Heterogeneous genome divergence, differential introgression, and the origin and structure of hybrid zones

Harrison, Richard G.; Larson, Erica L.

doi:10.1111/mec.13582

Cited by 198 publications

(226 citation statements)

References 111 publications

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“…The genomes of incompletely isolated species and locally adapted populations have long been thought of as mosaics of regions with high and low divergence (31,32). This pattern is due in part to variation in effective gene flow along the genome, created by an interaction of divergent selection and recombination (33,34).…”

Section: Discussionmentioning

confidence: 99%

Population-genomic inference of the strength and timing of selection against gene flow

Aeschbacher

Selby

Willis

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

117

122

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The interplay of divergent selection and gene flow is key to understanding how populations adapt to local environments and how new species form. Here, we use DNA polymorphism data and genome-wide variation in recombination rate to jointly infer the strength and timing of selection, as well as the baseline level of gene flow under various demographic scenarios. We model how divergent selection leads to a genome-wide negative correlation between recombination rate and genetic differentiation among populations. Our theory shows that the selection density (i.e., the selection coefficient per base pair) is a key parameter underlying this relationship. We then develop a procedure for parameter estimation that accounts for the confounding effect of background selection. Applying this method to two datasets from Mimulus guttatus, we infer a strong signal of adaptive divergence in the face of gene flow between populations growing on and off phytotoxic serpentine soils. However, the genome-wide intensity of this selection is not exceptional compared with what M. guttatus populations may typically experience when adapting to local conditions. We also find that selection against genomewide introgression from the selfing sister species M. nasutus has acted to maintain a barrier between these two species over at least the last 250 ky. Our study provides a theoretical framework for linking genome-wide patterns of divergence and recombination with the underlying evolutionary mechanisms that drive this differentiation.speciation with gene flow | local adaptation | recombination | divergence | Mimulus E stimating the timing and strength of divergent selection is fundamental to understanding the evolution and persistence of organismal diversity (1-3). Genes underlying local adaptation and speciation act as barriers to gene flow, such that genetic divergence around these loci is higher compared with the rest of the genome. However, a framework that explicitly links observable patterns of DNA polymorphism with the underlying evolutionary mechanisms and allows for robust parameter inference has so far been missing (4).One way of studying adaptive genomic divergence in the face of gene flow is to apply methods for demographic inference to scenarios of speciation (e.g., refs. 5 and 6). This approach allows dating population splits and inferring the presence or absence of gene flow, yet generally does not explicitly account for natural selection (but see ref. 7). Another approach is to scan genomes for loci that are statistical outliers of divergence among populations. These scans are used to identify candidate loci underlying speciation or local adaptation (e.g., refs. 8 and 9) and include the search for so-called genomic islands of divergence (e.g., ref. 10) (i.e., extended genomic regions of elevated divergence). Methods of this type can be confounded by other modes of selection, as well as demography, and will always propose a biased subset of candidate loci (11,12).A third approach is to test for a negative correlation between abso...

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Section: Discussionmentioning

confidence: 99%

Population-genomic inference of the strength and timing of selection against gene flow

Aeschbacher

Selby

Willis

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

117

122

View full text Add to dashboard Cite

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“…It is too early to speculate if these regions also contain genes of importance for reproductive isolation. However, investigating the genome‐wide pattern of differentiation for a much larger set of nuclear markers and investigating the genomic admixture proportions in birds with intermediate phenotypes will give a chance to identify regions that show elevated differentiation and assess if those have appeared as a result of restricted gene flow in particular genomic regions or as a consequence of adaptation to different habitats during separation (Harrison & Larson, 2016; Wolf & Ellegren, 2016). …”

Section: Discussionmentioning

confidence: 99%

Patterns of genetic, phenotypic, and acoustic variation across a chiffchaff (Phylloscopus collybita abietinus/tristis) hybrid zone

