Evolutionary relationships of anglerfishes (Lophiiformes) reconstructed using ultraconserved elements.

The macroevolutionary consequences of evolving in the deep-sea remain poorly understood and are compounded by the fact that convergent adaptations for living in this environment makes elucidating phylogenetic relationships difficult. Lophiiform anglerfishes exhibit extreme habitat and predatory specializations, including the use of a fin-spine system as a luring device and unique reproductive strategies where parasitic males attach and fuse to females. Despite their notoriety for these odd characteristics, evolutionary relationships among these fishes remain unclear. We sought to clarify the evolutionary history of Lophiiformes using data from 1000 ultraconserved elements and phylogenomic inference methods with particular interest paid to the Ceratioidei (deep-sea anglerfishes) and Antennarioidei (frogfishes and handfishes). At the suborder level, we recovered similar topologies in separate phylogenomic analyses: The Lophioidei (monkfishes) are the sister group to the rest of the Lophiiformes, Ogcocephaloidei (batfishes) and Antennarioidei (frogfishes) form a sister group, and Chaunacioidei (coffinfishes) and Ceratioidei (deep-sea anglerfishes) form a clade. The relationships we recover within the ceratioids disagree with most previous phylogenetic investigations, which used legacy phylogenetic markers or morphology. We recovered non-monophyletic relationships in the Antennarioidei and proposed three new families based on molecular and morphological evidence: Histiophrynidae, Rhycheridae, and Tathicarpidae. Antennariidae was re-evaluated to include what was known as Antennariinae, but not Histiophryninae. Non-bifurcating signal in splits network analysis indicated reticulations among and within suborders, supporting the complicated history of the Lophiiformes previously found with morphological data. Although we resolve relationships within Antennarioidei, Ceratioidei relationships remain somewhat unclear without better taxonomic sampling.

High postural costs and anaerobic metabolism during swimming support the hypothesis of a U-shaped metabolism-speed curve in fishes.

Swimming performance is considered a key trait determining the ability of fish to survive. Hydrodynamic theory predicts that the energetic costs required for fishes to swim should vary with speed according to a U-shaped curve, with an expected energetic minimum at intermediate cruising speeds and increasing expenditure at low and high speeds. However, to date no complete datasets have shown an energetic minimum for swimming fish at intermediate speeds rather than low speeds. To address this knowledge gap, we used a negatively buoyant fish, the clearnose skate Raja eglanteria, and took two approaches: a classic critical swimming speed protocol and a single-speed exercise and recovery procedure. We found an anaerobic component at each velocity tested. The two approaches showed U-shaped, though significantly different, speed-metabolic relationships. These results suggest that (i) postural costs, especially at low speeds, may result in J- or U-shaped metabolism-speed curves; (ii) anaerobic metabolism is involved at all swimming speeds in the clearnose skate; and (iii) critical swimming protocols might misrepresent the true costs of locomotion across speeds, at least in negatively buoyant fish.

An Intact Retroviral Gene Conserved in Spiny-Rayed Fishes for over 100 My.

We have identified a retroviral envelope gene with a complete, intact open reading frame (ORF) in 20 species of spiny-rayed fishes (Acanthomorpha). The taxonomic distribution of the gene, "percomORF", indicates insertion into the ancestral lineage >110 Ma, making it the oldest known conserved gene of viral origin in a vertebrate genome. Underscoring its ancient provenence, percomORF exists as an isolated ORF within the intron of a widely conserved host gene, with no discernible proviral sequence nearby. Despite its remarkable age, percomORF retains canonical features of a retroviral glycoprotein, and tests for selection strongly suggest cooption for a host function. Retroviral envelope genes have been coopted for a role in placentogenesis by numerous lineages of mammals, including eutherians and marsupials, representing a variety of placental structures. Therefore percomORF's presence within the group Percomorpha-unique among spiny-finned fishes in having evolved placentation and live birth-is especially intriguing.

A biorobotic model of the suction-feeding system in largemouth bass: the roles of motor program speed and hyoid kinematics.

