Speciation is a central and fundamental process in evolution that concerns the origin of reproductive isolation. The latest generation of genomic approaches provide remarkable opportunities to describe speciation and to learn about its underlying mechanisms.
Genome scans, which can now be carried out in a truly genome-wide scale and at base-pair resolution, reveal substantial genomic divergence among incipient species even in the face of gene flow and show that there is extensive genomic heterogeneity in the extent of differentiation, especially at early stages of speciation, both in sympatry and in allopatry.
The sources of this heterogeneity remain incompletely understood. The combination of genome scans with sophisticated population genetic modelling, quantitative trait locus mapping, admixture analyses and ecology has the potential to distinguish the influence of selection from demographic, historical and structural effects and to link these sources of genomic divergence to phenotypes and to reproductive isolation.
Available empirical data suggest that differentiation between parapatric populations can be restricted to few genomic islands, whereas incipient species that coexist in sympatry show differentiation that is widely distributed across the genome. This suggests that genomically widespread selection is required to permit the maintenance and perhaps the build-up of genetic differentiation in sympatry.
Recent genomic studies reveal that the genetic basis of reproductive isolation is often complex. The effects of pleiotropy, genetic correlations and patterns of recombination need to be considered alongside effects of ecological and sexual selection as well as genomic conflict.
A surprising recent discovery is the re-use of ancient genetic variants in speciation, which are acquired either from standing genetic variation or by introgressive hybridization.
In this Review, we propose a 'roadmap' for the development of speciation genomics towards answering classical and emerging questions in speciation research.
Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly important aspect of this research field. We review current understanding of genome-wide effects of accumulating reproductive isolation and of genomic properties that influence the process of speciation. Building on this work, we identify emergent trends and gaps in our understanding, propose new approaches to more fully integrate genomics into speciation research, translate speciation theory into hypotheses that are testable using genomic tools and provide an integrative definition of the field of speciation genomics.
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The authors thank the European Science Foundation networking programme Frontiers in Speciation Research (FroSpects) for funding a workshop on Genetics and Genomics of Speciation and for contributing towards travel expenses for graduate students, and N. Pepe and L. Greuter for help with the organization of the workshop. They thank C. Lexer and two anonymous reviewers for suggestions that improved this Review.
The authors declare no competing financial interests.
- Reproductive isolation
The absence or restriction of gene flow between populations beyond that caused by spatial separation.
- Gene flow
The movement of alleles between populations. For gene flow to occur, individuals must disperse between populations and successfully reproduce with local individuals. Therefore, gene flow can be reduced not only by dispersal barriers but also by either intrinsic or extrinsic reproductive isolation.
- Speciation genomics
The field of speciation research that addresses the influence of genomic properties on the evolution of reproductive barriers and the signatures of speciation processes that are observable in genomic patterns (for example, processes of diversity and divergence). Its aim is a conceptual and methodological integration of genomic approaches with other empirical and theoretical speciation research.
- Effect sizes
The magnitude of the influence of a locus or a specific allele on a phenotypic trait. This can be expressed, for example, as the proportion of phenotypic variation due to a specific locus or as the phenotypic difference between genotypes with and without a specific allele.
Effect of an allele on more than one trait.
- Divergent selection
Selection that favours different phenotypes in different populations.
- Extrinsic reproductive isolation
Fitness reduction in hybrids that is dependent on the environment and that is mediated by genotype–environment interactions.
- Genomic conflict
Conflict that arises between genes or genetic elements within the same genome either when they are not transmitted by the same rules (for example, biparental versus uniparental inheritance) or when a gene causes its own transmission to the detriment of the rest of the genome. The presence of elements that bias transmission (that is, distorter loci) is expected to lead to the evolution of loci that restore Mendelian segregation (that is, restorer loci).
- Intrinsic reproductive isolation
Fitness reduction in hybrids that is independent of the environment.
- Ecological speciation
The evolution of reproductive isolation as a consequence of divergent or disruptive natural selection between populations that inhabit different environments or exploit different resources.
- Postzygotic isolation
Effects of barriers that act after fertilization, such as hybrid sterility and hybrid inviability. It can be either extrinsic (that is, mediated by the environment) or intrinsic.
- Disruptive selection
Selection within a single population that favours extreme phenotypes over intermediate phenotypes.
- Sexual isolation
Reproductive isolation due to reduced mating between members of divergent populations, including behavioural assortative mate choice and assortative fertilization in animals, as well as pollinator-mediated assortative mating in plants. It is most often thought of as prezygotic but can also be postzygotic if there is disruptive sexual selection.
- FST-outlier analyses
The comparison of the distribution of FST values across loci with the distribution expected in the absence of divergent selection for the same average differentiation. A locus with an FST value that exceeds expectation is likely to be influenced by divergent selection, either on the locus itself or on a linked locus.
- Prezygotic isolation
Effect of barriers that act before or after mating but before fertilization, including the isolating effects of divergent mate choice, habitat preference, reproductive timing and gametic incompatibility.
- Bateson–Dobzhansky–Muller incompatibilities
(BDMI). Intrinsic postmating barriers that are the result of epistatic interactions between alleles at two or more loci that reduce fitness in hybrids but not in the parental populations.
