W. Leo Smith

Resolution of ray-finned fish phylogeny and timing of diversification

Ray-finned fishes make up half of all living vertebrate species. Nearly all ray-finned fishes are teleosts, which include most commercially important fish species, several model organisms for genomics and developmental biology, and the dominant component of marine and freshwater vertebrate faunas. Despite the economic and scientific importance of ray-finned fishes, the lack of a single comprehensive phylogeny with corresponding divergence-time estimates has limited our understanding of the evolution and diversification of this radiation. Our analyses, which use multiple nuclear gene sequences in conjunction with 36 fossil age constraints, result in a well-supported phylogeny of all major ray-finned fish lineages and molecular age estimates that are generally consistent with the fossil record. This phylogeny informs three long-standing problems: specifically identifying elopomorphs (eels and tarpons) as the sister lineage of all other teleosts, providing a unique hypothesis on the radiation of early euteleosts, and offering a promising strategy for resolution of the “bush at the top of the tree” that includes percomorphs and other spiny-finned teleosts. Contrasting our divergence time estimates with studies using a single nuclear gene or whole mitochondrial genomes, we find that the former underestimates ages of the oldest ray-finned fish divergences, but the latter dramatically overestimates ages for derived teleost lineages. Our time-calibrated phylogeny reveals that much of the diversification leading to extant groups of teleosts occurred between the late Mesozoic and early Cenozoic, identifying this period as the “Second Age of Fishes.”

Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes

Spiny-rayed fishes, or acanthomorphs, comprise nearly one-third of all living vertebrates. Despite their dominant role in aquatic ecosystems, the evolutionary history and tempo of acanthomorph diversification is poorly understood. We investigate the pattern of lineage diversification in acanthomorphs by using a well-resolved time-calibrated phylogeny inferred from a nuclear gene supermatrix that includes 520 acanthomorph species and 37 fossil age constraints. This phylogeny provides resolution for what has been classically referred to as the “bush at the top” of the teleost tree, and indicates acanthomorphs originated in the Early Cretaceous. Paleontological evidence suggests acanthomorphs exhibit a pulse of morphological diversification following the end Cretaceous mass extinction; however, the role of this event on the accumulation of living acanthomorph diversity remains unclear. Lineage diversification rates through time exhibit no shifts associated with the end Cretaceous mass extinction, but there is a global decrease in lineage diversification rates 50 Ma that occurs during a period when morphological disparity among fossil acanthomorphs increases sharply. Analysis of clade-specific shifts in diversification rates reveal that the hyperdiversity of living acanthomorphs is highlighted by several rapidly radiating lineages including tunas, gobies, blennies, snailfishes, and Afro-American cichlids. These lineages with high diversification rates are not associated with a single habitat type, such as coral reefs, indicating there is no single explanation for the success of acanthomorphs, as exceptional bouts of diversification have occurred across a wide array of marine and freshwater habitats.

The Covert World of Fish Biofluorescence: A Phylogenetically Widespread and Phenotypically Variable Phenomenon

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.

Repeated and Widespread Evolution of Bioluminescence in Marine Fishes

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.

Is sexual selection driving diversification of the bioluminescent ponyfishes (Teleostei: Leiognathidae)?

