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  • Review Article
  • Published:

Making sense of genomic islands of differentiation in light of speciation

Nature Reviews Genetics volume 18, pages 87–100 (2017)Cite this article

Subjects

Key Points

  • The genomic landscape of differentiation between diverging lineages is often heterogeneous, with 'islands' of elevated differentiation previously interpreted as 'speciation islands' under a model of speciation with gene flow.

  • Alternative processes can generate heterogeneous differentiation landscapes; notable processes include linked selection, variable recombination rates and/or density of targets of selection.

  • Genome scans for regions of elevated differentiation should be based on whole-genome re-sequencing of individually tagged samples with reads mapped to a reference genome assembly.

  • When designing speciation genomic studies, attention should be paid to the possibility of sampling across the speciation continuum and from replicate population pairs, and to the demography of the studied population, including potential gene flow.

  • Analyses of sequence data in speciation genomic studies should incorporate a suite of summary statistics.

  • The field is likely to move forward as a result of an increased use of long-read sequencing technology, the identification of structural variation, the inclusion of recombination rate data and, ultimately, functional studies.

Abstract

As populations diverge, genetic differences accumulate across the genome. Spurred by rapid developments in sequencing technology, genome-wide population surveys of natural populations promise insights into the evolutionary processes and the genetic basis underlying speciation. Although genomic regions of elevated differentiation are the focus of searches for 'speciation genes', there is an increasing realization that such genomic signatures can also arise by alternative processes that are not related to population divergence, such as linked selection. In this Review, we explore methodological trends in speciation genomic studies, highlight the difficulty in separating processes related to speciation from those emerging from genome-wide properties that are not related to reproductive isolation, and provide a set of suggestions for future work in this area.

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Figure 1: A schematic of alternative processes that generate regional genomic islands of elevated differentiation.
Figure 2: A summary of central aspects of our literature survey on speciation genomic studies.

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Acknowledgements

The authors are grateful to members of their laboratory groups and to many external visitors for years of stimulating discussions on the subject. Their research is supported by the European Research Council, the Swedish Research Council, and the Knut and Alice Wallenberg Foundation.

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Authors and Affiliations

  1. Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, Uppsala, SE-752 36, Sweden

    Jochen B. W. Wolf & Hans Ellegren

  2. Department of Biology II, Section of Evolutionary Biology, Ludwig Maximilian University of Munich, Grosshaderner Strasse 2, Planegg-Martinsried, 82152, Germany

    Jochen B. W. Wolf

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  1. Jochen B. W. Wolf
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Correspondence to Jochen B. W. Wolf or Hans Ellegren.

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Supplementary information

Supplementary information S1 (table)

A Compilation of a literature survey including 67 studies drawn from searching the ISI Web of Knowledge database for terms 'speciation genomics', 'islands of differentiation', 'islands of speciation' and 'speciation with gene flow', and complemented with other references. (XLSX 29 kb)

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Glossary

Postzygotic intrinsic isolation

Lowered hybrid fitness in the form of sterility or reduced viability of zygotes that are produced in a cross between two groups of individuals, often two species.

Gene flow

Movement of chromosomes (or chromosomal regions) across genetically structured populations, resulting in a change of allele frequencies.

Reproductive isolation

Any mechanism or process that reduces the probability of mating, survival or reproduction between members of different groups and their offspring.

Genetic drift

Random change in allele frequencies between generations as a consequence of stochastic sampling in a finite population.

Background selection

Change in allele frequencies and reduction in diversity at neutral loci as a result of selection against deleterious alleles at linked loci.

Genetic draft

Also known as genetic hitch-hiking. Pervasive reduction of genetic diversity owing to recurrent selective sweeps.

Divergent selection

Natural selection for different trait values in diverging lineages.

Disruptive selection

A special case of divergent selection in which natural selection favours two extreme values of a phenotypic distribution.

Meiotic drive

A mechanism of segregation distortion during female meiosis in which one allele at a locus is transmitted to the offspring (gametes) more often than are other alleles, even in the absence of a selective advantage of that allele.

Centromeric drive

A special case of meiotic drive involving centromeres that are in evolutionary conflict to increase their odds of transmission during asymmetric (female) meiosis.

Introgression

The transfer of genetic information (gene flow) between divergent populations or species as a result of hybridization and repeated backcrossing.

Good species

Well-separated lineages that clearly form distinct species and no longer interbreed.

Magic traits

Traits that are subjected to divergent selection and contribute to non-random mating; they facilitate speciation with gene flow.

Supergenes

Clusters of tightly linked loci where two or more haplotypes give distinctly different phenotypes.

F ST

A common statistical measure of genetic differentiation between populations that compares the variance in allele frequencies between populations to the variance within populations. It is sensitive to genetic drift, demographic change, mutation, migration and genetic variation of each population.

Linked selection

Selection that changes allele frequencies, often leading to reduced diversity, at loci genetically linked to the focal locus.

Effective population sizes

(Ne). A somewhat abstract population genetic measure of the size of an idealized population in which the strength of genetic drift is the same as that in the population of interest.

Time to the most recent common ancestor

In genetic genealogy, the time, in years or generations, to the most recent individual from whom all individuals in the sample under consideration descended.

Hybrid zones

Narrow geographical regions where two species or divergent populations are found in close proximity and hybridize.

Epistatic interactions

The interaction between two or more genes that causes a phenotype to be dependent on the particular combination of alleles at these loci.

Coalescent times

The most recent time-point in the past at which two gene copies share a common ancestor.

Structural genetic variation

Polymorphisms involving differences in the length, orientation, order, copy number or chromosomal organization of DNA sequences.

Quantitative trait loci

(QTLs). Genomic regions that are statistically associated with non-discrete variation in a phenotypic trait.

Isolation-by-ecology

Genome-wide differentiation between groups of individuals according to environmental or phenotypic contrasts between populations (rather than, for example, according to geographical distance).

Spatial autocorrelation

Genetic similarities that are attributable to geographical proximity between populations.

Lineage sorting

The process by which alleles segregating in the common ancestor converge to the overall phylogeny of diverging lineages.

Backcrosses

Crosses between hybrids and one of the parents or a genetically similar individual from the parental population.

ABBA-BABA tests

A type of statistical test for introgression.

Admixture analyses

Tests for introgression of alleles between hybridizing populations to establish individual ancestries of individuals and/or genomic regions.

Isolation-with-migration

The process of population divergence in the presence of gene flow.

Population bottlenecks

Sharp reductions in the size of a population.

Reduced-representation data

Genetic data from a defined subset of the genome.

Linkage disequilibrium

The non-random, statistical association between alleles at different loci.

Underdominance

Fitness reduction of heterozygous genotypes at a bi-allelic locus.

Long-read technology

Sequencing technologies that generate relatively long stretches of DNA sequence per read. The recent development of long-single-molecule sequencing (>20 kb) blurs the initial dichotomy of short reads (from sequencing-by-synthesis technology) versus long reads (∼1 kb Sanger reads).

Optical mapping

A technique for constructing high-resolution restriction maps from single molecules.

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Wolf, J., Ellegren, H. Making sense of genomic islands of differentiation in light of speciation. Nat Rev Genet 18, 87–100 (2017). https://doi.org/10.1038/nrg.2016.133

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