The vast majority of ray-finned fishes capture prey through suction feeding. The basis of this behavior is the generation of subambient pressure through rapid expansion of a highly kinetic skull. Over the last four decades, results from in vivo experiments have elucidated the general relationships between morphological parameters and subambient pressure generation. Until now, however, researchers have been unable to tease apart the discrete contributions of, and complex relationships among, the musculoskeletal elements that support buccal expansion. Fortunately, over the last decade, biorobotic models have gained a foothold in comparative research and show great promise in addressing long-standing questions in vertebrate biomechanics. In this paper, we present BassBot, a biorobotic model of the head of the largemouth bass (Micropterus salmoides). BassBot incorporates a 3D acrylic plastic armature of the neurocranium, maxillary apparatus, lower jaw, hyoid, suspensorium and opercular apparatus. Programming of linear motors permits precise reproduction of live kinematic behaviors including hyoid depression and rotation, premaxillary protrusion, and lateral expansion of the suspensoria. BassBot reproduced faithful kinematic and pressure dynamics relative to live bass. We show that motor program speed has a direct relationship to subambient pressure generation. Like vertebrate muscle, the linear motors that powered kinematics were able to produce larger magnitudes of force at slower velocities and, thus, were able to accelerate linkages more quickly and generate larger magnitudes of subambient pressure. In addition, we demonstrate that disrupting the kinematic behavior of the hyoid interferes with the anterior-to-posterior expansion gradient. This resulted in a significant reduction in subambient pressure generation and pressure impulse of 51% and 64%, respectively. These results reveal the promise biorobotic models have for isolating individual parameters and assessing their role in suction feeding.

Skating by: low energetic costs of swimming in a batoid fish.

We quantify the oxygen consumption rates and cost of transport (COT) of a benthic batoid fish, the little skate, Leucoraja erinacea, at three swimming speeds. We report that this species has the lowest mass-adjusted swimming metabolic rate measured for any elasmobranch; however, this species incurs a much higher COT at approximately five times the lowest values recorded for some teleosts. In addition, because skates lack a propulsive caudal fin and could not sustain steady swimming beyond a relatively low optimum speed of 1.25 body lengths s(-1), we propose that the locomotor efficiency of benthic rajiform fishes is limited to the descending portion of a single COT-speed relationship. This renders these species poorly suited for long-distance translocation and, therefore, especially vulnerable to regional-scale environmental disturbances.

The role of an overlooked adductor muscle in the feeding mechanism of ray-finned fishes: Predictions from simulations of a deep-sea viperfish.

In a majority of ray-finned fishes (Actinopterygii), effective acquisition of food resources is predicated on rapid jaw adduction. Although the musculoskeletal architecture of the feeding system has been the subject of comparative research for many decades, individual contributions of the major adductor divisions to closing dynamics have not been elucidated. While it is understood that the dorsal divisions that arise from the head and insert on the posterior of the lower jaw are major contributors to closing dynamics, the contribution of the ventral components of the adductor system has been largely overlooked. In many ray-finned fishes, the ventral component is comprised of a single division, the Aω, that originates on an intersegmental aponeurosis of the facialis divisions and inserts on the medial face of the dentary, anterior to the Meckelian tendon. This configuration resembles a sling applied at two offset points of attachment on a third-order lever. The goal of this study was to elucidate the contributions of the Aω to jaw adduction by modeling jaw closing in the deep-sea viperfish Chauliodus sloani. To do this, we simulated adduction with a revised computational model that incorporates the geometry of the Aω. By comparing results between simulations that included and excluded Aω input, we show that the Aω adds substantially to lower-jaw adduction dynamics in C. sloani by acting as a steering motor and displacing the line of action of the dorsal facialis adductor muscles and increasing the mechanical advantage and input moment arms of the jaw lever system. We also explored the effect of the Aω on muscle dynamics and found that overall facialis muscle shortening velocities are higher and normalized force production is lower in simulations including the Aω. The net effect of these changes in muscle dynamics results in similar magnitudes of peak power in the facialis divisions between simulations, however, peak power is achieved earlier in adduction Modifications of muscle mechanics and posture result in significant increases in closing performance, including static bite force, angular velocity, and adduction time. We compare this configuration to a similar design in crocodilians and suggest that the Aω configuration and similar sling configurations across the vertebrate tree of life indicate the importance of this musculoskeletal design in feeding.

Author Correction: Remora cranial vein morphology and its functional implications for attachment.

