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Review
. 2009 Jun 16;106 Suppl 1(Suppl 1):9939-46.
doi: 10.1073/pnas.0901397106. Epub 2009 Jun 15.

Natural selection in action during speciation

Sara Via  1
Affiliations
Review

Natural selection in action during speciation

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

Abstract

The role of natural selection in speciation, first described by Darwin, has finally been widely accepted. Yet, the nature and time course of the genetic changes that result in speciation remain mysterious. To date, genetic analyses of speciation have focused almost exclusively on retrospective analyses of reproductive isolation between species or subspecies and on hybrid sterility or inviability rather than on ecologically based barriers to gene flow. However, if we are to fully understand the origin of species, we must analyze the process from additional vantage points. By studying the genetic causes of partial reproductive isolation between specialized ecological races, early barriers to gene flow can be identified before they become confounded with other species differences. This population-level approach can reveal patterns that become invisible over time, such as the mosaic nature of the genome early in speciation. Under divergent selection in sympatry, the genomes of incipient species become temporary genetic mosaics in which ecologically important genomic regions resist gene exchange, even as gene flow continues over most of the genome. Analysis of such mosaic genomes suggests that surprisingly large genomic regions around divergently selected quantitative trait loci can be protected from interrace recombination by "divergence hitchhiking." Here, I describe the formation of the genetic mosaic during early ecological speciation, consider the establishment, effects, and transitory nature of divergence hitchhiking around key ecologically important genes, and describe a 2-stage model for genetic divergence during ecological speciation with gene flow.

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Conflict of interest statement

The author declares no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Two ways to study the process of speciation, which is visualized here as a continuum of divergence from a variable population to a divergent pair of populations, and on through the evolution of intrinsic barriers to gene flow to the recognition of good species. (A) Using the spyglass, the process is studied by attempting to look back to see the details of speciation from the vantage point of the present. (B) Using the magnifying glass, the mechanisms of reproductive isolation are studied in partially isolated divergent ecotypes that are used as models of an early stage of speciation.
Fig. 2.
Fig. 2.
Gene flow between sympatric populations does not necessarily prevent differentiation. (A) The simple vision of gene flow as a homogenizing force in populations. Free migration and random mating between locally adapted populations is simplistically visualized as homogenizing populations and eradicating local adaptation. (B) Ecologically based barriers to gene flow that evolve under divergent selection permit genetically based phenotypic divergence under selection to be maintained in the face of gene flow: habitat choice reduces migration, then selection against migrants, F1, and QTL recombinants reduces introgression of locally adapted alleles, maintaining divergence.
Fig. 3.
Fig. 3.
A diagram version of genomic heterogeneity of gene exchange and genetic divergence under divergent selection. One chromosome from each specialized parental population is shown, with the genomic regions that contain locally adapted genes (QTL) indicated in boxes. The color of each QTL corresponds to the specialized parent from which it came. Bidirectional arrows indicate gene exchange, with the color of the arrow tips showing that alleles from the other population are introgressing. Gene exchange can occur outside the regions containing the specialized genes, but is blocked from occurring within those regions for the reasons shown in Fig. 2B. This heterogeneous pattern of gene exchange under selection establishes the genetic mosaic of speciation in which genetic divergence is restricted to divergently selected portions of the genomes, whereas other regions share polymorphisms freely through ongoing gene exchange.
Fig. 4.
Fig. 4.
The relationship between the Fst values of amplified fragment length polymorphism markers, and their map distance from the nearest QTL involved in reproductive isolation between pea aphids on alfalfa and red clover. Fst outliers are shown as solid circles, and the dotted line at 10.6 cM marks the average distance from an outlier to the nearest QTL. The pink triangles are the predicted values from a logistic regression of the probability that a marker was an outlier on its distance to the nearest QTL. [Figure has been modified and reproduced with permission from ref. (2008, Wiley-Blackwell, Oxford, United Kingdom).]
Fig. 5.
Fig. 5.
Two views of how to delineate regions of divergence hitchhiking. (A) A region of divergence hitchhiking around several QTL is defined by the region covered by a cluster of Fst outliers. (B) Each outlier is within a separate hitchhiking region, bounded by a low Fst marker. Outliers are thought to be either under direct divergent selection or tightly linked to a selected gene. The double-pointed arrows show the hypothesized extent of divergence hitchhiking. Stars denote Fst outliers and circles denote markers with Fst in the expected range. Boxes show the map location of QTL under divergent selection, color-coded by the trait they affect, and with box size corresponding to effect size. Dashed lines either mark the boundaries of the hitchhiking region (A), or connect the Fst values of adjacent markers (B).
Fig. 6.
Fig. 6.
Visualizing the pattern of genetic divergence during ecological speciation. (A) The 2 stages of ecological speciation with gene flow. Stage 1 is noted by the blue arrow, and stage 2 is indicated by the green arrow. Events during each stage are as described in the text. (B) Diagram of gene trees within a species tree for ecological speciation with gene flow. Each gene is polymorphic in the original population, with a frequency (p) as noted on the axis at the left of the drawing. As time goes on, some loci quickly diverge at about the same time under divergent selection. The gene frequency at a given locus is shown as a dotted line before it diverges between the incipient species (at the time marked by the symbols), and then as a solid line. Red symbols are selected QTL, and blue symbols are divergence hitchhikers. This divergence is mostly complete by the end of stage 1. During stage 2, a handful of additional loci diverge under divergent selection (red), and loci that were unaffected by divergent selection diverge by independent responses to uniform or balancing selection or by drift (brown symbols). (C) Gene trees in a species tree under allopatry. Symbols are as in B. The heavy dashed line indicates a geographical barrier to gene flow. If an allopatric population enters a new environment, there may be a period of rapid response to divergent selection similar to stage 1 in A. Otherwise, as shown here, genes diverge over a long time period under any combination of divergent selection, independent responses to uniform or balancing selection, or drift, eventually all coming into concordance to produce the branching pattern of the new species.
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References

    1. Darwin C. On the Origin of Species by Means of Natural Selection or the Preservation of Favored Races in the Struggle for Life. London: J. Murray; 1859. - PMC - PubMed
    1. Coyne JA, Orr HA. Speciation. Sunderland, MA: Sinauer; 2004.
    1. Via S, West JA. The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol Ecol. 2008;17:4334–4345. - PubMed
    1. Schluter D. Ecology and the origin of species. Trends Ecol Evol. 2001;16:372–380. - PubMed
    1. Schluter D. Evidence for ecological speciation and its alternative. Science. 2009;323:737–741. - PubMed

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