Scaling of fast-start performance and its thermal dependence in mummichog Fundulus heteroclitus.

Fast-start predator-escape performance and its sensitivity to temperature (24, 30, and 36°C) were evaluated in mummichog Fundulus heteroclitus across a range of body sizes spanning YOY to adult (35-68 mm standard length). Mummichogs exhibit isometry of body dimensions and areas of the dorsal and anal fins but negative allometry of the caudal fin area. These scaling relationships are consistent with observed decreases in fast-start angular velocities with increasing body size. Linear velocity, on the contrary, does not vary with size, and both large and small mummichogs are capable of traversing similar distances in a given amount of time. In addition, temperature influences fast-start performance in similar ways over the size range, though the magnitude of the effect varies with size for some performance measures. In general, fast-start performance increases with test temperature, but mummichogs acclimated to warmer temperatures exhibit lower performance at each test temperature. Altogether, our results suggest that mummichogs across the adult size range may suffer decreases in their predator-escape performance as increasing sea temperatures combine with short-term temperature fluctuations in the estuaries these fish occupy.

Gliding Dragons and Flying Squirrels: Diversifying versus Stabilizing Selection on Morphology following the Evolution of an Innovation.

Evolutionary innovations and ecological competition are factors often cited as drivers of adaptive diversification. Yet many innovations result in stabilizing rather than diversifying selection on morphology, and morphological disparity among coexisting species can reflect competitive exclusion (species sorting) rather than sympatric adaptive divergence (character displacement). We studied the innovation of gliding in dragons (Agamidae) and squirrels (Sciuridae) and its effect on subsequent body size diversification. We found that gliding either had no impact (squirrels) or resulted in strong stabilizing selection on body size (dragons). Despite this constraining effect in dragons, sympatric gliders exhibit greater size disparity compared with allopatric gliders, a pattern consistent with, although not exclusively explained by, ecological competition changing the adaptive landscape of body size evolution to induce character displacement. These results show that innovations do not necessarily instigate further differentiation among species, as is so often assumed, and suggest that competition can be a powerful force generating morphological divergence among coexisting species, even in the face of strong stabilizing selection.

Fast-start escape performance across temperature and salinity gradients in mummichog Fundulus heteroclitus.

Fast-start predator-escape performance of mummichogs Fundulus heteroclitus was tested across field-informed variation in temperature (24, 30 and 36°C) and salinity (2, 12 and 32 ppt). Performance was similar across temperatures and salinities when fish were allowed to acclimate to these conditions. However, when mummichogs experienced acute temperature changes, performance exhibited thermal dependence in two contrasting ways. Fast-start turning rates and linear speeds varied directly with the temperature at which the manoeuvre was executed, but these aspects of performance varied inversely with acclimation temperature, with cool-acclimated fish exhibiting faster starts across test temperatures. Temperature effects were consistent across salinities. These results suggest that while mummichogs increase performance with acute temperature increases, long-term rises in sea temperature may cause these fish to become more susceptible to predation during abrupt cooling events, such as when storm events flood shallow water estuaries with cool rainwater.

Imperfect morphological convergence: variable changes in cranial structures underlie transitions to durophagy in moray eels.

Convergence is central to the study of evolution because it demonstrates the power of natural selection to deterministically shape phenotypic diversity. However, the conditions under which a common morphology repeatedly evolves may be restrictive. Many factors, such as differing genetic and environmental backgrounds and many-to-one mapping of form to function, contribute to variability in responses to selection. Nevertheless, lineages may evolve similar, even if not identical, forms given a shared selective regime, providing opportunities to examine the relative importance of natural selection, constraint, and contingency. Here, we show that following 10 transitions to durophagy (eating hard-shelled prey) in moray eels (Muraenidae), cranial morphology repeatedly evolved toward a novel region of morphological space indicative of enhanced feeding performance on hard prey. Disparity among the resulting 15 durophagous species, however, is greater than disparity among ancestors that fed on large evasive prey, contradicting the pattern expected under convergence. This elevated disparity is a consequence of lineage-specific responses to durophagy, in which independent transitions vary in the suites of traits exhibiting the largest changes. Our results reveal a pattern of imperfect convergence, which suggests shared selection may actually promote diversification because lineages often differ in their phenotypic responses to similar selective demands.

Biomechanical trade-offs bias rates of evolution in the feeding apparatus of fishes.

Morphological diversification does not proceed evenly across the organism. Some body parts tend to evolve at higher rates than others, and these rate biases are often attributed to sexual and natural selection or to genetic constraints. We hypothesized that variation in the rates of morphological evolution among body parts could also be related to the performance consequences of the functional systems that make up the body. Specifically, we tested the widely held expectation that the rate of evolution for a trait is negatively correlated with the strength of biomechanical trade-offs to which it is exposed. We quantified the magnitude of trade-offs acting on the morphological components of three feeding-related functional systems in four radiations of teleost fishes. After accounting for differences in the rates of morphological evolution between radiations, we found that traits that contribute more to performance trade-offs tend to evolve more rapidly, contrary to the prediction. While ecological and genetic factors are known to have strong effects on rates of phenotypic evolution, this study highlights the role of the biomechanical architecture of functional systems in biasing the rates and direction of trait evolution.

An integrative modeling approach to elucidate suction-feeding performance.

