scholarly journals The genomic landscape of divergence across the speciation continuum in island-colonising silvereyes (Zosterops lateralis)

2020 ◽  
Author(s):  
Ashley T. Sendell-Price ◽  
Kristen C. Ruegg ◽  
Eric C. Anderson ◽  
Claudio S. Quilodrán ◽  
Benjamin M. Van Doren ◽  
...  
Keyword(s):  
Gene Flow ◽  
Evolutionary Dynamics ◽  
Genomic Islands ◽  
Rad Sequencing ◽  
Zosterops Lateralis ◽  
Genome Wide ◽  
Genomic Landscape ◽  
Limited Support ◽  
Speciation Continuum ◽  
Genomic Patterns

ABSTRACTA goal of the genomic era is to infer the evolutionary dynamics at play during the process of speciation by analysing the genomic landscape of divergence. However, empirical assessments of genomic landscapes under varying evolutionary scenarios are few, limiting the ability to achieve this goal. Here we combine RAD-sequencing and individual-based simulations to evaluate the genomic landscape in the silvereye (Zosterops lateralis). Using comparisons matched for divergence timeframe and gene flow context, we document how genomic patterns accumulate along the speciation continuum. In contrast to previous predictions, our results provide limited support for the idea that divergence accumulates around loci under divergent selection or that genomic islands widen with time. While a small number of genomic islands were found in populations diverging with and without gene flow, in few cases were SNPs putatively under selection tightly associated with genomic islands. Furthermore, we modelled the transition from localised to genome-wide levels of divergence using individual-based simulations that considered only neutral processes. Our results challenge the ubiquity of existing verbal models that explain the accumulation of genomic differences across the speciation continuum and instead support the idea that divergence both within and outside of genomic islands is important during the speciation process.DATA ACCESSION NUMBERSResequencing data from this study have been submitted to the National Center for Biotechnology Information (NCBI; https://www.ncbi.nlm.nih.gov) under accession number PRJNA489169.

scholarly journals The Genomic Landscape of Divergence Across the Speciation Continuum in Island-Colonising Silvereyes (Zosterops lateralis)

2020 ◽  
Vol 10 (9) ◽  
pp. 3147-3163
Author(s):  
Ashley T Sendell-Price ◽  
Kristen C Ruegg ◽  
Eric C Anderson ◽  
Claudio S Quilodrán ◽  
Benjamin M Van Doren ◽  
...  
Keyword(s):  
Gene Flow ◽  
Evolutionary Dynamics ◽  
Population Genomics ◽  
A Priori ◽  
Genomic Islands ◽  
Zosterops Lateralis ◽  
Genome Wide ◽  
Genomic Landscape ◽  
Speciation Continuum ◽  
Genomic Patterns

Abstract Inferring the evolutionary dynamics at play during the process of speciation by analyzing the genomic landscape of divergence is a major pursuit in population genomics. However, empirical assessments of genomic landscapes under varying evolutionary scenarios that are known a priori are few, thereby limiting our ability to achieve this goal. Here we combine RAD-sequencing and individual-based simulations to evaluate the genomic landscape of divergence in the silvereye (Zosterops lateralis). Using pairwise comparisons that differ in divergence timeframe and the presence or absence of gene flow, we document how genomic patterns accumulate along the speciation continuum. In contrast to previous predictions, our results provide limited support for the idea that divergence accumulates around loci under divergent selection or that genomic islands widen with time. While a small number of genomic islands were found in populations diverging with and without gene flow, in few cases were SNPs putatively under selection tightly associated with genomic islands. The transition from localized to genome-wide levels of divergence was captured using individual-based simulations that considered only neutral processes. Our results challenge the ubiquity of existing verbal models that explain the accumulation of genomic differences across the speciation continuum and instead support the idea that divergence both within and outside of genomic islands is important during the speciation process.