Heterozygotic inferiority; that is, the phenotype expressed in heterozygotes has lower fitness than that of either homozygote. This can cause disruptive selection.
- Meiotic drivers
Factors that distort Mendelian segregation. At a heterozygous site, the driving variant will be found in more than half of the gametes.
- Sexual conflict
The evolution of phenotypic characteristics by sexual selection when the trait confers a fitness benefit on one sex but a fitness cost on the other.
Mating between individuals that belong to distinct species or populations. If postmating isolation is incomplete, hybridization leads to the introgression of genes from one population to another.
- Linkage disequilibrium
The statistical association of the alleles at two loci within gametes in a population. Although linkage disequilibrium tends to be greater between linked loci, it can also arise between physically unlinked loci (for example, because of selection, nonrandom mating or gene flow).
- Distorter loci
Loci that underlie meiotic drive, which is the non-Mendelian segregation of alleles in meiosis. Distorter loci may act on other loci, so-called responder loci.
- Responder loci
Loci that show deviations from Mendelian segregation (that is, meiotic drive) owing to the effect of distorter loci.
- Speciation continuum
Variation of the strength of reproductive isolation between two incipient species either in different locations or in different species pairs that belong to the same evolutionary lineage and that diverge in similar ways.
- Genome scan
Comparison of genome-wide patterns of diversity within populations and/or divergence between populations at hundreds or thousands of markers. Until recently, most studies used amplified fragment length polymorphisms (AFLPs) but this has recently changed, and single-nucleotide polymorphisms (SNPs) generated by next-generation sequencing or SNP chips are being used.
- Divergence hitchhiking
When divergent selection on a locus reduces the effective migration rate for physically linked regions, which increases the opportunity for divergence at loci under weaker selection in the surrounding regions. Regions of divergence hitchhiking may remain much larger than those of traditional hitchhiking after a selective sweep within populations because of the persistent reduction in the ability of flanking regions to recombine away from a divergently selected gene.
Pertaining to organisms, populations or species that inhabit either adjacent geographical regions or spatially distinct but adjacent habitats and that may exchange genes.
Pertaining to organisms, populations or species that share the same geographical region and that overlap in their use of space with no spatial barriers to gene exchange.
- F ST
(Also known as Wright's fixation index). A measure of population subdivision that compares the correlation between two gene copies that are randomly drawn from the same population to that between two gene copies that are drawn from two different populations. An FST of 1 indicates that two populations are fixed for alternative alleles.
Pertaining to organisms, populations or species that inhabit distinct geographical regions and are therefore not exchanging genes.
The merging of two genetic lineages in a common ancestor.
- Incomplete lineage sorting
The situation in which some alleles share a more recent common ancestor with alleles in another species than with other alleles in the same species.
Increases in frequencies of alleles and closely linked chromosomal segments due to positive selection. Sweeps initially reduce variation and subsequently lead to a local excess of rare alleles as new unique mutations accumulate.
- D xy
The average number of nucleotide substitutions per site between two populations.
- Secondary contact
The meeting of the distribution ranges of two distinct populations or species after a period of evolutionary divergence in geographical isolation (that is, allopatry).
- Gene-flow–selection balance
A level of differentiation between subpopulations at which the homogenizing effect of gene flow and the differentiating effect of divergent selection are in equilibrium.
Pertaining to divergent selection that acts on multiple traits.
Directional variation in phenotype or genotype, or change in frequency (for example, of an allele) across a geographical region.
A statistical framework for the analysis of genetic data, in which the alleles that are shared by populations or species are traced back in time to their most recent common ancestor.
- Quantitative trait locus
(QTL). A chromosomal region that has a significant effect on a phenotype.
- Admixture mapping
The identification of genetic loci that contribute to phenotypic differences between ancestral populations by investigating genotype–phenotype correlations in a population of mixed ancestry.
- Standing genetic variation
Allelic variation that is currently segregating within a population, as opposed to alleles that arise through new mutation events.
- Introgressive hybridization
The introduction of genes from one population or species into another through hybridization.
The situation in which a mutation or a variant has achieved a frequency of 100% in a population.
A zone in which there is a transition between two distinct biological communities, for example, between forest and grassland or between aquatic and terrestrial habitats. It is typically associated with changes in the physical environment.
Selection for the strengthening of prezygotic barriers to avoid the production of unfit hybrids between taxa that have previously evolved some postzygotic isolation.
- One-allele mechanisms
Mechanisms that produce reproductive barriers through the spread of the same allele in each of two diverging populations, such as alleles for behavioural imprinting or reduced migration.
- Two-allele mechanisms
Mechanisms that produce reproductive barriers through the spread of different alleles at the same locus in two diverging populations, such as alleles for different habitat or mating preferences.
- Hybrid zones
Spatially restricted regions where the distribution ranges of distinct populations or incipient species come into contact and where hybrids are formed.
The additive genetic variance–covariance matrix that summarizes the variance within and the covariance between multiple phenotypic traits.
- Correlational selection
Selection for optimal combinations of characteristics.
- Transgressive phenotypes
Phenotypes in hybrids that exceed the range of phenotypes that are observed in the parental taxa.
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Seehausen, O., Butlin, R., Keller, I. et al. Genomics and the origin of species. Nat Rev Genet 15, 176–192 (2014). https://doi.org/10.1038/nrg3644
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