Mark W. Westneat

EVOLUTIONARY HISTORY OF THE PARROTFISHES: BIOGEOGRAPHY, ECOMORPHOLOGY, AND COMPARATIVE DIVERSITY

Abstract The family Scaridae comprises about 90 species of herbivorous coral reef, rock reef, and seagrass fishes. Parrotfishes are important agents of marine bioerosion who rework the substrate with their beaklike oral jaws. Many scarid populations are characterized by complex social systems including highly differentiated sexual stages, terri‐toriality, and the defense of harems. Here, we test a hypothesis of relationships among parrotfish genera derived from nearly 2 kb of nuclear and mitochondrial DNA sequence. The DNA tree is different than a phylogeny based on comparative morphology and leads to important reinterpretations of scarid evolution. The molecular data suggest a split among seagrass and coral reef associated genera with nearly 80% of all species in the coral reef clade. Our phylogenetic results imply an East Tethyan origin of the family and the recurrent evolution of excavating and scraping feeding modes. It is likely that ecomorphological differences played a significant role in the initial divergence of major scarid lineages, but that variation in color and breeding behavior has triggered subsequent diversification. We present a two‐phase model of parrotfish evolution to explain patterns of comparative diversity. Finally, we discuss the application of this model to other adaptively radiating clades.

Mechanical performance of aquatic rowing and flying.

Aquatic flight, performed by rowing or flapping fins, wings or limbs, is a primary locomotor mechanism for many animals.We used a computer simulation to compare the mechanical performance of rowing and flapping appendages across a range of speeds. Flapping appendages proved to be more mechanically efficient than rowing appendages at all swimming speeds, suggesting that animals that frequently engage in locomotor behaviours that require energy conservation should employ a flapping stroke. The lower efficiency of rowing appendages across all speeds begs the question of why rowing occurs at all. One answer lies in the ability of rowing fins to generate more thrust than flapping fins during the power stroke. Large forces are necessary for manoeuvring behaviours such as accelerations, turning and braking, which suggests that rowing should be found in slow–swimming animals that frequently manoeuvre. The predictions of the model are supported by observed patterns of behavioural variation among rowing and flapping vertebrates.

Evolution of Levers and Linkages in the Feeding Mechanisms of Fishes

Abstract The evolution of feeding mechanisms in the ray-finned fishes (Actinopterygii) is a compelling example of transformation in a musculoskeletal complex involving multiple skeletal elements and numerous muscles that power skull motion. Biomechanical models of jaw force and skull kinetics aid our understanding of these complex systems and enable broad comparison of feeding mechanics across taxa. Mechanical models characterize how muscles move skeletal elements by pulling bones around points of rotation in lever mechanisms, or by transmitting force through skeletal elements connected in a linkage. Previous work has focused on the feeding biomechanics of several lineages of fishes, but a broader survey of skull function in the context of quantitative models has not been attempted. This study begins such a survey by examining the diversity of mechanical design of the oral jaws in 35 species of ray-finned fishes with three main objectives: (1) analyze lower jaw lever models in a broad phylogenetic range of taxa, (2) identify the origin and evolutionary patterns of change in the linkage systems that power maxillary rotation and upper jaw protrusion, and (3) analyze patterns of change in feeding design in the context of actinopterygian phylogeny. The mandibular lever is present in virtually all actinopterygians, and the diversity in lower jaw closing force transmission capacity, with mechanical advantage ranging from 0.04 to 0.68, has important functional consequences. A four-bar linkage for maxillary rotation arose in the Amiiformes and persists in various forms in many teleost species. Novel mechanisms for upper jaw protrusion based on this linkage for maxillary rotation have evolved independently at least five times in teleosts. The widespread anterior jaws linkage for jaw protrusion in percomorph fishes arose initially in Zeiformes and subsequently radiated into a wide range of premaxillary protrusion capabilities.

