Carrasco et al., 2014). A major common pattern emerging from this research is a usually striking heterogeneity of differentiation along the genome, with regions of accentuated differentiation widespread across otherwise less differentiated genomes – as widespread and in several cases so markedly codistributed with genomic features (e.g. White et al., 2010; Burri et al., 2015), as to question these regions’ role in speciation (Noor & Bennett, 2009; Nachman & Payseur, 2012; Cruickshank & Hahn, 2014). In their review, Ravinet et al. (2017) discuss the complex evolution of differentiation landscapes, involving multiway interactions of diverse processes, and propose a road map through the challenge of disentangling the footprints of speciation from those of confounding processes. Here, I outline a few complementary angles from a linked selection's perspective. (i) I revisit the effects of linked selection, suggesting that they may depend on the dynamics of recombination rate evolution. (ii) I then emphasize the need for analyses to target the most likely footprints of speciation given a system's evolutionary history and its history of linked selection. (iii) Finally, I highlight how long-range sequencing will empower the characterization of genomic landscapes beyond differentiation. In isolation, selection and variation in recombination rate and density of functional sites are not expected to contribute to heterogeneous genomic landscapes (Fig. 1a). In interaction, however, they combine to a powerful process with a deep impact on the genomic distribution of diversity and differentiation (Fig. 1b) – linked selection (Cutter & Payseur, 2013). Under the action of selection, variation in recombination rate and functional densities along the genome give rise to heterogeneous landscapes of diversity and hence differentiation (Fig. 1b). Likewise, demographic effects are unaffected by variation in molecular features alone (Fig. 1), without a major effect on the heterogeneity of differentiation landscapes beyond introducing variance. However, demographic effects acting on a heterogeneous diversity landscape – such as resulting from linked selection – may further pronounce already markedly heterogeneous landscapes, with stronger effects expected in genomic regions with reduced effective population size (Ne) (Fig. 1), although the importance of such effects remains largely unexplored. Recombination rate and functional density, therefore, may be seen as modulators of the effects of selection (Fig. 1), determining the physical size of the genomic region affected by selection and the frequency with which it is acted upon by selection, respectively. The effect of recombination on the long-term evolution of differentiation landscapes – and by which it contributes to confound footprints of speciation – may strongly depend on the dynamics of recombination rate evolution, which may vary markedly among species (Smukowski & Noor, 2011). First, confounding effects mediated by recombination depend on the extent of recombination rate variation, having a weaker impact in genomic regions (e.g. non-recombining parts of sex chromosomes) or species with little to no recombination rate variation. Second, the recombination-mediated effects may strongly depend on the timescale across which the same genome regions have experienced low recombination and been exposed to stronger linked selection, and hence on the stability of the recombination landscape. In birds, for instance, recombination landscapes are stable across tens of millions of years (Singhal et al., 2015), implying long time periods during which the diversity-reducing effects of linked selection have time to accumulate more in low-recombination regions. Indeed, linked selection appears to have reduced diversity and increased differentiation in the same genomic regions among species as far diverged as 50 my (Dutoit et al., 2017; Van Doren et al., 2017; Vijay et al., 2017), resulting in correlated differentiation landscapes. Similar patterns, though over shorter timescales, have been documented, for example, in sunflowers (Renaut et al., 2014) and butterflies (Martin et al., 2013). In such species, recombination rate variation complicates the interpretation of accentuated differentiation in terms of adaptation or speciation: it may be the result of a local reduction in Ne through (i) background selection (Charlesworth et al., 1993) rather than sweeps, or (ii) sweeps in ancestral lineages combined with drift in extant lineages (e.g. Munch et al., 2016). Both processes are unrelated to speciation, and their effects expected to be strongest in species with stable recombination landscapes. In contrast, in systems with a rapid turnover of the recombination landscape, such as related to the PRDM9-dominated recombination regulation of many mammals (Oliver et al., 2009; Baudat et al., 2010), the more dynamic movement of low-recombination regions may distribute the effects of linked selection more equally along the genome, potentially rendering such systems less prone to confounding effects of linked selection. As Ravinet et al. (2017) outline, considering a system's evolutionary history may represent a most crucial first step towards dissecting differentiation landscapes. Moreover, the above suggests that to assess the confounding effects of linked selection, differentiation landscapes need to be characterized beyond the focal system. Failure to do so risks to result in a misleading