The assembly of modern ocean ecosystems was fundamentally affected by the Cretaceous-Palaeogene (K-Pg) mass extinction. Among the casualties of this event were many extinct clades of large pelagic predatory fishes. The extinction of these lineages is thought to have created ecological opportunity that spurred the diversification of living large-bodied (> 2 m) marine predatory fishes such as tunas and mackerels (Scombridae). However, it remains unclear whether a large, endothermic body plan evolved in tunas and mackerels directly after the K-Pg boundary or in a stepwise manner throughout the Cenozoic. Here, we demonstrate that Scombridae, which includes half of living endothermic ray-finned fish species, evolved endothermy and large body sizes long after the initial radiation of the clade at the K-Pg boundary. Our time-calibrated phylogeny also reveals that the origins of endothermy, large body size and increased longevity in true tunas are staggered over evolutionary time. These findings indicate that the evolution of large endothermic scombrids was not triggered by the K-Pg extinction and substantiate the protracted development of the endothermic predatory body plans of tunas and relatives over more than 50 million years of evolutionary history.

The external appearance of frog skin varies among species and across body regions. Although this variation has long been recognized, it remains an understudied aspect of frog diversity. Further, the evolutionary processes driving this variation are unclear because previous work has been largely qualitative. Here we quantify the skin texture of 187 species spanning 45 of the 57 frog families using standardized gel-based profilometry. Using phylogenetic comparative models we explore the extent to which skin texture differs among body regions, how these differences have evolved across major frog clades, and whether microhabitat, climate, and body size help explain texture patterns. We find that the ventral posterior region, which functions in water uptake and rehydration, tends to be rougher than other body regions, yet skin texture evolves at similar rates across the body. Microhabitat, particularly arboreality, is linked to greater skin texture variation among body regions. Among species occupying more terrestrial microhabitats (e.g., arboreal, burrowing, leaflitter), we find that body size and local climate has little effect on skin texture. By comparing skin texture across a wide range of species and environments worldwide, our study tests hypotheses about external skin diversity in frogs that have previously received limited comparative evaluation and highlights texture as an informative component of amphibian skin biology.

Abstract Slippery, mucus-coated body surfaces are widespread in aquatic vertebrates, but their contribution to locomotion is unclear. Fish mucus has long been proposed to reduce drag, yet direct experimental evidence of a swimming benefit is limited. A series of four mucus-inspired, lubricant-infused aluminum substrates incorporating SLIPS (slippery liquid-infused porous surfaces) were fabricated to assess the effects of a slippery coating on motion under both static (drag-based) and dynamic (propulsive) conditions. The aluminum substrates were textured by conversion of the surface to nanostructured aluminum oxyhydroxide (boehmite), chemically functionalized, and infused with synthetic Newtonian liquids spanning the viscosity range of measured trout mucus and compared to that of unstructured and lubricant-free controls. Viscosity measurements were also performed on skin mucus collected from brook trout (S. fontinalis). SLIPS-coated surfaces were found to reduce the static drag by up to 9.1% and enhance the lift-to-drag ratio by up to 8.7%. Furthermore, SLIPS coatings improved both the thrust and efficiency of flapping plates actuated in heave and pitch by up to 3.6% and 4.1%, respectively, with performance improvements observed over a broad range of motion parameters, lubricant chemistries, and viscosities. Boundary layer flow measurements over a flat plate revealed that SLIPS experienced a reduced skin friction drag of up to 5.2% under laminar flow conditions. Nanostructured, functionalized, lubricated coatings thus act both to reduce drag and to enhance the propulsive thrust and efficiency of fishlike propulsion, providing one explanation for the presence of such structures on a diversity of animal surfaces.

The primary function of the vertebrate jaw is the dorsoventral movement that occurs during opening and closing. Yet, several lineages have evolved the ability to move their jaws laterally, enabling major innovations, like chewing. While lateral jaw motions are primarily known in tetrapods, here, we show that an ecologically dominant lineage of reef fishes (Zanclidae and Acanthuridae) has evolved the ability to laterally rotate their jaws during feeding. This unique function substantially expands both the kinematic versatility and known diversity of vertebrate jaw mechanisms, adding to the growing list of innovations that followed the origin of jaws. Within Acanthuridae, this increased kinematic versatility may allow for algal detachment with minimal movement of the rest of the body, facilitating rapid biting within the same microtopographic location, and thus, this lineage having the highest bite rates among biting reef fishes. This innovation may have thus helped create one of the most ecologically diverse and speciose herbivorous reef fish lineages. Our results highlight the ecological and evolutionary impact of lateral jaw rotation within vertebrates, and potentially how this novelty led to a significant change in coral reef trophodynamics.