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

2018 ◽  
Author(s):  
Sean Stankowski ◽  
Madeline A. Chase ◽  
Allison M. Fuiten ◽  
Murillo F. Rodrigues ◽  
Peter L. Ralph ◽  
...  
Keyword(s):  
Gene Flow ◽  
Local Density ◽  
Background Selection ◽  
Deleterious Mutations ◽  
Evolutionary Processes ◽  
Genome Wide ◽  
Genomic Landscape ◽  
Genome Features ◽  
Genomic Studies ◽  
Genomic Basis

AbstractSpeciation 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.

scholarly journals Interactions between natural selection and recombination shape the genomic landscape of introgression

2021 ◽  
Author(s):  
Maud Duranton ◽  
John Pool
Keyword(s):  
North American ◽  
African Ancestry ◽  
North American Population ◽  
Evolutionary Forces ◽  
The North ◽  
Genome Wide ◽  
Genomic Landscape ◽  
The One ◽  
The Relationship ◽  
Genomic Patterns

AbstractHybridization between lineages that have not reached complete reproductive isolation appears more and more like a common phenomenon. Indeed, speciation genomics studies have now extensively shown that many species’ genomes have hybrid ancestry. However, genomic patterns of introgression are often heterogeneous across the genome. In many organisms, a positive correlation between introgression levels and recombination rate has been observed. It is usually explained by the purging of deleterious introgressed material due to incompatibilities. However, the opposite relationship was observed in a North American population of Drosophila melanogaster with admixed European and African ancestry. In order to explore how directional and epistatic selection can impact the relationship between introgression and recombination, we performed forward simulations of whole D. melanogaster genomes reflecting the North American population’s history. Our results revealed that the simplest models of positive selection often yield negative correlations between introgression and recombination such as the one observed in D. melanogaster. We also confirmed that incompatibilities tend to produce positive introgression-recombination correlations. And yet, we identify parameter space under each model where the predicted correlation is reversed. These findings deepen our understanding of the evolutionary forces that may shape patterns of ancestry across genomes, and they strengthen the foundation for future studies aimed at estimating genome-wide parameters of selection in admixed populations.

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

2019 ◽  
Author(s):  
Jing Wang ◽  
Nathaniel R. Street ◽  
Eung-Jun Park ◽  
Jianquan Liu ◽  
Pär K. Ingvarsson
Keyword(s):  
Recurrent Selection ◽  
Balancing Selection ◽  
Forest Tree ◽  
Species Variation ◽  
Recombination Rates ◽  
Genome Wide ◽  
Genomic Landscape ◽  
Speciation Continuum ◽  
Whole Genome Resequencing

AbstractIncreasing our understanding of how various evolutionary processes drive the genomic landscape of variation is fundamental to a better understanding of the genomic consequences of speciation. However, the genome-wide patterns of within- and between-species variation have not been fully investigated in most forest tree species despite their global ecological and economic importance. Here, we use whole-genome resequencing data from four Populus species spanning the speciation continuum to reconstruct their demographic histories, investigate patterns of diversity and divergence, infer their genealogical relationships and estimate the extent of ancient introgression across the genome. Our results show substantial variation in these patterns along the genomes although this variation is not randomly distributed but is strongly predicted by the local recombination rates and the density of functional elements. This implies that the interaction between recurrent selection and intrinsic genomic features has dramatically sculpted the genomic landscape over long periods of time. In addition, our findings provide evidence that, apart from background selection, recent positive selection and long-term balancing selection are also crucial components in shaping patterns of genome-wide variation during the speciation process.

scholarly journals Transitions from Single- to Multi-locus Processes during Speciation

2018 ◽  
Author(s):  
Martin P. Schilling ◽  
Sean P. Mullen ◽  
Marcus Kronforst ◽  
Rebecca J. Safran ◽  
Patrik Nosil ◽  
...  
Keyword(s):  
Linkage Disequilibrium ◽  
Gene Flow ◽  
Empirical Data ◽  
Theoretical Work ◽  
Statistical Characteristics ◽  
Genome Resequencing ◽  
Multiple Loci ◽  
Genome Wide ◽  
Speciation Continuum ◽  
Statistical Consequence

During speciation-with-gene-flow, a transition from single-locus to multi-locus processes can occur, as strong coupling of multiple loci creates a barrier to gene flow. Testing predictions about such transitions with empirical data requires building upon past theoretical work and the continued development of quantitative approaches. We simulated genomes under different evolutionary scenarios of gene flow and divergent selection, extending previous work with the additions of neutral sites and coupling statistics, allowing us to investigate if and how selected and neutral sites differ in the conditions they require for transitions during speciation. As the per-locus strength of selection grew and/or migration decreased, it became easier for selected sites to show divergence – and thus to rise in linkage disequilibrium (LD) with each other as a statistical consequence – farther in advance of the conditions under which neutral sites could diverge. Indeed, even very low rates of gene flow were sufficient to prevent differentiation at neutral sites. However, once strong enough, coupling among selected sites eventually reduced gene flow at neutral sites as well. To explore whether similar transitions might be detectable in empirical data, we used published genome resequencing data from three taxa of Heliconius butterflies. We found that allele-frequency outliers and F ST outliers exhibited stronger patterns of LD than the genomic background, as expected. The statistical characteristics of LD – likely indicative of the strength of coupling of barrier loci – varied between chromosomes and taxonomic comparisons. Broad qualitative agreement between the patterns we observed in the empirical data and our simulations suggests that selection drives rapid genome-wide transitions to multi-locus coupling, illustrating how divergence and gene flow interact along the speciation continuum.

scholarly journals Genomic islands of divergence or opportunities for introgression?

