Trends in Genetics
Volume 31, Issue 9, September 2015, Pages 491-499
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Review
The genomics of organismal diversification illuminated by adaptive radiations

https://doi.org/10.1016/j.tig.2015.07.002Get rights and content

Highlights

  • We review progress in understanding adaptive radiation based on genomic approaches.

  • Features of genome architecture promoting diversification have not been identified.

  • Access to ancient genetic variation emerges as a key driver of diversification.

  • Convergent evolution facilitates the detection of adaptation genes.

Adaptive radiation is the rapid and extensive ecological diversification of an organismal lineage to generate both phenotypic disparity (divergence) and similarity (convergence). Demonstrating particularly clear evidence of the power of natural selection, adaptive radiations serve as outstanding systems for studying the mechanisms of evolution. We review how the first wave of genomic investigation across major archetypal adaptive radiations has started to shed light on the molecular basis of adaptive diversification. Notably, these efforts have not yet identified consistent features of genomic architecture that promote diversification. However, access to a pool of ancient adaptive variation via genetic exchange emerges as an important driver of adaptive radiation. We conclude by highlighting avenues for future research on adaptive radiations, including the discovery of ‘adaptation genes’ based on genome scans using replicate convergent populations.

Section snippets

Outbursts of life

In adaptive radiation and in every part of the whole, wonderful history of life, all the modes and all the factors of evolution are inextricably interwoven. The total process cannot be made simple, but it can be analyzed in part. (G.G. Simpson, 1953 [1])

The history of life is a cumulative story of evolutionary radiations (see Glossary); such outbursts of unprecedented forms are thought to be responsible for much of the extant and extinct organismal diversity on Earth 1, 2, 3, 4. For example,

Key elements of ARs

AR is defined as the rapid diversification of an organismal lineage into an array of closely related species as a consequence of adaptation to different ecological niches 1, 2, 3 (a more comprehensive characterization is provided in Box 1). Closer inspection of such bouts of diversification reveals two important elements. The first is the generation of unique, distinct phenotypes specialized to different ecological niches – divergent evolution. This aspect of diversification is epitomized by

Genomic determinants of AR

It has long been recognized that the question why some groups of organisms diversify more extensively than others is tightly connected to the pivotal concept of ecological opportunity: ARs are triggered by access to novel or hitherto under-utilized ecological niches 1, 2, 12, sometimes in combination with sexual selection [22]. The answer to the question about the determinants of organismal diversification is thus partly ecological and also includes historical contingency 14, 23, but will

The genetic basis of phenotypic divergence in ARs

Ever since G.G. Simpson [1] emphasized the importance of ‘distinctive new adaptive types’ in triggering adaptive radiation, the identification of such evolutionary (key) innovations has been a major focus of adaptive radiation research. With progress in molecular genetic tools, emphasis has partly shifted to investigations of the molecular basis of adaptive divergence – an endeavor of course not restricted to ARs. The promise is to gain a general understanding of several longstanding issues in

Concluding remarks

In this review we have described the potential of molecular investigations in ARs to improve our understanding of the mechanisms underlying biological diversification. One of the major insights that has emerged is that rapid and extensive diversification and convergent evolution is facilitated by the diffusion of ancient adaptive variation, thus blurring the distinction between incomplete lineage sorting, standing genetic variation, and gene flow via introgressive hybridization. Certainly, a

Acknowledgments

We thank the Editor R. Macrae for the invitation and for comments; C. Jiggins plus an anonymous reviewer and the members of the laboratory of W.S. for discussion and comments on the manuscript; and J. Losos for providing photographs. This work was supported, in part, from grants from the Swiss National Science Foundation (SNF) to D.B. and W.S., and from the European Research Council (ERC, CoG ‘CICHLID∼X’) to W.S.

Glossary

Divergence mapping
marker-based search for genome regions exhibiting exceptionally strong differentiation (typically quantified by the fixation index FST) between ecologically-different populations as a consequence of divergent natural selection on specific loci.
dN/dS ratio
index combining the frequency of non-synonymous (i.e., amino acid changing) and synonymous (i.e., not amino acid changing) nucleotide substitutions across a gene to explore the type of selection that has acted on the gene.

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