Tunas are high-performance pelagic fishes of considerable economic importance and have a suite of biological adaptations for high-speed locomotion. In contrast to our understanding of tuna body and muscle function, mechanosensory systems of tuna are poorly understood. Here we present the discovery of a remarkable sensory lateral line canal within the bilateral tuna keels with tubules that extend to the upper and lower keel surfaces. Neuromast mechanoreceptor organs are found periodically along the canal lumen, enclosed within tubular ossifications surrounding the canal that we interpret as modified lateral line scales. In addition, a series of segmental, elongated skeletal elements of unknown homology support the posterior end of the keel. These observations suggest that the bilateral tuna keels act as flow sensing structures, perhaps providing information on tail beat frequency, amplitude, force, and water flow dynamics over the caudal region of the tuna body axis during locomotion.

Shark skin is covered in denticles that provide texture important for hydrodynamic function. In bony fishes, both skin texture and function are modified by mucus that covers the outermost layer of the skin and scales. Despite the similar potential for mucus to change skin texture and function in shark skin, little is known about the occurrence and effect of external mucus in sharks. Specifically, we do not know where mucus is present along the shark body or how mucus alters surface texture, which could alter denticle function. To fill these gaps, we obtained individuals of Mustelus canis (dusky smooth-hound shark) and used gel-based profilometry to quantify the texture of the three-dimensional surface at eight body regions under two conditions: (1) a live anesthetized condition with mucus and (2) a condition after mucus was removed during preservation. We discovered that mucus covers and obscures the denticles on the dorsal fin and tail trailing edge tips; as a result, these regions were smoother and had a different surface texture than the preserved condition at the same region. Specifically, five parameters were significantly changed by mucus in these regions: roughness, skew, kurtosis, developed interfacial area ratio, and exposed area of the denticles. Notably, mucus did not change surface texture at any of the other body regions. Both the tips of the dorsal fin and tail are regions where flow separates and vortices are shed, so these results could indicate that mucus is modifying the boundary layer flow. Our results demonstrate that shark skin mucus is secreted selectively in particular body regions and that it can drastically change the surface texture when present. These findings suggest a need to both explore the morphology and properties of shark mucus and to consider mucus in studies of shark skin hydrodynamics.

As they grow, sharks both replace lost denticles and proliferate the number of denticles by developing new (de novo) denticles without prior denticle shedding. The loss and replacement of denticles has potential impacts on the energetic cost of maintaining the skin surface, the biomechanical functions of shark skin, as well as our ability to predict shark abundance from fossil denticle occurrence in sediment cores. Here, we seek to better understand patterns of denticle loss and to show how denticles are being replaced in mature sharks. We illustrate shark skin surfaces with missing denticles and quantify both within-species and between-species patterns of missing denticles using images from across regions of the body for two species and images at similar body regions for 16 species of sharks. Generally, sharks are missing similar numbers of denticles (0%-6%) between species and regions. However, there are exceptions: in the smooth dogfish, the nose region is missing significantly more denticles than most posterior-body and fin regions, and the common thresher shark is missing significantly more denticles than the smooth dogfish, leopard shark, angel shark, bonnethead, and gulper shark. Denticle regrowth starts with crown development and mineralization beneath the epidermis, followed by eruption of the crown, and finally the mineralization of the root. The pulp cavity of replacement denticles is initially large and surrounded by a thin shell of enameloid upon eruption of the denticle. After eruption of the denticle, the deposition of dentine continues internally after the denticle reaches its final position. Replacement of missing denticles, representing less than 6% of the skin surface at any one time, may not compromise hydrodynamic function, but by constantly updating the skin surface throughout life, sharks may reduce surface fouling and maintain a functional complex skin surface by repairing local damage to individual denticles.

