- Proceedings of the National Academy of Sciences of the United States of America
- Published over 5 years ago
A major challenge in understanding the origin of terrestrial vertebrates has been knowledge of the pelvis and hind appendage of their closest fish relatives. The pelvic girdle and appendage of tetrapods is dramatically larger and more robust than that of fish and contains a number of structures that provide greater musculoskeletal support for posture and locomotion. The discovery of pelvic material of the finned elpistostegalian, Tiktaalik roseae, bridges some of these differences. Multiple isolated pelves have been recovered, each of which has been prepared in three dimensions. Likewise, a complete pelvis and partial pelvic fin have been recovered in association with the type specimen. The pelves of Tiktaalik are paired and have broad iliac processes, flat and elongate pubes, and acetabulae that form a deep socket rimmed by a robust lip of bone. The pelvis is greatly enlarged relative to other finned tetrapodomorphs. Despite the enlargement and robusticity of the pelvis of Tiktaalik, it retains primitive features such as the lack of both an attachment for the sacral rib and an ischium. The pelvic fin of Tiktaalik (NUFV 108) is represented by fin rays and three endochondral elements: other elements are not preserved. The mosaic of primitive and derived features in Tiktaalik reveals that the enhancement of the pelvic appendage of tetrapods and, indeed, a trend toward hind limb-based propulsion have antecedents in the fins of their closest relatives.
Inspired by the relatively simple morphological blueprint provided by batoid fish such as stingrays and skates, we created a biohybrid system that enables an artificial animal–a tissue-engineered ray–to swim and phototactically follow a light cue. By patterning dissociated rat cardiomyocytes on an elastomeric body enclosing a microfabricated gold skeleton, we replicated fish morphology at 1/10 scale and captured basic fin deflection patterns of batoid fish. Optogenetics allows for phototactic guidance, steering, and turning maneuvers. Optical stimulation induced sequential muscle activation via serpentine-patterned muscle circuits, leading to coordinated undulatory swimming. The speed and direction of the ray was controlled by modulating light frequency and by independently eliciting right and left fins, allowing the biohybrid machine to maneuver through an obstacle course.
Fishes are extremely speciose and also highly disparate in their fin configurations, more specifically in the number of fins present as well as their structure, shape, and size. How they achieved this remarkable disparity is difficult to explain in the absence of any comprehensive overview of the evolutionary history of fish appendages. Fin modularity could provide an explanation for both the observed disparity in fin configurations and the sequential appearance of new fins. Modularity is considered as an important prerequisite for the evolvability of living systems, enabling individual modules to be optimized without interfering with others. Similarities in developmental patterns between some of the fins already suggest that they form developmental modules during ontogeny. At a macroevolutionary scale, these developmental modules could act as evolutionary units of change and contribute to the disparity in fin configurations. This study addresses fin disparity in a phylogenetic perspective, while focusing on the presence/absence and number of each of the median and paired fins.
The pectoral fins of ancestral fishes had multiple proximal elements connected to their pectoral girdles. During the fin-to-limb transition, anterior proximal elements were lost and only the most posterior one remained as the humerus. Thus, we hypothesised that an evolutionary alteration occurred in the anterior-posterior (AP) patterning system of limb buds. In this study, we examined the pectoral fin development of catshark (Scyliorhinus canicula) and revealed that the AP positional values in fin buds are shifted more posteriorly than mouse limb buds. Furthermore, examination of Gli3 function and regulation shows that catshark fins lack a specific AP patterning mechanism, which restricts its expression to an anterior domain in tetrapods. Finally, experimental perturbation of AP patterning in catshark fin buds results in an expansion of posterior values and loss of anterior skeletal elements. Together, these results suggest that a key genetic event of the fin-to-limb transformation was alteration of the AP patterning network.
Underwater locomotion is challenging due to the high friction and resistance imposed on a body moving through water and energy lost in the wake during undulatory propulsion. While aquatic organisms have evolved streamlined shapes to overcome such resistance, underwater locomotion has long been considered a costly exercise. Recent evidence for a range of swimming vertebrates, however, has suggested that flapping paired appendages around a rigid body may be an extremely efficient means of aquatic locomotion. Using intermittent flow-through respirometry, we found exceptional energetic performance in the Bluelined wrasse Stethojulis bandanensis, which maintains tuna-like optimum cruising speeds (up to 1 metre s(-1)) while using 40% less energy than expected for their body size. Displaying an exceptional aerobic scope (22-fold above resting), streamlined rigid-body posture, and wing-like fins that generate lift-based thrust, S. bandanensis literally flies underwater to efficiently maintain high optimum swimming speeds. Extreme energetic performance may be key to the colonization of highly variable environments, such as the wave-swept habitats where S. bandanensis and other wing-finned species tend to occur. Challenging preconceived notions of how best to power aquatic locomotion, biomimicry of such lift-based fin movements could yield dramatic reductions in the power needed to propel underwater vehicles at high speed.
