Repeated and Widespread Evolution of Bioluminescence in Marine Fishes

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.

Fig 1. Evolution of Bioluminescence across Ray-Finned Fishes.

Evolutionary relationships and divergence times of ray-finned fishes inferred from 11 gene fragments. Letters at nodes correspond to clades indicated in Fig 4. Branch colors indicate the presence of bioluminescence and whether the mechanism of bioluminescence is intrinsic, bacterially mediated, or unknown. Examples of bioluminescent ray-finned fishes include the A: midshipman (Porichthys: intrinsic), and B: flashlight fish (Anomalops: bacterially mediated).

Fig 2. Evolutionary Relationships and Divergence Times of Ray-Finned Fishes Inferred from Eleven Gene Fragments.

Numbers at nodes correspond to ancestral-character-state-reconstruction distributions of the evolution of bioluminescence indicated in Fig 3. Blue branches and taxa labels indicate the presence of bioluminescence, all of which occur in marine habitats. Green taxa labels indicate additional marine taxa. Pink labels indicate lineages with marine and freshwater taxa, and white labels indicate lineages that are predominantly found in freshwater habitats.

Fig 3. Ancestral-Character Evolution of Bioluminescence in Sixteen Major Lineages of Fishes.

Bayesian ancestral-character-states reconstruction of bioluminescence across a distribution of 500 trees that resulted from the Bayesian inference of divergence times. Each rectangle includes 500 individual reconstructions across this distribution of 500 trees. Blue indicates the presence of bioluminescence and black indicates absence.

Fig 4. Patterns of Diversification across Ray-Finned Fishes and Bioluminescent Lineages.

Temporal hypothesis of the relationships of ray-finned fishes with net diversification rates and relative rates of extinction estimated by MEDUSA. Species richness curves indicate the 95 percent confidence interval for the expected number of species given clade age given a net diversification rate and relative rate of extinction. Letters indicate bioluminescent lineages of fishes in Fig 1.