Rapid radiation in a very diverse marine environment

Importance

Adaptive radiation, the evolutionary process by which a lineage diversifies over a short period of time, often occurs in geographically isolated or newly formed habitats where colonizing species encounter unoccupied niches and reduced selective pressures. Rapid radiation can also occur in diverse and complex environments, but these cases are less well documented. Here we show that hamlets, a group of Caribbean reef fishes, have radiated over the past 10,000 generations in a burst of diversification that ranks among the fastest growing fish. Genomic analysis suggests that the diversity of color patterns is generated by different combinations of alleles on a few genes with a large effect. Such a modular genomic architecture of diversification appears as a common denominator to a variety of radiations.

Summary

Rapid diversification is often seen when founding species invade isolated or newly formed habitats that provide an ecological opportunity for adaptive radiation. However, most of Earth’s diversity has arisen in diverse environments where ecological opportunities appear to be more limited. Here we present a vivid example of rapid radiation in a highly diverse marine habitat. Hamlets, a group of wider Caribbean reef fishes, radiated in an astonishing diversity of color patterns, but showed little divergence on other ecological axes. Although the Hamlet lineage is about 26 Ma old, the radiation appears to have occurred over the last 10,000 generations in a spurt of diversification that ranks among the fastest in fish. As such, hamlets provide a compelling backdrop for uncovering the genomic elements associated with phenotypic diversification and an excellent opportunity to construct a broader comparative framework for understanding the drivers of adaptive radiation. Analysis of 170 genomes suggests that the diversity of color patterns is generated by different combinations of alleles at a few high-effect loci. Such a modular genomic architecture of diversification has already been documented in Heliconius butterflies, capuchino finches and munia finches, three other tropical radiations that took place in very diverse and complex environments. The radiation from the hamlet also occurred in a context of high effective population size, typical of marine populations. This allows the accumulation of new variants by mutation and the retention of ancestral genetic variation, both of which appear to be important in this radiation.

Footnotes

    • Accepted November 18, 2021.
  • Author contributions: research designed by KH, MH, WOM and OP; KH, MH and OP conducted research; KH, MH and OP analyzed the data; and KH, MH, WOM and OP wrote the article.

  • The authors declare no competing interests.

  • This article is a direct PNAS submission.

  • This article contains additional information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2020457119/-/DCSupplemental.

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