Gene flow, linked selection, and divergent sorting of ancient polymorphism shape genomic divergence landscape in a group of edaphic specialists

2021 ◽  
Author(s):  
Fushi Ke ◽  
Liette Vasseur ◽  
Huiqin Yi ◽  
Lihua Yang ◽  
Xiao Wei ◽  
...  
Nature ◽  
2020 ◽  
Vol 588 (7836) ◽  
pp. 106-111 ◽  
Author(s):  
Andreas F. Kautt ◽  
Claudius F. Kratochwil ◽  
Alexander Nater ◽  
Gonzalo Machado-Schiaffino ◽  
Melisa Olave ◽  
...  

AbstractThe transition from ‘well-marked varieties’ of a single species into ‘well-defined species’—especially in the absence of geographic barriers to gene flow (sympatric speciation)—has puzzled evolutionary biologists ever since Darwin1,2. Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process3. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs4, but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories5. Here, within a young species complex of neotropical cichlid fishes (Amphilophus spp.), we analysed genomic divergence among populations and species. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry.


2017 ◽  
Vol 115 (2) ◽  
pp. E236-E243 ◽  
Author(s):  
Tao Ma ◽  
Kun Wang ◽  
Quanjun Hu ◽  
Zhenxiang Xi ◽  
Dongshi Wan ◽  
...  

How genome divergence eventually leads to speciation is a topic of prime evolutionary interest. Genomic islands of elevated divergence are frequently reported between diverging lineages, and their size is expected to increase with time and gene flow under the speciation-with-gene-flow model. However, such islands can also result from divergent sorting of ancient polymorphisms, recent ecological selection regardless of gene flow, and/or recurrent background selection and selective sweeps in low-recombination regions. It is challenging to disentangle these nonexclusive alternatives, but here we attempt to do this in an analysis of what drove genomic divergence between four lineages comprising a species complex of desert poplar trees. Within this complex we found that two morphologically delimited species, Populus euphratica and Populus pruinosa, were paraphyletic while the four lineages exhibited contrasting levels of gene flow and divergence times, providing a good system for testing hypotheses on the origin of divergence islands. We show that the size and number of genomic islands that distinguish lineages are not associated with either rate of recent gene flow or time of divergence. Instead, they are most likely derived from divergent sorting of ancient polymorphisms and divergence hitchhiking. We found that highly diverged genes under lineage-specific selection and putatively involved in ecological and morphological divergence occur both within and outside these islands. Our results highlight the need to incorporate demography, absolute divergence measurement, and gene flow rate to explain the formation of genomic islands and to identify potential genomic regions involved in speciation.


2019 ◽  
Author(s):  
Claudio S. Quilodrán ◽  
Kristen Ruegg ◽  
Ashley T. Sendell-Price ◽  
Eric Anderson ◽  
Tim Coulson ◽  
...  

Abstract1. The way that organisms diverge into reproductively isolated species is a major question in biology. The recent accumulation of genomic data provides promising opportunities to understand the genomic landscape of divergence, which describes the distribution of differences across genomes. Genomic areas of unusually high differentiation have been called genomic islands of divergence. Their formation has been attributed to a variety of mechanisms, but a prominent hypothesis is that they result from divergent selection over a small portion of the genome, with surrounding areas homogenised by gene flow. Such islands have often been interpreted as being associated with divergence with gene flow. However other mechanisms related to genetic architecture and population history can also contribute to the formation of genomic islands of divergence.2. We currently lack a quantitative framework to examine the dynamics of genomic landscapes under the complex and nuanced conditions that are found in natural systems. Here, we develop an individual-based simulation to explore the dynamics of diverging genomes under various scenarios of gene flow, selection and genotype-phenotype maps.3. Our modelling results are consistent with empirical observations demonstrating the formation of genomic islands under genetic isolation. Importantly, we have quantified the range of conditions that produce genomic islands. We demonstrate that the initial level of genetic diversity, drift, time since divergence, linkage disequilibrium, strength of selection and gene flow are all important factors that can influence the formation of genomic islands. Because the accumulation of genomic differentiation over time tends to erode the signal of genomic islands, genomic islands are more likely to be observed in recently divergent taxa, although not all recently diverged taxa will necessarily exhibit islands of genomic divergence. Gene flow primarily slows the swamping of islands of divergence with time.4. By using this framework, further studies may explore the relative influence of particular suites of events that contribute to the emergence of genomic islands under sympatric, parapatric and allopatric conditions. This approach represents a novel tool to explore quantitative expectations of the speciation process, and should prove useful in elucidating past and projecting future genomic evolution of any taxa.


2011 ◽  
Vol 29 (1) ◽  
pp. 279-291 ◽  
Author(s):  
D. Weetman ◽  
C. S. Wilding ◽  
K. Steen ◽  
J. Pinto ◽  
M. J. Donnelly

2016 ◽  
Vol 33 (7) ◽  
pp. 1754-1767 ◽  
Author(s):  
Jing Wang ◽  
Nathaniel R. Street ◽  
Douglas G. Scofield ◽  
Pär K. Ingvarsson

2020 ◽  
Author(s):  
Steven M. Van Belleghem ◽  
Jared M. Cole ◽  
Gabriela Montejo-Kovacevich ◽  
Caroline N. Bacquet ◽  
W. Owen McMillan ◽  
...  

AbstractCharacterizing the genetic architecture of species boundaries remains a difficult task. Hybridizing species provide a powerful system to identify the factors that shape genomic variation and, ultimately, identify the regions of the genome that maintain species boundaries. Unfortunately, complex histories of isolation, admixture and selection can generate heterogenous genomic landscapes of divergence which make inferences about the regions that are responsible for species boundaries problematic. However, as the signal of admixture and selection on genomic loci varies with recombination rate, their relationship can be used to infer their relative importance during speciation. Here, we explore patterns of genomic divergence, admixture and recombination rate among hybridizing lineages across the Heliconius erato radiation. We focus on the incipient species, H. erato and H. himera, and distinguish the processes that drive genomic divergence across three contact zones where they frequently hybridize. Using demographic modeling and simulations, we infer that periods of isolation and selection have been major causes of genome-wide correlation patterns between recombination rate and divergence between these incipient species. Upon secondary contact, we found surprisingly highly asymmetrical introgression between the species pair, with a paucity of H. erato alleles introgressing into the H. himera genomes. We suggest that this signal may result from a current polygenic species boundary between the hybridizing lineages. These results contribute to a growing appreciation for the importance of polygenic architectures of species boundaries and pervasive genome-wide selection during the early stages of speciation with gene flow.


Evolution ◽  
2013 ◽  
Vol 67 (9) ◽  
pp. 2577-2591 ◽  
Author(s):  
Samuel M. Flaxman ◽  
Jeffrey L. Feder ◽  
Patrik Nosil

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