2017 ◽  
Vol 284 (1850) ◽  
pp. 20162414 ◽  
Author(s):  
Rachael A. Bay ◽  
Kristen Ruegg
Keyword(s):  
Gene Flow ◽  
Reproductive Isolation ◽  
Genomic Islands ◽  
Secondary Contact ◽  
Catharus Ustulatus ◽  
Adaptive Introgression ◽  
Evolutionary Forces ◽  
Genome Wide ◽  
Isolating Mechanisms ◽  
Migratory Songbird

In animals, introgression between species is often perceived as the breakdown of reproductive isolating mechanisms, but gene flow between incipient species can also represent a source for potentially beneficial alleles. Recently, genome-wide datasets have revealed clusters of differentiated loci (‘genomic islands of divergence’) that are thought to play a role in reproductive isolation and therefore have reduced gene flow. We use simulations to further examine the evolutionary forces that shape and maintain genomic islands of divergence between two subspecies of the migratory songbird, Swainson's thrush ( Catharus ustulatus ), which have come into secondary contact since the last glacial maximum. We find that, contrary to expectation, gene flow is high within islands and is highly asymmetric. In addition, patterns of nucleotide diversity at highly differentiated loci suggest selection was more frequent in a single ecotype. We propose a mechanism whereby beneficial alleles spread via selective sweeps following a post-glacial demographic expansion in one subspecies and move preferentially across the hybrid zone. We find no evidence that genomic islands are the result of divergent selection or reproductive isolation, rather our results suggest that differentiated loci both within and outside islands could provide opportunities for adaptive introgression across porous species boundaries.

scholarly journals Genome-Wide Congealing and Rapid Transitions across the Speciation Continuum during Speciation with Gene Flow

2014 ◽  
Vol 105 (S1) ◽  
pp. 810-820 ◽  
Author(s):  
Jeffrey L. Feder ◽  
Patrik Nosil ◽  
Aaron C. Wacholder ◽  
Scott P. Egan ◽  
Stewart H. Berlocher ◽  
...  
Keyword(s):  
Gene Flow ◽  
Genome Wide ◽  
Speciation Continuum

scholarly journals Establishment of new mutations under divergence and genome hitchhiking

2012 ◽  
Vol 367 (1587) ◽  
pp. 461-474 ◽  
Author(s):  
Jeffrey L. Feder ◽  
Richard Gejji ◽  
Sam Yeaman ◽  
Patrik Nosil
Keyword(s):  
Gene Flow ◽  
Theoretical Models ◽  
Critical Issue ◽  
Genomic Islands ◽  
Genome Wide ◽  
A Genome ◽  
Physical Linkage ◽  
Genome Divergence ◽  
Analytical Approaches ◽  
New Mutations

Theoretical models addressing genome-wide patterns of divergence during speciation are needed to help us understand the evolutionary processes generating empirical patterns. Here, we examine a critical issue concerning speciation-with-gene flow: to what degree does physical linkage ( r < 0.5) of new mutations to already diverged genes aid the build-up of genomic islands of differentiation? We used simulation and analytical approaches to partition the probability of establishment for a new divergently selected mutation when the mutation (i) is the first to arise in an undifferentiated genome (the direct effect of selection), (ii) arises unlinked to any selected loci ( r = 0.5), but within a genome that has some already diverged genes (the effect of genome-wide reductions in gene flow for facilitating divergence, which we term ‘genome hitchhiking’), and (iii) arises in physical linkage to a diverged locus (divergence hitchhiking). We find that the strength of selection acting directly on a new mutation is generally the most important predictor for establishment, with divergence and genomic hitchhiking having smaller effects. We outline the specific conditions under which divergence and genome hitchhiking can aid mutation establishment. The results generate predictions about genome divergence at different points in the speciation process and avenues for further work.

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