Sexual selection may facilitate genetic isolation among populations and result in increased rates of diversification. As a mechanism driving diversification, sexual selection has been invoked and upheld in numerous empirical studies across disparate taxa, including birds, plants and spiders. In this study, we investigate the potential impact of sexual selection on the tempo and mode of ponyfish evolution. Ponyfishes (Leiognathidae) are bioluminescent marine fishes that exhibit sexually dimorphic features of their unique light‐organ system (LOS). Although sexual selection is widely considered to be the driving force behind ponyfish speciation, this hypothesis has never been formally tested. Given that some leiognathid species have a sexually dimorphic LOS, whereas others do not, this family provides an excellent system within which to study the potential role of sexual selection in diversification and morphological differentiation. In this study, we estimate the phylogenetic relationships and divergence times for Leiognathidae, investigate the tempo and mode of ponyfish diversification, and explore morphological shape disparity among leiognathid clades. We recover strong support for a monophyletic Leiognathidae and estimate that all major ponyfish lineages evolved during the Paleogene. Our studies of ponyfish diversification demonstrate that there is no conclusive evidence that sexually dimorphic clades are significantly more species rich than nonsexually dimorphic lineages and that evidence is lacking to support any significant diversification rate increases within ponyfishes. Further, we detected a lineage‐through‐time signal indicating that ponyfishes have continuously diversified through time, which is in contrast to many recent diversification studies that identify lineage‐through‐time patterns that support mechanisms of density‐dependent speciation. Additionally, there is no evidence of sexual selection hindering morphological diversity, as sexually dimorphic taxa are shown to be more disparate in overall shape morphology than nonsexually dimorphic taxa. Our results suggest that if sexual selection is occurring in ponyfish evolution, it is likely acting only as a genetic isolating mechanism that has allowed ponyfishes to continuously diversify over time, with no overall impact on increases in diversification rate or morphological disparity.

The origins of adipose fins: an analysis of homoplasy and the serial homology of vertebrate appendages.

Adipose fins are appendages found on the dorsal midline between the dorsal and caudal fins in more than 6000 living species of teleost fishes. It has been consistently argued that adipose fins evolved once and have been lost repeatedly across teleosts owing to limited function. Here, we demonstrate that adipose fins originated repeatedly by using phylogenetic and anatomical evidence. This suggests that adipose fins are adaptive, although their function remains undetermined. To test for generalities in the evolution of form in de novo vertebrate fins, we studied the skeletal anatomy of adipose fins across 620 species belonging to 186 genera and 55 families. Adipose fins have repeatedly evolved endoskeletal plates, anterior dermal spines and fin rays. The repeated evolution of fin rays in adipose fins suggests that these fins can evolve new tissue types and increased structural complexity by expressing fin-associated developmental modules in these new territories. Patterns of skeletal elaboration differ between the various occurrences of adipose fins and challenge prevailing hypotheses for vertebrate fin origin. Adipose fins represent a powerful and, thus far, barely studied model for exploring the evolution of vertebrate limbs and the roles of adaptation and generative biases in morphological evolution.

Phylogeny and taxonomy of sculpins, sandfishes, and snailfishes (Perciformes: Cottoidei) with comments on the phylogenetic significance of their early-life-history specializations.

Despite recent progress on the higher-level relationships of the Cottoidei and its familial components, phylogenetic conflict and uncertainty remain within the Cottoidea. We analyzed a dataset composed of 4518 molecular (mitochondrial 12S, tRNA-Val, 16S, and cytochrome b and nuclear TMO-4c4, Histone H3, and 28S) and 72 morphological characters for 69 terminals to address cottoid intrarelationships. The resulting well-resolved phylogeny was used to produce a revised taxonomy that is consistent with the available molecular and morphological data and recognizes six families: Agonidae, Cottidae, Jordaniidae, Psychrolutidae, Rhamphocottidae, and Scorpaenichthyidae. The traditional Agonidae was expanded to include traditional hemitripterids and Hemilepidotus. The traditional Cottidae was restricted to Leptocottus, Trachidermus, and the riverine, lacustrine, and Lake Baikal freshwater cottoids. Jordaniidae (Jordania and Paricelinus) was separated from the traditional cottids; Psychrolutidae was expanded from the traditional grouping to include nearly all traditional marine cottids and the single species of bathylutichthyid. Rhamphocottidae was expanded to include the traditional ereuniids, and Scorpaenichthyidae separated Scorpaenichthys from the traditional cottids. The importance of early-life-history characters to the resulting phylogeny and taxonomy were highlighted.