interpretation of regions of accentuated differentiation. In systems like birds, the repeated observation of accentuated differentiation in independent lineages alone cannot be taken as replication to confirm a genomic regions’ involvement in adaptation/speciation, nor as evidence for parallel evolution. Rather, accentuated differentiation in the same (low recombination) regions – even in independent species pairs – is predicted under linked selection in stable recombination landscapes, and not necessarily related to speciation or adaptation of extant lineages (Burri, 2017). Therefore, the observation of differentiation landscapes that are correlated between the focal system and closely related lineages should raise a warning flag to caution against adaptation- or speciation-related interpretations. Genome-wide association studies that link genetic variants to phenotypes or environment and group individuals according to the latter may suffer less from these caveats, because individuals are randomized with respect to their history of linked selection and genetic drift. However, it is not clear to which extent long-term linked selection may introduce spurious results as a consequence of reduced genetic diversity. In either case, a comparative population genomics approach may help assessing whether the outlined problems connected with the long-term effects of linked selection apply to the system and timescale in question. Furthermore, this approach enables an empirical formulation of a dynamic differentiation baseline along the genome that takes into account the temporal dynamics of correlated differentiation landscapes against which candidate regions can be discriminated (Burri, 2017). Ravinet et al. (2017) lay out in detail the genomic footprints of the speciation process and how they may vary among different evolutionary histories. In particular, the history of gene flow may determine the most prevalent footprints of speciation to be expected, and to which sequencing experiments and population genomic analyses should be tailored. Under speciation-with-gene-flow, the demonstration of gene flow may be limited to direct observations of dispersers, and genomic footprints largely limited to those left by speciation-associated selection at barrier loci. In contrast, in cases of gene flow at secondary contact, speciation-associated selection may be more challenging to trace. They may not exist because reproductive incompatibilities have fixed neutrally; or selection related to reproductive isolation may have occurred far in the past and its footprints have been eroded. Meanwhile, gene flow may be more readily detectable, for instance in haplotype structure (Hellenthal et al., 2014) or by simultaneous accentuations of differentiation (FST) and sequence divergence (dXY) (Cruickshank & Hahn, 2014). Since Cruickshank & Hahn (2014) advocated the latter approach, it has become popular to confirm regions of accentuated differentiation as barrier loci. However, the limits of this approach remain vastly underappreciated. As illustrated in Fig. 2, this approach has no power whatsoever at early stages of differentiation and is limited to systems with considerable divergence (in allopatry, Fig. 2b, or at barrier loci, Fig. 2c). To make things worse, in heterogeneous recombination landscapes the effect of barriers to gene flow is likely masked by linked selection (Fig. 2d-f). In conclusion, the importance of considering the system's evolutionary history – including colonization history, form and timing of gene flow, and divergence times – but also the impact of linked selection should be emphasized. Over the past decades, the quest for barrier loci has strongly relied on SNP-based scans for accentuated differentiation. As Ravinet et al.'s (2017) review makes clear, this approach is not without its caveats, and the future quest for genomic regions involved in speciation and adaptation is bound to move towards including molecular variation beyond SNPs, and footprints beyond diversity and differentiation; and ultimately towards de novo-based population genomics (Chaisson et al., 2015). Cost-effective long-range sequencing technologies (e.g. Illumina synthetic long reads, 10× Genomics Chromium) promise important steps in this direction in the near future. Benefits of this technology include access to large-scale structural variants, such as hypothesized inversions linked to speciation (e.g. Poelstra et al., 2014), and more contiguous reference genomes (Chin et al., 2016) with better annotations (Dong et al., 2015). Maybe more importantly, the physically phased long-range haplotypes delivered by long-range sequencing empower a more sophisticated characterization of haplotype structure and its dynamics along the genome that ultimately provide a more detailed picture of the genomic landscape, and the processes that shape it: footprints of sweeps (e.g. Voight et al., 2006; Sabeti et al., 2007), timing and extent of gene flow (Hellenthal et al., 2014) – the events we are ultimately interested in in the quest for the loci of adaptation and speciation. I thank Marta Promerová and Sam Yeaman for helpful comments on the manuscript." @default.
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• W2743705067 date "2017-08-01" @default.
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• W2743705067 title "Dissecting differentiation landscapes: a linked selection's perspective" @default.
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