Ecomorphology of locomotion in labrid fishes

The Labridae is an ecologically diverse group of mostly reef associated marine fishes that swim primarily by oscillating their pectoral fins. To generate locomotor thrust, labrids employ the paired pectoral fins in motions that range from a fore-aft rowing stroke to a dorso-ventral flapping stroke. Species that emphasize one or the other behavior are expected to benefit from alternative fin shapes that maximize performance of their primary swimming behavior. We document the diversity of pectoral fin shape in 143 species of labrids from the Great Barrier Reef and the Caribbean. Pectoral fin aspect ratio ranged among species from 1.12 to 4.48 and showed a distribution with two peaks at about 2.0 and 3.0. Higher aspect ratio fins typically had a relatively long leading edge and were narrower distally. Body mass only explained 3% of the variation in fin aspect ratio in spite of four orders of magnitude range and an expectation that the advantages of high aspect ratio fins and flapping motion are greatest at large body sizes. Aspect ratio was correlated with the angle of attachment of the fin on the body (r = 0.65), indicating that the orientation of the pectoral girdle is rotated in high aspect ratio species to enable them to move their fin in a flapping motion. Field measures of routine swimming speed were made in 43 species from the Great Barrier Reef. Multiple regression revealed that fin aspect ratio explained 52% of the variation in size-corrected swimming speed, but the angle of attachment of the pectoral fin only explained an additional 2%. Labrid locomotor diversity appears to be related to a trade-off between efficiency of fast swimming and maneuverability in slow swimming species. Slow swimmers typically swim closer to the reef while fast swimmers dominate the water column and shallow, high-flow habitats. Planktivory was the most common trophic associate with high aspect ratio fins and fast swimming, apparently evolving six times.

A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes.

Fish skulls are complex kinetic systems with movable components that are powered by muscles. Cranial muscles for jaw closing pull the mandible around a point of rotation at the jaw joint using a third-order lever mechanism. The present study develops a lever model for the jaw of fishes that uses muscle design and the Hill equation for nonlinear length-tension properties of muscle to calculate dynamic power output. The model uses morphometric data on skeletal dimensions and muscle proportions in order to predict behavior and force transmission mediated by lever action. The computer model calculates a range of dynamic parameters of jaw function including muscle force, torque, effective mechanical advantage, jaw velocity, bite duration, bite force, work and power. A complete list of required morphometrics is presented and a software program (MandibLever 2.0) is available for implementing lever analysis. Results show that simulations yield kinematics and timing profiles similar to actual fish feeding events. Simulation of muscle properties shows that mandibles reach their peak velocity near the start of jaw closing, peak force at the end of jaw closing, and peak power output at about 25% of the closing cycle time. Adductor jaw muscles with different mechanical designs must have different contractile properties and/or different muscle activity patterns to coordinate jaw closing. The effective mechanical advantage calculated by the model is considerably lower than the mechanical advantage estimated from morphological lever ratios, suggesting that previous studies of morphological lever ratios have overestimated force and underestimated velocity transmission to the mandible. A biomechanical model of jaw closing can be used to interpret the mechanics of a wide range of jaw mechanisms and will enable studies of the functional results of developmental and evolutionary changes in skull morphology and physiology.

Ontogeny of feeding motor patterns in infant rats: an electromyographic analysis of suckling and chewing.

During mammalian ontogeny, there is a transition from suckling to the chewing of food. The question was asked: Is suckling a neuromuscular precursor to chewing, or are suckling and chewing independent systems? Electromyograms (EMGs) were recorded in rat pups of ages 6, 9, 12, 15, 18, and 21 days from the superficial masseter, anterior digastric, sternohyoideus, and genioglossus muscles during suckling and chewing. The EMG patterns of the 3 components of suckling behavior (nipple attachment, rhythmic sucking and the stretch response) are distinctive from one another and reflect the musculoskeletal biomechanics of suckling. Chewing EMGs are present by 12 days of age and attain the adult pattern by 18-21 days of age. During nipple attachment, pups exhibit a motor pattern that is similar to that of adult chewing, but other aspects of suckling differ from chewing in some EMG features. Comparison of EMGs between behaviors and between ages allowed interpretation of the degree of contunity of muscular activity across the suckling-to-chewing transition.

Local phylogenetic divergence and global evolutionary convergence of skull function in reef fishes of the family Labridae

The Labridae is one of the most structurally and functionally diversified fish families on coral and rocky reefs around the world, providing a compelling system for examination of evolutionary patterns of functional change. Labrid fishes have evolved a diverse array of skull forms for feeding on prey ranging from molluscs, crustaceans, plankton, detritus, algae, coral and other fishes. The species richness and diversity of feeding ecology in the Labridae make this group a marine analogue to the cichlid fishes. Despite the importance of labrids to coastal reef ecology, we lack evolutionary analysis of feeding biomechanics among labrids. Here, we combine a molecular phylogeny of the Labridae with the biomechanics of skull function to reveal a broad pattern of repeated convergence in labrid feeding systems. Mechanically fast jaw systems have evolved independently at least 14 times from ancestors with forceful jaws. A repeated phylogenetic pattern of functional divergence in local regions of the labrid tree produces an emergent family-wide pattern of global convergence in jaw function. Divergence of close relatives, convergence among higher clades and several unusual ‘breakthroughs’ in skull function characterize the evolution of functional complexity in one of the most diverse groups of reef fishes.

