Jeffrey A. Walker

Constraints on Adaptive Evolution: The functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata)

The empirical study of natural selection reveals that adaptations often involve trade‐offs between competing functions. Because natural selection acts on whole organisms rather than isolated traits, adaptive evolution may be constrained by the interaction between traits that are functionally integrated. Yet, few attempts have been made to characterize how and when such constraints are manifested or whether they limit the adaptive divergence of populations. Here we examine the consequences of adaptive life‐history evolution on locomotor performance in the live‐bearing guppy. In response to increased predation from piscivorous fish, Trinidadian guppies evolve an increased allocation of resources toward reproduction. These populations are also under strong selection for rapid fast‐start swimming performance to evade predators. Because embryo development increases a female’s wet mass as she approaches parturition, an increased investment in reproductive allocation should impede fast‐start performance. We find evidence for adaptive but constrained evolution of fast‐start swimming performance in laboratory trials conducted on second‐generation lab‐reared fish. Female guppies from high‐predation localities attain a faster acceleration and velocity and travel a greater distance during fast‐start swimming trials. However, velocity and distance traveled decline more rapidly over the course of pregnancy in these same females, thus reducing the magnitude of divergence in swimming performance between high‐ and low‐predation populations. This functional trade‐off between reproduction and swimming performance reveals how different aspects of the phenotype are integrated and highlights the complexity of adaptation at the whole‐organism level.

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 pelvic reduction in threespine stickleback fish : a test of competing hypotheses

Reimchen hypothesized that pelvic reduction in threespine stickleback is favored by an absence of piscivorous fishes and the resulting increase in predation by insects, but Giles hypothesized that the predation regime is unimportant and that a low dissolved calcium concentration favors evolution of pelvic reduction. Substantial pelvic reduction in threespine stickleback sampled from 179 lakes around Cook Inlet, Alaska is strongly associated both with an absence of predatory fishes and a low calcium concentration. However, the association of pelvic reduction with low calcium concentration appears to be contingent on the absence of predatory fishes. These results emphasize the importance of interactions between seemingly unrelated environmental variables for selection of a single trait. However, these results also conflict with some observations elsewhere and do not rule out the possibility that other environmental factors are important for selection for pelvic reduction in threespine stickleback.

Multi-trait Selection, Adaptation, and Constraints on the Evolution of Burst Swimming Performance

Abstract Whole organism performance represents the integration of numerous physiological, morphological, and behavioral traits. How adaptive changes in performance evolve therefore requires an understanding of how selection acts on multiple integrated traits. Two approaches that lend themselves to studying the evolution of performance in natural populations are the use of quantitative genetics models for estimating the strength of selection acting on multiple quantitative traits and ecological genetic comparisons of populations exhibiting phenotypic differences correlated with environmental variation. In both cases, the ultimate goal is to understand how suites of traits and trade-offs between competing functions respond to natural selection. Here we consider how these two complimentary approaches can be applied to study the adaptive evolution of escape performance in fish. We first present an extension of Arnolds (1983) quantitative genetic approach that explicitly considers how trade-offs between different components of performance interact with the underlying genetics. We propose that such a model can reveal the conditions under which multiple selection pressures will cause adaptive change in traits that influence more than one component of fitness. We then review work on the Atlantic silversides and Trinidadian guppies as two case studies where an ecological genetics approach has been successfully applied to evaluate how the evolution of escape performance trades-off with other components of fitness. We conclude with the general lesson that whole organism performance is embedded in a complex phenotype, and that the net outcome of selection acting on different aspects of the organism will often result in a compromise among competing influences.

Structure, function, and neural control of pectoral fins in fishes

Fin-based propulsion systems perform well for both high-speed cruising and high maneuverability in fishes, making them good models for propulsors of autonomous underwater vehicles. Labriform locomotion in fishes is actuated by oscillation of the paired pectoral fins. Here, we present recent research on fin structure, fin motion, and neural control in fishes to outline important future directions for this field and to assist engineers in attempting biomimicry of maneuverable fin-based locomotion in shallow surge zones. Three areas of structure and function are discussed in this review: 1) the anatomical structure of the fin blade, skeleton, and muscles that drive fin motion; 2) the rowing and flapping motions that fins undergo for propulsion in fishes; and 3) the neuroanatomy, neural circuitry, and electrical muscle activity that are characteristic of pectoral fins. Research on fin biomechanics, muscle physiology and neural control is important to the comparative biology of locomotion in fishes and application of fin function for aid in aquatic vehicle design. Recommendations are made regarding fin propulsor designs based on the fin shape, activation pattern, and motion. Research on neural control of fins is a key piece in the puzzle for a complete understanding of comparative fin function and may provide important principles for engineers designing control systems for fin-like propulsors.

