Widespread selection and gene flow shape the genomic landscape during a radiation of monkeyflowers

Abstract

Speciation genomic studies aim to interpret patterns of genome-wide variation in light of the processes that give rise to new species. However, interpreting the genomic ‘landscape’ of speciation is difficult, because many evolutionary processes can impact levels of variation. Facilitated by the first chromosome-level assembly for the group, we use whole-genome sequencing and simulations to shed light on the processes that have shaped the genomic landscape during a recent radiation of monkeyflowers. After inferring the phylogenetic relationships among the nine taxa in this radiation, we show that highly similar diversity (π) and differentiation (FST) landscapes have emerged across the group. Variation in these landscapes was strongly predicted by the local density of functional elements and the recombination rate, suggesting that the landscapes have been shaped by widespread natural selection. Using the varying divergence times between pairs of taxa, we show that the correlations between FST and genome features arose almost immediately after a population split and have become stronger over time. Simulations of genomic landscape evolution suggest that background selection (i.e., selection against deleterious mutations) alone is too subtle to generate the observed patterns, but scenarios that involve positive selection and genetic incompatibilities are plausible alternative explanations. Finally, tests for introgression among these taxa reveal widespread evidence of heterogeneous selection against gene flow during this radiation. Thus, combined with existing evidence for adaptation in this system, we conclude that the correlation in FST among these taxa informs us about the genomic basis of adaptation and speciation in this system.Author summaryWhat can patterns of genome-wide variation tell us about the speciation process? The answer to this question depends upon our ability to infer the evolutionary processes underlying these patterns. This, however, is difficult, because many processes can leave similar footprints, but some have nothing to do with speciation per se. For example, many studies have found highly heterogeneous levels of genetic differentiation when comparing the genomes of emerging species. These patterns are often referred to as differentiation ‘landscapes’ because they appear as a rugged topography of ‘peaks’ and ‘valleys’ as one scans across the genome. It has often been argued that selection against deleterious mutations, a process referred to as background selection, is primarily responsible for shaping differentiation landscapes early in speciation. If this hypothesis is correct, then it is unlikely that patterns of differentiation will reveal much about the genomic basis of speciation. However, using genome sequences from nine emerging species of monkeyflower coupled with simulations of genomic divergence, we show that it is unlikely that background selection is the primary architect of these landscapes. Rather, differentiation landscapes have probably been shaped by adaptation and gene flow, which are processes that are central to our understanding of speciation. Therefore, our work has important implications for our understanding of what patterns of differentiation can tell us about the genetic basis of adaptation and speciation.

Standing genetic variation and chromosomal rearrangements facilitate local adaptation in a marine fish

“…Our modelling approach indicated that approximately 45-50% of the genome was undergoing linked selection (Table 2) and that effective population size (ܰ ) was locally reduced to approximately 10-20% of its size due to Hill-Robertson interference ( Table 2). The role of such a linked selection process, unrelated to speciation, is increasingly recognized as being implicated in observed patterns of genome-wide divergence (Cruickshank & Hahn 2014, Burri 2017, and has been empirically demonstrated elsewhere (e.g., Burri et al 2015, Roux et al 2016, Wang et al 2016, Rougemont & Bernatchez, 2018, Stankowski et al 2019. Admittedly, further estimates of recombination rate variation along the genome will be needed to help disentangling how linked selective processes are currently affecting genome-wide divergence patterns.…”

Senecio as a model system for integrating studies of genotype, phenotype and fitness

“…Schilling et al, 2018) and empirically (e.g. Chapman et al, 2016;Safran et al, 2016;Doellman et al, 2018;Stankowski et al, 2019). Senecio contains multiple systems where these evolutionary dynamics can be studied.…”

Evidence for widespread selection in shaping the genomic landscape during speciation of Populus

“…Furthermore, studying variation in levels of differentiation within and between closely related species has the potential to yield important insights into the process of speciation (Ravinet et al, 2017; Wolf & Ellegren, 2017). Studies in a broad range of taxonomic groups have revealed a picture of a highly heterogeneous genomic landscape with peaks and valleys of diversity and differentiation (Han et al, 2017; Nadeau et al, 2012; Stankowski et al, 2019; Turner, Hahn, & Nuzhdin, 2005). Local peaks of elevated divergence are usually referred to as “speciation islands” and are thought to represent regions that drive the reproductive isolation between incipient species (Abbott et al, 2013; Wu, 2001).…”

“…As deleterious mutations are assumed to be much more common compared to beneficial mutations, background selection has been argued to play a major role in the evolution of diversity (Burri, 2017; Lohmueller et al, 2011; Phung et al, 2016). However, many recent simulation studies have shown that background selection alone is far from sufficient for generating the heterogenous genomic landscapes observed in empirical studies of recently diverged species, and other evolutionary processes (such as positive selection) are thus required to explain the observed patterns (Matthey‐Doret & Whitlock, 2019; Stankowski et al, 2019).…”

“…Furthermore, studying variation in levels of differentiation within and between closely related species has the potential to yield important insights into the process of speciation (Ravinet et al, 2017;. Studies in a broad range of taxonomic groups have revealed a picture of a highly heterogeneous genomic landscape with peaks and valleys of diversity and differentiation (Han et al, 2017;Nadeau et al, 2012;Stankowski et al, 2019;Turner, Hahn, & Nuzhdin, 2005).…”