Determining why convergent traits use distinct versus shared genetic components is crucial for understanding how evolutionary processes generate and sustain biodiversity. However, the factors dictating the genetic underpinnings of convergent traits remain incompletely understood. Here, we use heterologous protein expression, biochemical assays, and phylogenetic analyses to confirm the origin of a luciferase gene from haloalkane dehalogenases in the brittle star Amphiura filiformis. Through database searches and gene tree analyses, we also show a complex pattern of the presence and absence of haloalkane dehalogenases across organismal genomes. These results first confirm parallel evolution across a vast phylogenetic distance, because octocorals like Renilla also use luciferase derived from haloalkane dehalogenases. This parallel evolution is surprising, even though previously hypothesized, because many organisms that also use coelenterazine as the bioluminescence substrate evolved completely distinct luciferases. The inability to detect haloalkane dehalogenases in the genomes of several bioluminescent groups suggests that the distribution of this gene family influences its recruitment as a luciferase. Together, our findings highlight how biochemical function and genomic availability help determine whether distinct or shared genetic components are used during the convergent evolution of traits like bioluminescence.

Biology of Marine Organisms and Biomimetics Unit Biosciences Research Institute University of Mons 7000 Mons Belgium

Centre for Life's Origins and Evolution Department of Genetics Evolution and Environment University College London London UK

Department of Biological Engineering University of California Santa Barbara Santa Barbara CA 93106 USA

Department of Chemical Engineering University of California Santa Barbara Santa Barbara CA 93106 USA

Department of Chemistry University of California Santa Barbara Santa Barbara CA 93106 USA

Department of Ecology Evolution and Marine Biology University of California Santa Barbara Santa Barbara CA 93106 USA

Department of Zoology University of Cambridge Cambridge CB2 1TN UK

International Clinical Research Center St Anne's University Hospital Brno 656 91 Brno Czech Republic

Laboratory of Cellular and Molecular Immunology GIGA Research Institute University of Liège 4000 Liège Belgium

Loschmidt Laboratories Department of Experimental Biology and RECETOX Faculty of Science Masaryk University 625 00 Brno Czech Republic

Neuroscience Research Institute University of California Santa Barbara Santa Barbara CA 93106 USA

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bioRxiv. 2024 Oct 17:2024.10.14.618359. doi: 10.1101/2024.10.14.618359. PubMed

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