A General Model of Functional Constraints on Phenotypic Evolution

A general model of the functional constraints on the rate and direction of phenotypic evolution is developed using a decomposition of the Lande‐Arnold model of multivariate phenotypic evolution. The important feature of the model is the F matrix of performance coefficients reflecting the causal relationship between morphophysiological (m‐p) and functional performance traits. The structure of F, which reflects the functional architecture of the organism, constrains the shape of the adaptive landscape and thus the rate and direction of m‐p trait evolution. The rate of m‐p trait evolution is a function of the pattern of coefficients in a row of F. The sums and variances of these rows are related to current concepts of evolvability. The direction of m‐p trait evolution through m‐p trait space is a function of the functional covariances among m‐p traits. The functional covariance between a pair of m‐p traits is a measure of how much the traits function together and is computed as the covariance between rows of F. Finally, it is shown that genetic covariances between m‐p traits and performance traits are a function of the F matrix, but a G matrix that includes these covariances cannot be used to model functional constraints effectively.

Kinematics, Dynamics, and Energetics of Rowing and Flapping Propulsion in Fishes

Abstract The shape and motion of the pectoral fins vary considerably among fishes that swim in the labriform mode. Pectoral fin motion in fishes is highly variable, but one conspicuous axis of this variation is the rowing-flapping axis. At one extreme of this axis, paddle-shaped fins row back and forth in a plane that is parallel to fish motion, while at the other extreme, wing-shaped fins flap up and down in a plane that is perpendicular to fish motion. We have used two fish, the threespine stickleback (Gasterosteus aculeatus) and the bird wrasse (Gomphosus varius), that fall near the extremes of the rowing-flapping axis to study the dynamic, energetic, and ecological and evolutionary consequences of this kinematic variation. Our work confirms some traditionally held assumptions about rowing and flapping dynamics and energetics but reject others. A computer simulation experiment of virtual rowing and flapping appendages makes several predictions about differences in maneuvering performance and swimming energetics between rowing and flapping, which, in turn, make predictions about the behavior and ecological distribution of fishes that vary along the rowing-flapping axis. Both laboratory and field studies of labrid swimming ability and distribution support these predictions.

Functional morphology and virtual models: physical constraints on the design of oscillating wings, fins, legs, and feet at intermediate reynolds numbers.

Abstract Why do some animals swim by rowing appendages back and forth while others fly by flapping them up and down? One hypothesis suggests the answer lies in the sharply divergent physical environments encountered by small, slow animals, and large, fast animals. Flapping appendages allow large animals to move through a fluid environment quickly and efficiently. As size and speed decrease, however, viscous drag increasingly dominates the force balance, with negative consequences for both rowing and flapping appendages. Nevertheless, comparative data suggest that flapping does not occur in animals at Reynolds numbers (Re) less than about 15. I used a computer simulation experiment to address the question, “Below what Re is rowing more effective than flapping?” The simulation, which employed a simple quasi-steady, blade-element model of virtual oscillating appendages, has several important results. First, the mechanical efficiency of both rowing and flapping decrease dramatically with scale. Second, the performance of rowing can increase substantially by taking advantage of several dynamic shape modifications, including area and span reduction during the recovery stroke. Finally, the relative performance of rowing and flapping is dependent on the advance ratio, which is a function of the travel speed relative to the oscillation frequency. The model predicts that rowing is more efficient than flapping at Re < 20 for animals moving throughout the range of typically observed advance ratios.

Kinematics and performance of maneuvering control surfaces in teleost fishes

Many fishes routinely exploit resources in high-energy marine habitats of interest to ocean engineers, including rocky coasts and coral reefs. How fishes modulate fin motions to correct perturbations to the preferred heading or to maneuver in complex structure should interest both biologists and ocean engineers. These fin motions are reviewed in order to generate simple models of causal relationships between fin design, motion, and maneuvering performance. The available data on maneuvering performance in fishes is reviewed to compare to the simple models, to identify gaps in our knowledge, and to outline a research program to address these gaps more effectively.

Dynamics of Pectoral Fin Rowing in a Fish with an Extreme Rowing Stroke: The threespine stickleback (Gasterosteus aculeatus)

SUMMARY The dynamics of pectoral fin rowing in the threespine stickleback are investigated by measuring the instantaneous force balance on freely swimming fish throughout the stroke cycle and comparing the measured forces with fin motions and an unsteady, blade-element model of pectoral fin propulsion. Both measured and modeled forces suggest that attached vortex and circulatory forces and not inertial (added mass) forces dominate the force balance. Peak forces occur at midstrokes. There is no evidence for large force peaks at the stroke transitions due to either rapid fin rotation (supination) or rapid fin closure against the body. The energetics of pectoral fin rowing are estimated using the unsteady blade-element model and an indirect method based on the center of mass dynamics. The results indicate that the mechanical efficiency of pectoral fin rowing is low (0.1–0.3) relative to a flapping mechanism and possibly relative to axial undulation at comparable speeds.