The covert world of fish biofluorescence: a phylogenetically widespread and phenotypically variable phenomenon

Abstract

The discovery of fluorescent proteins has revolutionized experimental biology. Whereas the majority of fluorescent proteins have been identified from cnidarians, recently several fluorescent proteins have been isolated across the animal tree of life. Here we show that biofluorescence is not only phylogenetically widespread, but is also phenotypically variable across both cartilaginous and bony fishes, highlighting its evolutionary history and the possibility for discovery of numerous novel fluorescent proteins. Fish biofluorescence is especially common and morphologically variable in cryptically patterned coral-reef lineages. We identified 16 orders, 50 families, 105 genera, and more than 180 species of biofluorescent fishes. We have also reconstructed our current understanding of the phylogenetic distribution of biofluorescence for ray-finned fishes. The presence of yellow long-pass intraocular filters in many biofluorescent fish lineages and the substantive color vision capabilities of coral-reef fishes suggest that they are capable of detecting fluoresced light. We present species-specific emission patterns among closely related species, indicating that biofluorescence potentially functions in intraspecific communication and evidence that fluorescence can be used for camouflage. This research provides insight into the distribution, evolution, and phenotypic variability of biofluorescence in marine lineages and examines the role this variation may play.

Figure 1. Diversity of fluorescent patterns and colors in marine fishes.

A, swell shark (Cephaloscyllium ventriosum); B, ray (Urobatis jamaicensis); C, sole (Soleichthys heterorhinos); D, flathead (Cociella hutchinsi); E, lizardfish (Synodus dermatogenys); F, frogfish (Antennarius maculatus); G, false stonefish (Scorpaenopsis diabolus); H, false moray eel (Kaupichthys brachychirus); I, false moray eel (Kaupichthys nuchalis); J, pipefish (Corythoichthys haematopterus); K, sand stargazer (Gillellus uranidea); L, goby (Eviota sp.); M, goby (Eviota atriventris); N, surgeonfish (Acanthurus coeruleus, larval); O, threadfin bream (Scolopsis bilineata).

Figure 2. Observed occurrences of green and red fluorescent emissions indicate the evolution of biofluorescence is widespread across the evolutionary history of ray-finned fishes (Actinopterygii).

Family-level tree showing evolutionary relationships of ray-finned fishes inferred from maximum likelihood analysis of 221 species and six (one mitochondrial, five nuclear) genes. Note: Not all biofluorescent lineages are shown due to sampling limitations (see Table S1, Fig. S1).

Figure 3

Top panel: Interspecific variation in fluorescent emission pattern (from top: lateral, ventral, and dorsal views) in two congeneric and sympatric members of the lizardfish genus Synodus. A, S. synodus. B, S. saurus. Bottom panel: Interspecific variation in coloration and pigmentation pattern under white light (top: lateral; bottom: dorsal) in same two congeneric and sympatric members of the lizardfish genus Synodus. A, S. synodus. B, S. saurus.

Figure 4. Plot of emission spectra for representative green and red fluorescing marine fishes, also showing the spectra for enhanced green fluorescent protein (eGFP) for comparison.

Key to species sampled: Ray (family Urotrygonidae, genus Urobatis); Eel (family Chlopsidae, genus Kaupichthys); Scorpionfish (family Scorpaenidae, genus Scorpeana); Goby (family Gobiidae, genus Eviota).

Figure 5. Images of reef fishes fluorescing in their natural habitat captured with a Red Epic video camera at night in the Solomon Islands.

(A) A red fluorescing scorpionfish, Scorpaenopsis papuensis, perched on red fluorescing algae. (B) A green fluorescing nemipterid (bream), Scolopsis bilineata, near a green fluorescing Acropora sp. coralhead.