Major trade-offs often manifest as axes of diversity in organismal functional systems. Overarching trade-offs may result in high trait integration and restrict the trajectory of diversification to be along a single axis. Here, we explore the diversification of the feeding mechanism in coral reef fishes to establish the role of trade-offs and complexity in a spectacular ecological radiation. We show that the primary axis of variation in the measured musculo-skeletal traits is aligned with a trade-off between mobility and force transmission, spanning species that capture prey with suction and those that bite attached prey. We found weak or no covariation between about half the traits, reflecting deviations from the trade-off axis. The dramatic trophic range found among reef fishes occurs along the primary trade-off axis, with numerous departures that use a mosaic of trait combinations to adapt the feeding mechanism to diverse challenges. We suggest that morphological evolution both along and independent of a major axis of variation is a widespread mechanism of diversification in complex systems where a global trade-off shapes major patterns of diversity. Significant additional diversity emerges as systems use weak integration and complexity to assemble functional units with many trait combinations that meet varying ecological demands. The diversity of coral reef fishes' feeding apparatus aligns with the trade-off between mobility and force transmission, but weak trait covariation and complexity allow jaw traits to evolve independently to adapt to diverse ecological challenges.

In functional systems composed of many traits, selection for specialized function can induce trait evolution by acting directly on individual components within the system, or indirectly through networks of trait integration. However, strong integration can also hinder diversification into regions of trait space that are not aligned with axes of covariation among traits. Thus, non-independence among traits may limit functional expansion. We explore this dynamic in the evolution of fin shapes in 106 species from 38 families of coral reef fishes, a polyphyletic assemblage that shows exceptional diversity in locomotor function. Despite expectations of a strong match between form and function, we find subtantial fin shape disparity across species that share a swimming mode. The evolution of fin shape is weakly integrated across the four functionally dominant fins in swimming and integration is weakened as derived swimming modes evolve. The weak integration among fins in the ancestral locomotor condition provides a primary axis of diversification while allowing for off-axis diversification via independent trait responses to selection. However, the evolution of novel locomotor modes coincides with a loss of integration among fins. Our study highlights the need for additional work on the functional consequences of fin shape in fishes.

The scales and skin mucus of bony fishes are both proposed to have a role in beneficially modifying the hydrodynamics of water flow over the body surface. However, it has been challenging to provide direct experimental evidence that tests how mucus and fish scales change the boundary layer in part due to the difficulties in working with live animal tissue and difficulty directly imaging the boundary layer. In this manuscript, we use direct imaging and flow tracking within the boundary layer to compare boundary layer dynamics over surfaces of fish skin with mucus, without mucus, and a flat control surface. Our direct measurements of boundary layer flows for these three different conditions are repeated for two different species, bluegill sunfish (Lepomis macrochirus) and blue tilapia (Oreochromis aureus). Our goals are to understand if mucus and scales reduce drag, shed light on mechanisms underlying drag reduction, compare these results between species, and evaluate the relative contributions to hydrodynamic function for both mucus and scales. We use our measurements of boundary layer flow to calculate shear stress (proportional to friction drag), and we find that mucus reduces drag overall by reducing the velocity gradient near the skin surface. Both bluegill and tilapia showed similar patterns of surface velocity reduction. We also note that scales alone do not appear to reduce drag, but that mucus may reduce friction drag up to 50% compared to scaled surfaces without mucus or flat controls.

Geographic isolation is the primary driver of speciation in many vertebrate lineages. This trend is exemplified by North American darters, a clade of freshwater fishes where nearly all sister species pairs are allopatric and separated by millions of years of divergence. One of the only exceptions is the Lake Waccamaw endemic Etheostoma perlongum and its riverine sister species Etheostoma maculaticeps, which have no physical barriers to gene flow. Here we show that lacustrine speciation of E. perlongum is characterized by morphological and ecological divergence likely facilitated by a large chromosomal inversion. While E. perlongum is phylogenetically nested within the geographically widespread E. maculaticeps, there is a sharp genetic and morphological break coinciding with the lake-river boundary in the Waccamaw River system. Despite recent divergence, an active hybrid zone, and ongoing gene flow, analyses using a de novo reference genome reveal a 9 Mb chromosomal inversion with elevated divergence between E. perlongum and E. maculaticeps. This region exhibits striking synteny with known inversion supergenes in two distantly related fish lineages, suggesting deep evolutionary convergence of genomic architecture. Our results illustrate that rapid, ecological speciation with gene flow is possible even in lineages where geographic isolation is the dominant mechanism of speciation.