Shipilina

Serbyn

Иваницкий

et al. 2017

Ecology and Evolution

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Characterizing patterns of evolution of genetic and phenotypic divergence between incipient species is essential to understand how evolution of reproductive isolation proceeds. Hybrid zones are excellent for studying such processes, as they provide opportunities to assess trait variation in individuals with mixed genetic background and to quantify gene flow across different genomic regions. Here, we combine plumage, song, mtDNA and whole‐genome sequence data and analyze variation across a sympatric zone between the European and the Siberian chiffchaff (Phylloscopus collybita abietinus/tristis) to study how gene exchange between the lineages affects trait variation. Our results show that chiffchaff within the sympatric region show more extensive trait variation than allopatric birds, with a large proportion of individuals exhibiting intermediate phenotypic characters. The genomic differentiation between the subspecies is lower in sympatry than in allopatry and sympatric birds have a mix of genetic ancestry indicating extensive ongoing and past gene flow. Patterns of phenotypic and genetic variation also vary between regions within the hybrid zone, potentially reflecting differences in population densities, age of secondary contact, or differences in mate recognition or mate preference. The genomic data support the presence of two distinct genetic clades corresponding to allopatric abietinus and tristis and that genetic admixture is the force underlying trait variation in the sympatric region—the previously described subspecies (“fulvescens”) from the region is therefore not likely a distinct taxon. In addition, we conclude that subspecies identification based on appearance is uncertain as an individual with an apparently distinct phenotype can have a considerable proportion of the genome composed of mixed alleles, or even a major part of the genome introgressed from the other subspecies. Our results provide insights into the dynamics of admixture across subspecies boundaries and have implications for understanding speciation processes and for the identification of specific chiffchaff individuals based on phenotypic characters.

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“…Hybrid zones, regions where two genetically distinct populations interbreed, are excellent natural laboratories to explore these locus-specific patterns of introgression (Hewitt 1988;Harrison 1990;Harrison and Larson 2016), especially in combination with the application of geographical cline theory (Barton and Hewitt 1985). Cline theory provides a framework to analyse changes in traits or allele frequencies as a function of geographic distance across a hybrid zone transect.…”

Section: Genomic Clines In Hybrid Zonesmentioning

confidence: 99%

Avian introgression in the genomic era

et al. 2017

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Introgression, the incorporation of genetic material from one (sub)species into the gene pool of another by means of hybridization and backcrossing, is a common phenomenon in birds and can provide important insights into the speciation process. In the last decade, the toolkit for studying introgression has expanded together with the development of molecular markers. In this review, we explore how genomic data, the most recent step in this methodological progress, impacts different aspects in the study of avian introgression. First, the detection of hybrids and backcrosses has improved dramatically. The most widely used software package is STRUCTURE. Phylogenetic discordance (i.e. different loci resulting in discordant gene trees) is another means for the detection of introgression, although it should be regarded as a starting point for further analyses, not as a definitive proof of introgression. Specifically, disentangling introgression from other biological processes, such as incomplete lineage sorting, remains a challenging endeavour, although new techniques, such as the D-statistic, are being developed. In addition, phylogenetics might require a shift from trees to networks. Second, the study of hybrid zones by means of geographical or genomic cline analysis has led to important insights into the complex interplay between hybridization and speciation. However, because each hybrid zone study is just a single snapshot of a complex and continuously changing interaction, hybrid zones should be studied across different temporal and/or spatial scales. A third powerful tool is the genome scan. The debate on which evolutionary processes underlie the genomic landscape is still ongoing, as is the question whether loci involved in reproductive isolation cluster together in 'islands of speciation' or whether they are scattered throughout the genome. Exploring genomic landscapes across the avian tree of life will be an exciting field for further research. Finally, the findings from these different methods should be incorporated into specific speciation scenarios, which can consequently be tested using a modelling approach. All in all, this genomic perspective on avian hybridization and speciation will further our understanding in evolution in general.

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Heterogeneous genome divergence, differential introgression, and the origin and structure of hybrid zones

Cited by 198 publications

References 111 publications

Population-genomic inference of the strength and timing of selection against gene flow

Population-genomic inference of the strength and timing of selection against gene flow

Patterns of genetic, phenotypic, and acoustic variation across a chiffchaff (Phylloscopus collybita abietinus/tristis) hybrid zone

Avian introgression in the genomic era

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