Feeding mechanism of Epibulus insidiator (Labridae; Teleostei): Evolution of a novel functional system

The feeding mechanism of Epibulus insidiator is unique among fishes, exhibiting the highest degree of jaw protrusion ever described (65% of head length). The functional morphology of the jaw mechanism in Epibulus is analyzed as a case study in the evolution of novel functional systems. The feeding mechanism appears to be driven by unspecialized muscle activity patterns and input forces, that combine with drastically changed bone and ligament morphology to produce extreme jaw protrusion. The primary derived osteological features are the form of the quadrate, interopercle, and elongate premaxilla and lower jaw. Epibulus has a unique vomero‐interopercular ligament and enlarged interoperculo‐mandibular and premaxilla‐maxilla ligaments. The structures of the opercle, maxilla, and much of the neurocranium retain a primitive labrid condition. Many cranial muscles in Epibulus also retain a primitive structural condition, including the levator operculi, expaxialis, sternohyoideus, and adductor mandibulae. The generalized perciform suction feeding pattern of simultaneous peak cranial elevation, gape, and jaw protrusion followed by hyoid depression is retained in Epibulus. Electromyography and high‐speed cinematography indicate that patterns of muscle activity during feeding and the kinematic movements of opercular rotation and cranial elevation produce a primitive pattern of force and motion input. Extreme jaw protrusion is produced from this primitive input pattern by several derived kinematic patterns of modified bones and ligaments. The interopercle, quadrate, and maxilla rotate through angles of about 100 degrees, pushing the lower jaw into a protruded position. Analysis of primitive and derived characters at multiple levels of structural and functional organization allows conclusions about the level of design at which change has occurred to produce functional novelties.

Advances in Biological Structure, Function, and Physiology Using Synchrotron X-Ray Imaging*

Studies of the physiology and biomechanics of small ( approximately 1 cm) organisms are often limited by the inability to see inside the animal during a behavior or process of interest and by a lack of three-dimensional morphology at the submillimeter scale. These constraints can be overcome by an imaging probe that has sensitivity to soft tissue, the ability to penetrate opaque surfaces, and high spatial and temporal resolution. Synchrotron X-ray imaging has been successfully used to visualize millimeter-centimeter-sized organisms with micrometer-range spatial resolutions in fixed and living specimens. Synchrotron imaging of small organisms has been the key to recent novel insights into structure and function, particularly in the area of respiratory physiology and function of insects. X-ray imaging has been effectively used to examine the morphology of tracheal systems, the mechanisms of tracheal and air sac compression in insects, and the function of both chewing and sucking mouthparts in insects. Synchrotron X-ray imaging provides an exciting new window into the internal workings of small animals, with future promise to contribute to a range of physiological and biomechanical questions in comparative biology.

The horizontal septum: mechanisms of force transfer in locomotion of Scombrid fishes (Scombridae, perciformes)

We describe the complex shapes of myomeres and myosepta in the mackerels and tunas (Scombridae: Teleostei), and we reveal the orientation of two major systems of collagen fibers in myosepta and horizontal septa with respect to points of attachment to skeleton and skin. Our goal is to identify the likely pathways of the transmission of muscle forces during locomotion. Our primary conclusions are (1) that the collagen fibers of myosepta, horizontal septa, and skin are the organs that transfer locomotor forces from the contraction of myomeres to the backbone and caudal fin during locomotion, and (2) that locomotor muscle pulls against a three‐dimensional structure of tendons, septa, and skin that is kept in tension by the radial expansion of the contracting muscle. The main horizontal septum is formed by the convergence of myosepta and is likely to be the major transmitter of muscle force to the axial skeleton. The geometry of the myomeres, the position of red muscle, and particularly the geometric conformation of crossed‐fiber arrays of collagen in the main horizontal septum suggest specific mechanisms for the transfer of muscle force to the backbone among scombrid fishes. Morphometrics and the construction of physical models help us to identify musculoskeletal mechanisms of locomotion, and we present two quantitative models of locomotor mechanics in fishes.