Repeated and Widespread Evolution of Bioluminescence in Marine Fishes.

Matthew P. Davis,John S. Sparks,W. Leo Smith,Erik V. Thuesen

doi:10.1371/journal.pone.0155154

Matthew P. Davis, John S. Sparks + Show 2 more

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https://doi.org/10.1371/journal.pone.0155154

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Abstract

Bioluminescence is primarily a marine phenomenon with 80% of metazoan bioluminescent genera occurring in the world’s oceans. Here we show that bioluminescence has evolved repeatedly and is phylogenetically widespread across ray-finned fishes. We recover 27 independent evolutionary events of bioluminescence, all among marine fish lineages. This finding indicates that bioluminescence has evolved many more times than previously hypothesized across fishes and the tree of life. Our exploration of the macroevolutionary patterns of bioluminescent lineages indicates that the present day diversity of some inshore and deep-sea bioluminescent fish lineages that use bioluminescence for communication, feeding, and reproduction exhibit exceptional species richness given clade age. We show that exceptional species richness occurs particularly in deep-sea fishes with intrinsic bioluminescent systems and both shallow water and deep-sea lineages with luminescent systems used for communication.

Highlights

Bioluminescence, the production and emission of light from a living organism, is a fascinating phenomenon that is documented in over 700 genera of metazoans across the tree of life, with the vast majority living in the ocean [1,2,3]
Previous survey studies [1,2] have identified bioluminescence in 11 orders of marine fishes; the phylogeny and classification of fishes has changed considerably since these previous studies, and the authors of these earlier studies did not investigate this phenomenon in a phylogenetic framework, identify independent evolutionary events of bioluminescence, or explore macroevolutionary patterns of bioluminescent lineages
We further examine whether any bioluminescent lineages of ray-finned fishes exhibit exceptional species richness given their clade age for taxa living both in the deep sea, where there are few obvious physical barriers to reproduction, and shallow water habitats, to provide a roadmap for future macroevolutionary work

Summary

Introduction

Bioluminescence, the production and emission of light from a living organism, is a fascinating phenomenon that is documented in over 700 genera of metazoans across the tree of life, with the vast majority living in the ocean [1,2,3]. Bioluminescence has evolved in cartilaginous (Chondrichthyes) [1,2,3,4] and ray-finned fishes (Actinopterygii) [1,2,3], and it is not observed in any lobe-finned fishes or tetrapods (Sarcopterygii). Broad studies of bioluminescence have typically counted fishes as a single evolutionary event among the 40 independent higher-level evolutionary events of bioluminescence documented across the tree of life [2,3]; a focused study of the bioluminescent ray-finned fishes is critical to determine the number and identity of bioluminescent fish clades.

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