Biofluorescence in Catsharks (Scyliorhinidae): Fundamental Description and Relevance for Elasmobranch Visual Ecology

Biofluorescence has recently been found to be widespread in marine fishes, including sharks. Catsharks, such as the Swell Shark (Cephaloscyllium ventriosum) from the eastern Pacific and the Chain Catshark (Scyliorhinus retifer) from the western Atlantic, are known to exhibit bright green fluorescence. We examined the spectral sensitivity and visual characteristics of these reclusive sharks, while also considering the fluorescent properties of their skin. Spectral absorbance of the photoreceptor cells in these sharks revealed the presence of a single visual pigment in each species. Cephaloscyllium ventriosum exhibited a maximum absorbance of 484 ± 3 nm and an absorbance range at half maximum (λ1/2max) of 440–540 nm, whereas for S. retifer maximum absorbance was 488 ± 3 nm with the same absorbance range. Using the photoreceptor properties derived here, a “shark eye” camera was designed and developed that yielded contrast information on areas where fluorescence is anatomically distributed on the shark, as seen from other sharks’ eyes of these two species. Phylogenetic investigations indicate that biofluorescence has evolved at least three times in cartilaginous fishes. The repeated evolution of biofluorescence in elasmobranchs, coupled with a visual adaptation to detect it; and evidence that biofluorescence creates greater luminosity contrast with the surrounding background, highlights the potential importance of biofluorescence in elasmobranch behavior and biology.

Mitochondrial Intergenic Spacer in Fairy Basslets (Serranidae: Anthiinae) and the Simultaneous Analysis of Nucleotide and Rearrangement Data

Abstract We present the results of a study that implements a recently developed phylogenetic algorithm that combines fixed-states nucleotide optimization with breakpoint analysis to identify and examine the evolution of a mitochondrial intergenic spacer between the tRNAVal and 16S rRNA loci in a clade of fairy basslets (Serranidae: Anthiinae). The results of the analysis indicate that this spacer evolved once and that it may be increasing in size through evolutionary time. The resulting molecular hypothesis corroborates much of the previous morphological phylogenetic work.

Morphology and evolution of bioluminescent organs in the glowbellies (Percomorpha: Acropomatidae) with comments on the taxonomy and phylogeny of Acropomatiformes

Bioluminescent organs have evolved many times within teleost fishes and exhibit a wide range of complexity and anatomical derivation. Although some bioluminescent organs have been studied in detail, the morphology of the bacterial light organs in glowbellies (Acropoma) is largely unknown. This study describes the anatomy of the bioluminescent organs in Hanedas Glowbelly (Acropoma hanedai) and the Glowbelly (Acropoma japonicum) and places the evolution of this light‐producing system in the context of a new phylogeny of glowbellies and their relatives. Gross and histological examination of the bioluminescent organs indicate that they are derived from perianal ectodermal tissue, likely originating from the developmental proctodeum, contrary to at least one prior suggestion that the bioluminescent organ in Acropoma is of endodermal intestinal derivation. Additionally, anterior bioluminescent organ development in both species is associated with lateral spreading of the bacteria‐containing arms of the bioluminescent organ from an initial median structure. In the context of a 16‐gene molecular phylogeny, the bioluminescent organ in Acropoma is shown to have evolved within the Acropomatidae in the ancestor of Acropoma. Further, ancestral‐states reconstruction demonstrates that the bioluminescent organs in Acropoma evolved independently from the light organs in related howellid and epigonid taxa which have esophageal or intestinally derived bioluminescent organs. Across the acropomatiforms, our reconstructions indicate that bioluminescent organs evolved independently four or five times. Based on the inferred phylogeny of the order where Acropoma and Doederleinia were separated from other traditional acropomatids, the familial taxonomy of the Acropomatidae was modified such that the previously described Malakichthyidae and Synagropidae were recognized. We also morphologically diagnose and describe the family Lateolabracidae.