Review
A Combinatorial View on Speciation and Adaptive Radiation

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Highlights

Recent studies show that cases of rapid speciation and rapid species radiations often involve old genetic variants that arose long before the speciation events.

Old genetic variation, previously tested by selection and occurring at higher allele frequency than new mutations, is a good substrate for speciation.

Admixture variation from divergent lineages may be particularly important, potentially causing intrinsic and extrinsic incompatibilities, transgressive traits, or novel trait combinations in hybrid populations.

We review the evidence for rapid speciation involving a ‘combinatorial mechanism’ – the reassembly of old genetic variants into novel combinations.

This genetic mechanism might not only facilitate rapid speciation but also adaptive radiation and sympatric speciation, and it might contribute to variation in speciation rates among lineages.

Speciation is often thought of as a slow process due to the waiting times for mutations that cause incompatibilities, and permit ecological differentiation or assortative mating. Cases of rapid speciation and particularly cases of rapid adaptive radiation into multiple sympatric species have remained somewhat mysterious. We review recent findings from speciation genomics that reveal an emerging commonality among such cases: reassembly of old genetic variation into new combinations facilitating rapid speciation and adaptive radiation. The polymorphisms in old variants frequently originated from hybridization at some point in the past. We discuss why old variants are particularly good fuel for rapid speciation, and hypothesize that variation in access to such old variants might contribute to the large variation in speciation rates observed in nature.

Section snippets

Speciation Genomics Reveals an Important Role of Old Genetic Variants

The population genomics of speciation, ‘speciation genomics’, is a flourishing area of enquiry with much potential to address some of the big questions in speciation biology. The first generation of speciation genomics studies generated several new insights, but it is becoming clear that we are only beginning to understand the genomic basis of speciation. With the exception of a much improved understanding of the nature of genomic islands of differentiation and their link to speciation 1, 2,

The Problem: Rapid Speciation, but Slow Mutation

Many lineages accumulate species diversity at the relatively slow pace of a few new species every few million years [3]. However, some lineages appear inherently prone to rapid speciation and species radiations 4, 5, 6, 7. This leads to dramatic variation in speciation rates among lineages, and thus to highly imbalanced phylogenetic patterns of species richness [8]. Some cichlid fishes (Cichlidae) [9], some postglacial freshwater fishes (e.g., Salmonidae 10, 11), Darwin’s finches [12],

The Data: Ancient Genetic Variation Fuels Much More Recent Speciation Events

A key to understanding rapid speciation might lie in asking which loci best reflect the speciation process and in reconstructing the source of variation in these genes. Inherent to the idea of ‘speciation genes’ was a close link between the evolutionary history of alleles causing reproductive isolation [2], namely their mutational origin, and the speciation process, in other words the evolution of reproductive isolation between populations. That evolutionary history differs markedly among loci

A Combinatorial View on the Genetics of Speciation

The recent speciation genomic findings exemplified by case studies in Table 1 conflict with standard speciation models (Box 1) in many of which the origin of alleles involved in speciation marks the beginning of the speciation process. In the studies we highlight, new species evolved through new combinations of old alleles (Table 1 and Table S1 in the supplemental information online). Such a pattern is expected under an alternative set of speciation models, including recombinational speciation

Old Genetic Variation in Standing or Admixture Variation

Old genetic variation – divergent haplotypes combined into the same gene pool by hybridization or that are present as standing variation – might be a particularly good substrate for speciation compared with haplotypes that are gradually building from new mutations (Box 2). Standing genetic variation and admixture variation can represent two ends of a continuum, particularly if admixture took place in the more distant past. Similarly, in a metapopulation context, it is arbitrary whether

Admixture Variation Is a Particularly Good Substrate for Speciation

We predict that old genetic variation derived from recent hybridization (‘admixture variation’) will be more powerful than standing genetic variation in facilitating rapid speciation and species radiations. We summarize the major reasons below. All apply to speciation in general, but for rapid speciation and rapid species radiations they are likely to be particularly important.

Implications

Speciation via a combinatorial mechanism has many implications. One consequence is the decoupling of the speciation process from the slow rate of accumulation of mutations relevant to phenotypic differentiation and reproductive isolation (Figure 2 and Box 1). A second consequence is the facilitation of the evolution of linkage disequilibrium between genes even in the face of gene flow, and with it the partial alleviation of constraints to speciation imposed by sympatry [88]. Thereby, a

Concluding Remarks

Speciation through combinatorial mechanisms, by which new combinations of old gene variants quickly generate reproductively isolated species, offers a perspective on speciation that contrasts with the gradual growth of reproductive isolation through accumulation of differences generated by de novo mutations. Such a mechanism has the potential to explain how speciation can sometimes be very fast, and how multiple new species can arise nearly simultaneously and can persist in sympatry very soon

Glossary

Adaptive radiation from a hybrid swarm
several ecologically differentiated species evolve from a single hybrid population, wherein admixture variation not only facilitates adaptation to a variety of new niches but importantly also reproductive isolation among the emerging species.
Balancing selection
a selective process by which two or more alleles are maintained in the gene pool of a population at frequencies larger than expected under neutrality. Mechanisms include negative frequency-dependent

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