Fish scales are bony plates embedded in the skin that vary extensively in shape across taxa. Despite a plethora of hypotheses regarding form function relationships in scales, we know little about the ecological selective factors that shape their diversity. Here we examine evolutionary patterns of scale morphology using novel three-dimensional topography from the surfaces of 59 species of damselfishes, a prominent radiation of coral reef fishes. We find evidence that scale morphology changes with different flow environments, such that species that spend more time in open-water habitats have smoother scales. We also show that other aspects of ecology lead to highly derived scales. For example, anemonefishes show an evolutionary transition to smaller scales and smaller ctenii (scale spines). Moreover, changes in body shape, which may reflect ecological differentiation, are related to scale shape but not surface properties. We also demonstrate weak evolutionary integration among multiple aspects of scale morphology; however, scale size and shape are related, and scale morphology is correlated between different body regions. Finally, we also identify a relationship between aspects of lateral line pore morphology, such that the number of lateral line pores per scale and the size of those pores are inversely related. Overall, our study provides insights into the multidimensionality of scale evolution and improves our understanding of some of the factors that can give rise to the diversity of scales seen across fishes.

Many aquatic animals swim by undulatory body movements and understanding the diversity of these movements could unlock the potential for designing better underwater robots. Here, we analyzed the steady swimming kinematics of a diverse group of fish species to investigate whether their undulatory movements can be represented using a series of interconnected multi-segment models, and if so, to identify the key factors driving the segment configuration of the models. Our results show that the steady swimming kinematics of fishes can be described successfully using parsimonious models, 83% of which had fewer than five segments. In these models, the anterior segments were significantly longer than the posterior segments, and there was a direct link between segment configuration and swimming kinematics, body shape, and Reynolds number. The models representing eel-like fishes with elongated bodies and fishes swimming at high Reynolds numbers had more segments and less segment length variability along the body than the models representing other fishes. These fishes recruited their anterior bodies to a greater extent, initiating the undulatory wave more anteriorly. Two shape parameters, related to axial and overall body thickness, predicted segment configuration with moderate to high success rate. We found that head morphology was a good predictor of its segment length. While there was a large variation in head segments, the length of tail segments was similar across all models. Given that fishes exhibited variable caudal fin shapes, the consistency of tail segments could be a result of an evolutionary constraint tuned for high propulsive efficiency. The bio-inspired multi-segment models presented in this study highlight the key bending points along the body and can be used to decide on the placement of actuators in fish-inspired robots, to model hydrodynamic forces in theoretical and computational studies, or for predicting muscle activation patterns during swimming.

The coastal waters of the North Pacific are home to the northern clingfish (Gobiesox maeandricus), Pacific spiny lumpsucker (Eumicrotremus orbis) and marbled snailfish (Liparis dennyi) - three fishes that have evolved ventral adhesive discs. Clingfish adhesive performance has been studied extensively, but relatively little is known about the performance of other sticky fishes. Here, we compared the peak adhesive forces and work to detachment of clingfish, lumpsuckers and snailfish on surfaces of varying roughness and over ontogeny. We also investigated the morphology of their adhesive discs through micro-computed tomography scanning and scanning electron microscopy. We found evidence that adhesive performance is tied to the intensity and variability of flow regimes in the fishes' habitats. The northern clingfish generates the highest adhesive forces and lives in the rocky intertidal zone where it must resist exposure to crashing waves. Lumpsuckers and snailfish both generate only a fraction of the clingfish's adhesive force, but live more subtidal where currents are slower and less variable. However, lumpsuckers generate more adhesive force relative to their body weight than snailfish, which we attribute to their higher-drag body shape and frequent bouts into the intertidal zone. Even so, the performance and morphology data suggest that snailfish adhesive discs are stiffer and built more efficiently than lumpsucker discs. Future studies should focus on sampling additional diversity and designing more ecologically relevant experiments when investigating differences in adhesive performance.