A correction to this article has been published and is linked from the HTML version of this paper. The error has been fixed in the paper.

Skin stiffness in ray-finned fishes: Contrasting material properties between species and body regions.

The skin of aquatic vertebrates surrounds all the mechanical lineages of the body and must, therefore, play an important role in locomotion. A cross-woven collagenous dermal design has converged across several clades of vertebrates. Despite this intriguing pattern, the biomechanical role of skin in swimming fishes remains largely unknown. A direct force transmission role for fish skin has been proposed, a hypothesis that is supported by the arrangement of the connective tissues linking the skin to the axial musculature. To evaluate this direct force-transmission hypothesis, we undertook hundreds of uniaxial tensile tests on skin samples from coho salmon (Oncorhynchus kisutch), Florida pompano (Trachinotus carolinus), and red snapper (Lutjanus campechanus). To do this, we developed highly precise, low-cost, custom-built material testing units. To augment our data, we also assembled a data set of skin stiffness of four additional species of actinopterygians fishes from previously published studies. We found that stiffness varies significantly between species and that the skin of our study species was increasingly stiff along a rostrocaudal gradient. Placing our results in the context of the limited body of previous work, we found that species with lower skin stiffness exhibit shorter propulsive wavelengths and low thrust production at the caudal fin and species with higher skin stiffness possess longer propulsive wavelengths and high thrust production at the caudal fin. In addition, we found that mean collagen fiber angle was close to 50° and that fiber angle was lower in posterior samples than in anterior and midlateral samples. Taken as a whole, our mechanical and morphological results support the hypothesis that the skin functions as an important direct force-transmission device in actinopterygians whereby muscular force generated in anterior myotomes is transmitted to the posterior of the body through the increasingly stiff skin.

Remora cranial vein morphology and its functional implications for attachment.

Remora fishes adhere to, and maintain long-term, reversible attachment with, surfaces of varying roughness and compliance under wetted high-shear conditions using an adhesive disc that evolved from the dorsal fin spines typical of other fishes. Evolution of this complex hierarchical structure required extensive reorganization of the skull and fin spines, but the functional role of the soft tissues of the disc are poorly understood. Here I show that remora cranial veins are highly-modified in comparison to those of other vertebrates; they are transposed anteriorly and enlarged, and lie directly ventral to the disc on the dorsum of the cranium. Ancestrally, these veins lie inside the neurocranium, in the dura ventral to the brain, and return blood from the eyes, nares, and brain to the heart. Repositioning of these vessels to lie in contact with the ventral surface of the disc lamellae implies functional importance associated with the adhesive mechanism. The position of the anterior cardinal sinus suggests that it may aid in pressurization equilibrium during attachment by acting as a hydraulic differential.

A biorobotic adhesive disc for underwater hitchhiking inspired by the remora suckerfish.

Remoras of the ray-finned fish family Echeneidae have the remarkable ability to attach to diverse marine animals using a highly modified dorsal fin that forms an adhesive disc, which enables hitchhiking on fast-swimming hosts despite high magnitudes of fluid shear. We present the design of a biologically analogous, multimaterial biomimetic remora disc based on detailed morphological and kinematic investigations of the slender sharksucker (Echeneis naucrates). We used multimaterial three-dimensional printing techniques to fabricate the main disc structure whose stiffness spans three orders of magnitude. To incorporate structures that mimic the functionality of the remora lamellae, we fabricated carbon fiber spinules (270 µm base diameter) using laser machining techniques and attached them to soft actuator-controlled lamellae. Our biomimetic prototype can attach to different surfaces and generate considerable pull-off force-up to 340 times the weight of the disc prototype. The rigid spinules and soft material overlaying the lamellae engage with the surface when rotated, just like the discs of live remoras. The biomimetic kinematics result in significantly enhanced frictional forces across the disc on substrates of different roughness. Using our prototype, we have designed an underwater robot capable of strong adhesion and hitchhiking on a variety of surfaces (including smooth, rough, and compliant surfaces, as well as shark skin). Our results demonstrate that there is promise for the development of high-performance bioinspired robotic systems that may be used in a number of applications based on an understanding of the adhesive mechanisms used by remoras.