Data synthesis required for large-scale macroevolutionary studies is challenging with the current tools available for integration. Using a classic question regarding the frequency of paired fin loss in teleost fishes as a case study, we sought to create automated methods to facilitate the integration of broad-scale trait data with a sizable species-level phylogeny. Similar to the evolutionary pattern previously described for limbs, pelvic and pectoral fin reduction and loss are thought to have occurred independently multiple times in the evolution of fishes. We developed a bioinformatics pipeline to identify the presence and absence of pectoral and pelvic fins of 12,582 species. To do this, we integrated a synthetic morphological supermatrix of phenotypic data for the pectoral and pelvic fins for teleost fishes from the Phenoscape Knowledgebase (two presence/absence characters for 3,047 taxa) with a species-level tree for teleost fishes from the Open Tree of Life project (38,419 species). The integration method detailed herein harnessed a new combined approach by utilizing data based on ontological inference, as well as phylogenetic propagation, to reduce overall data loss. Using inference enabled by ontology-based annotations, missing data were reduced from 98.0% to 85.9%, and further reduced to 34.8% by phylogenetic data propagation. These methods allowed us to extend the data to an additional 11,293 species for a total of 12,582 species with trait data. The pectoral fin appears to have been independently lost in a minimum of 19 lineages and the pelvic fin in 48. Though interpretation is limited by lack of phylogenetic resolution at the species level, it appears that following loss, both pectoral and pelvic fins were regained several (3) to many (14) times respectively. Focused investigation into putative regains of the pectoral fin, all within one clade (Anguilliformes), showed that the pectoral fin was regained at least twice following loss. Overall, this study points to specific teleost clades where strategic phylogenetic resolution and genetic investigation will be necessary to understand the pattern and frequency of pectoral fin reversals.
Phenotypic adaptations can allow organisms to relax abiotic selection and facilitate their ecological success in challenging habitats, yet we have relatively little data for the prevalence of this phenomenon at macroecological scales. Using data on the relative abundance of coral reef wrasses and parrotfishes (f. Labridae) spread across three ocean basins and the Red Sea, we reveal the consistent global dominance of extreme wave-swept habitats by fishes in the genus Thalassoma, with abundances up to 15 times higher than any other labrid. A key locomotor modification-a winged pectoral fin that facilitates efficient underwater flight in high-flow environments-is likely to have underpinned this global success, as numerical dominance by Thalassoma was contingent upon the presence of high-intensity wave energy. The ecological success of the most abundant species also varied with species richness and the presence of congeneric competitors. While several fish taxa have independently evolved winged pectoral fins, Thalassoma appears to have combined efficient high-speed swimming (to relax abiotic selection) with trophic versatility (to maximize exploitation of rich resources) to exploit and dominate extreme coral reef habitats around the world.
- Proceedings. Biological sciences / The Royal Society
- Published over 3 years ago
Ecological communities that occupy similar habitats may exhibit functional convergence despite significant geographical distances and taxonomic dissimilarity. On coral reefs, steep gradients in key environmental variables (e.g. light and wave energy) restrict some species to shallow depths. We show that depth-generalist reef fishes are correlated with two species-level traits: caudal fin aspect ratio and diet. Fishes with high aspect ratio (lunate) caudal fins produce weaker vortices in the water column while swimming, and we propose that ‘silent swimming’ reduces the likelihood of detection and provides an advantage on deeper reefs with lower light irradiance and water motion. Significant differences in depth preference among trophic guilds reflect variations in the availability of different food sources along a depth gradient. The significance of these two traits across three geographically and taxonomically distinct assemblages suggests that deep-water habitats exert a strong environmental filter on coral reef-fish assemblages.
A new stem-neopterygian fish from the Middle Triassic of China shows the earliest over-water gliding strategy of the vertebrates
- Proceedings. Biological sciences / The Royal Society
- Published over 6 years ago
Flying fishes are extraordinary aquatic vertebrates capable of gliding great distances over water by exploiting their enlarged pectoral fins and asymmetrical caudal fin. Some 50 species of extant flying fishes are classified in the Exocoetidae (Neopterygii: Teleostei), which have a fossil record no older than the Eocene. The Thoracopteridae is the only pre-Cenozoic group of non-teleosts that shows an array of features associated with the capability of over-water gliding. Until recently, however, the fossil record of the Thoracopteridae has been limited to the Upper Triassic of Austria and Italy. Here, we report the discovery of exceptionally well-preserved fossils of a new thoracopterid flying fish from the Middle Triassic of China, which represents the earliest evidence of an over-water gliding strategy in vertebrates. The results of a phylogenetic analysis resolve the Thoracopteridae as a stem-group of the Neopterygii that is more crown-ward than the Peltopleuriformes, yet more basal than the Luganoiiformes. As the first record of the Thoracopteride in Asia, this new discovery extends the geographical distribution of this group from the western to eastern rim of the Palaeotethys Ocean, providing new evidence to support the Triassic biological exchanges between Europe and southern China. Additionally, the Middle Triassic date of the new thoracopterid supports the hypothesis that the re-establishment of marine ecosystems after end-Permian mass extinction is more rapid than previously thought.
The transition from fins to limbs was an important terrestrial adaptation, but how this crucial evolutionary shift arose developmentally is unknown. Current models focus on the distinct roles of the apical ectodermal ridge (AER) and the signalling molecules that it secretes during limb and fin outgrowth. In contrast to the limb AER, the AER of the fin rapidly transitions into the apical fold and in the process shuts off AER-derived signals that stimulate proliferation of the precursors of the appendicular skeleton. The differing fates of the AER during fish and tetrapod development have led to the speculation that fin-fold formation was one of the evolutionary hurdles to the AER-dependent expansion of the fin mesenchyme required to generate the increased appendicular structure evident within limbs. Consequently, a heterochronic shift in the AER-to-apical-fold transition has been postulated to be crucial for limb evolution. The ability to test this model has been hampered by a lack of understanding of the mechanisms controlling apical fold induction. Here we show that invasion by cells of a newly identified somite-derived lineage into the AER in zebrafish regulates apical fold induction. Ablation of these cells inhibits apical fold formation, prolongs AER activity and increases the amount of fin bud mesenchyme, suggesting that these cells could provide the timing mechanism proposed in Thorogood’s clock model of the fin-to-limb transition. We further demonstrate that apical-fold-inducing cells are progressively lost during gnathostome evolution; the absence of such cells within the tetrapod limb suggests that their loss may have been a necessary prelude to the attainment of limb-like structures in Devonian sarcopterygian fish.