The multiple population genetic and demographic routes to islands of genomic divergence

Abstract

1 1 1. The way that organisms diverge into reproductively isolated species is a major question in 1 2 biology. The recent accumulation of genomic data provides promising opportunities to 1 3 understand the genomic landscape of divergence, which describes the distribution of 1 4 differences across genomes. Genomic areas of unusually high differentiation have been called 1 5 genomic islands of divergence. Their formation has been attributed to a variety of 1 6 mechanisms, but a prominent hypothesis is that they result from divergent selection over a 1 7 small portion of the genome, with surrounding areas homogenised by gene flow. Such islands 1 8 have often been interpreted as being associated with divergence with gene flow. However 1 9other mechanisms related to genetic architecture and population history can also contribute to 2 0 the formation of genomic islands of divergence. 2 1 2. We currently lack a quantitative framework to examine the dynamics of genomic landscapes 2 2 under the complex and nuanced conditions that are found in natural systems. Here, we 2 3 develop an individual-based simulation to explore the dynamics of diverging genomes under 2 4 various scenarios of gene flow, selection and genotype-phenotype maps. 2 5 3. Our modelling results are consistent with empirical observations demonstrating the formation 2 6of genomic islands under genetic isolation. Importantly, we have quantified the range of 2 7 conditions that produce genomic islands. We demonstrate that the initial level of genetic 2 8 diversity, drift, time since divergence, linkage disequilibrium, strength of selection and gene 2 9 flow are all important factors that can influence the formation of genomic islands. Because the 3 0 accumulation of genomic differentiation over time tends to erode the signal of genomic 3 1 islands, genomic islands are more likely to be observed in recently divergent taxa, although 3 2 not all recently diverged taxa will necessarily exhibit islands of genomic divergence. Gene 3 3 flow primarily slows the swamping of islands of divergence with time. 3 44. By using this framework, further studies may explore the relative influence of particular suites 3 5 of events that contribute to the emergence of genomic islands under sympatric, parapatric and 3 6 allopatric conditions. This approach represents a novel tool to explore quantitative 3 7 expectations of the speciation process, and should prove useful in elucidating past and 3 8 projecting future genomic evolution of any taxa. 3 9 4 0

Speciation genomics and the role of depth in the divergence of rockfishes (Sebastes) revealed through Pool‐seq analysis of enriched sequences

“…miniatus pair, which is expected given the disparity in divergence time observed in these taxa (Hyde & Vetter, 2007). Recently diverged species pairs are likely to retain signals of divergent selection associated with speciation as these signals erode over the amount of time species pairs are isolated (Quilodrán et al, 2020). Enriched GO terms for genes found within the S. chlorostictus–S.…”

“…It is possible that our approach is not applicable to more diverged species pairs and would benefit from methods that could account for levels of intraspecific variation (Cruickshank & Hahn, 2014). The amount of divergence between S. crocotulus and S. miniatus has likely eroded most of the signal associated with speciation due to the increased effects of drift and recombination (Quilodrán et al, 2020). The significant gene ontology terms that we did identify for this pair were associated with basic housekeeping functions (actin regulation of polymerization, the SWI/SNF pathways, histone lysine methylation pathways, tight junction, and regulation of actin filament polymerization) and cannot be associated with differences in depth for this species pair.…”

“…Our comparisons include two species pairs that span a range of divergence across the speciation continuum (Behrens et al, 2021; Hyde et al, 2008). Identification of clear regions of divergence in the more diverged species pair possesses additional challenges, as drift and recombination may erode any signals associated with speciation‐related divergence (Quilodrán et al, 2020).…”

Geographical context outweighs habitat disturbance effects in explaining mistletoe population genetic differentiation at a regional scale

“…On the one hand, historical events can determine large‐scale genetic variation patterns, related to the geographical context (e.g., coast vs. interior, or lowlands vs. highlands). For example, genetic divergence is more common in insular systems as each island has different ecological conditions, driving independent evolutionary processes, which reduce genetic diversity, and isolation increases genetic structure (De Kort et al, 2021; Quilodran et al, 2020). Thus, major biogeographical events such as orogenesis, glaciations or desertification determine the geographical context, altering large‐scale gene flow and genetic diversity and increasing genetic differentiation among populations (Darroch et al, 2021; Myers et al, 2020).…”

Genomic islands of divergence betweenDrosophila yakubasubspecies predominantly overlap with chromosomal inversions

“…However, a plethora of mechanisms may also lead to heterogeneous patterns of genetic differentiation across the genome even in the absence of divergent selection. Most importantly, variation in recombination rate, due to heterochromatin content or structural variation, strongly affects the rate of the accumulation of genetic differences in natural populations (Feder and Nosil 2009; Cruickshank and Hahn 2014; Quilodrán et al 2019; Huang et al 2020). Chromosomal inversions are among the most common forms of structural variation, and a number of studies have unraveled an overlap between inversions and GIDs (Feder and Nosil 2009; Michel et al 2010; Ellegren et al 2012; Sodeland et al 2016; Huang et al 2020).…”