The complex evolutionary history of seeing red: molecular phylogeny and the evolution of an adaptive visual system in deep-sea dragonfishes (Stomiiformes: Stomiidae).

The vast majority of deep-sea fishes have retinas composed of only rod cells sensitive to only shortwave blue light, approximately 480-490 nm. A group of deep-sea dragonfishes, the loosejaws (family Stomiidae), possesses far-red emitting photophores and rhodopsins sensitive to long-wave emissions greater than 650 nm. In this study, the rhodopsin diversity within the Stomiidae is surveyed based on an analysis of rod opsin-coding sequences from representatives of 23 of the 28 genera. Using phylogenetic inference, fossil-calibrated estimates of divergence times, and a comparative approach scanning the stomiid phylogeny for shared genotypes and substitution histories, we explore the evolution and timing of spectral tuning in the family. Our results challenge both the monophyly of the family Stomiidae and the loosejaws. Despite paraphyly of the loosejaws, we infer for the first time that far-red visual systems have a single evolutionary origin within the family and that this shift in phenotype occurred at approximately 15.4 Ma. In addition, we found strong evidence that at approximately 11.2 Ma the most recent common ancestor of two dragonfish genera reverted to a primitive shortwave visual system during its evolution from a far-red sensitive dragonfish. According to branch-site tests for adaptive evolution, we hypothesize that positive selection may be driving spectral tuning in the Stomiidae. These results indicate that the evolutionary history of visual systems in deep-sea species is complex and a more thorough understanding of this system requires an integrative comparative approach.

Comparative innervation of cephalic photophores of the loosejaw dragonfishes (Teleostei: Stomiiformes: Stomiidae): evidence for parallel evolution of long-wave bioluminescence.

Four genera of the teleost family Stomiidae, the loosejaw dragonfishes, possess accessory cephalic photophores (AOs). Species of three genera, Aristostomias, Malacosteus, and Pachystomias, are capable of producing far-red, long-wave emissions (>650nm) from their AOs, a character unique among vertebrates. Aristostomias and Malacosteus posses a single far-red AO, while Pachystomias possesses anterior and posterior far-red AOs, each with smaller separate photophores positioned in their ventral margins. The purpose of this study was to establish the primary homology of the loosejaw AOs based on topological similarity of cranial nerve innervation, and subject these homology conjectures to tests of congruence under a phylogenetic hypothesis for the loosejaw dragonfishes. On the basis of whole-mount, triple-stained specimens, innervation of the loosejaw AOs is described. The AO of Aristostomias and the anterior AO of Pachystomias are innervated by the profundal ramus of the trigeminal (Tpr), while the far-red AO of Malacosteus and a small ventral AO of Pachystomias are innervated by the maxillary ramus of the trigeminal (Tmx). The largest far-red AO of Pachystomias, positioned directly below the orbit, and the short-wave AO of Photostomias are innervated by a branch of the mandibular ramus of the trigeminal nerve. Conjectures of primary homology drawn from these neuroanatomical similarities were subjected to tests of congruence on a phylogeny of the loosejaws inferred from a reanalysis of a previously published morphological dataset. Optimized for accelerated transformation, the AO innervated by the Tpr appears as a single transformation on the new topology, thereby establishing secondary homology. The AOs innervated by the Tmd found in Pachystomias and Photostomias appear as two transformations in a reconstruction on the new topology, a result that rejects secondary homology of this structure. The secondary homology of AOs innervated by the Tmx found in Malacosteus and Pachystomias is rejected on the same grounds. Two short-wave cephalic photophores present in all four genera, the suborbital (SO) and the postorbital (PO), positioned in the posteroventral margin of the orbit and directly posterior to the orbit, respectively, are innervated by separate divisions of the Tmd. The primary homologies of the loosejaw PO and SO across loosejaw taxa are proposed on the basis of similar innervation patterns. Because of dissimilar innervation of the loosejaw SO and SO of basal stomiiforms, primary homology of these photophores cannot be established. Because of similar function and position, the PO of all other stomiid taxa is likely homologous with the loosejaw PO. Nonhomology of loosejaw long-wave photophores is corroborated by previously published histological evidence. The totality of evidence suggests that the only known far-red bioluminescent system in vertebrates has evolved as many as three times in a closely related group of deep-sea fishes.