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Rapid radiation in a diverse marine environment

Rapid radiation in a diverse marine environment

Significance

Adaptive radiation, which is the evolution process by which a lineage diversifies in a short amount of time, often occurs where colonizing species meet unoccupied niches or reduced selective pressures. Although rapid radiations may occur in complex and diverse environments, these cases are not well documented. We show that the hamlets, which are a group of Caribbean reef fishes have radiated in the last 10,000 years in a burst that ranks among the most rapid in fishes. Genomic analysis indicates that color pattern diversity may be caused by different combinations of alleles at very few genes. This modular genomic architecture for diversification is emerging as a common factor in a variety of radiations.

Abstract

Rapid diversification can often be observed when new species invade habitats that offer ecological opportunities for adaptive radiation. Most of the Earth’s diversity was created in diverse environments with limited ecological opportunities. This is a striking example of rapid radiation in a marine habitat that is rich in diversity. The hamlets, which are a group of reef fishes originating from the Caribbean, have radiated into an astonishing diversity of color patterns, but show low divergence across all other ecological axes. The hamlet’s lineage is 26 Mys in age, but the radiation occurred in the last 10,000 generations in an explosion of diversification that ranks amongst fishes’ fastest. The hamlets are a compelling context to reveal the genomic elements involved in phenotypic diversification. They also offer an excellent opportunity for building a comparative framework that will allow us to understand the drivers and consequences of adaptive radiation. An analysis of 170 genomes revealed that color pattern diversity is caused by different combinations of alleles at just a few large-effect loci. This modular genomic architecture of diversity has been previously documented in HeliconiusThree other tropical radiations occurred in extremely diverse and complex environments. The hamlet radiation occurred in a context with a large effective population size, which is typical for marine populations. This allows for the accumulation and retention of genetic variation through mutation, which are both important in this radiation.

Footnotes

    • Accepted November 18, 2021
  • Author contributions: K.H.., M.H.., W.O.M., and O.P. K.H., M.H. and O.P. conceived research. K.H.M.H., O.P., and O.P. conducted research Analyzed data; K.H. M.H. W.O.M. and O.P. The paper was written.

  • The authors declare that they have no competing interests.

  • This article is a PNAS Direct Submission.

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

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