Research on suction-feeding performance has mostly focused on measuring individual underlying components such as suction pressure, flow velocity, ram or the effects of suction-induced forces on prey movement during feeding. Although this body of work has advanced our understanding of aquatic feeding, no consensus has yet emerged on how to combine all of these variables to predict prey-capture performance. Here, we treated the aquatic predator-prey encounter as a hydrodynamic interaction between a solid particle (representing the prey) and the unsteady suction flows around it, to integrate the effects of morphology, physiology, skull kinematics, ram and fluid mechanics on suction-feeding performance. We developed the suction-induced force-field (SIFF) model to study suction-feeding performance in 18 species of centrarchid fishes, and asked what morphological and functional traits underlie the evolution of feeding performance on three types of prey. Performance gradients obtained using SIFF revealed that different trait combinations contribute to the ability to feed on attached, evasive and (strain-sensitive) zooplanktonic prey because these prey types impose different challenges on the predator. The low overlap in the importance of different traits in determining performance also indicated that the evolution of suction-feeding ability along different ecological axes is largely unconstrained. SIFF also yielded estimates of feeding ability that performed better than kinematic traits in explaining natural patterns of prey use. When compared with principal components describing variation in the kinematics of suction-feeding events, SIFF output explained significantly more variation in centrarchid diets, suggesting that the inclusion of more mechanistic hydrodynamic models holds promise for gaining insight into the evolution of aquatic feeding performance.

A Comparative Approach to Understanding Floral Adaptation to Climate and Pollinators During Diversification in European and Mediterranean Silene.

Pollinator selection on floral traits is a well-studied phenomenon, but less is known about the influence of climate on this species interaction. Floral trait evolution could be a result of both adaptation to climate and pollinator-mediated selection. In addition, climate may also determine pollinator communities, leading to an indirect influence of climate on floral traits. In this study, we present evidence of both direct and indirect effects of climate on plant morphology through a phylogenetic comparative analysis of the relationships between climate, pollinators, and morphology in 89 European and Mediterranean Silene species. Climate directly influences vegetative morphology, where both leaf size and internode length were found to be smaller in habitats that are warmer in the driest quarter of the year and that have more precipitation in the coldest quarter of the year. Similarly, flower size was directly influenced by climate, where smaller calyxes were also associated with habitats that are warmer in the driest quarter of the year. These results suggest that reduced leaf and flower size promote water conservation in species that occupy arid climates. Floral traits also evolved in response to pollinators, with elongated calyxes associated with nocturnal pollination, though we also found evidence that climate influences pollinator distribution. Nocturnal pollinators of Silene are found in habitats that have more temperature evenness across seasons than diurnal pollinators. Correspondingly, nocturnally-pollinated Silene are more likely to occur in habitats that have lower daily temperature fluctuation and more temperature evenness across seasons. Altogether these results show that climate can directly influence vegetative and floral morphology, but it can also affect pollinator distribution, which in turn drives floral adaptation. Our study therefore suggests that climate mediates the influence of species interactions on trait evolution by imposing direct selective demands on floral phenotypes and by determining the pollinator community that imposes its own selective demands on flowers.

Functional complexity can mitigate performance trade-offs.

Trade-offs are believed to impose major constraints on adaptive evolution, and they arise when modification of a trait improves one aspect of performance but incurs a cost in another. Here we show that performance costs that result from competing demands on one trait can be mitigated by compensatory changes in other traits, so long as performance has a complex basis. Numerical simulations indicate that increases in the number of traits that determine performance decrease the strength of performance trade-offs. In centrarchid fishes, multiple traits underlie suction feeding performance, and experimental data and hydrodynamic modeling show that combinations of traits evolve to increase the ability to feed on attached prey while mitigating costs to performance on evasive prey. Diet data for centrarchid species reveal a weak trade-off between these prey types, corroborating the results based on hydrodynamic modeling and suggesting that complexity in the functional basis of suction feeding performance enhances trophic diversification. Complexity may thus permit the evolution of combinations of high-performance behaviors that appear to violate underlying trade-offs, such as the ability to exert high suction forces with large gape. This phenomenon may promote morphological, functional, and ecological diversification in the face of the myriad selective demands organisms encounter.

Body shape transformations by alternate anatomical adaptive peak shifts in blenniiform fishes.

Extreme body elongation has occurred repeatedly in the evolutionary history of ray-finned fishes. Lengthening of the anterior-posterior body axis relative to depth and width can involve changes in the cranial skeleton and vertebral column, but to what extent is anatomical evolution determined by selective factors and intrinsic constraints that are shared broadly among closely related lineages? In this study, we fit adaptive (Ornstein-Uhlenbeck) evolutionary models to body shape and its anatomical determinants and identified two instances of extreme elongation by divergent anatomical peak shifts in the Blenniiformes, a radiation of small-bodied substrate-associated marine teleost fishes. Species in the genus Xiphasia (hairtail blennies) evolved toward a peak defined by a highly elongated caudal vertebral region but ancestral cranial and precaudal vertebral morphology. In contrast, a clade that includes the genera Chaenopsis and Lucayablennius (pike and arrow blennies) evolved toward a peak with a long slender skull but ancestral axial skeletal anatomy. Neither set of anatomical peak shifts aligns closely with the major axis of anatomical diversification in other blenniiform fishes. These results provide little evidence that ancestral constraints have affected body shape transformation, and instead suggest that extreme elongation arose with distinct shifts in selective factors and development.

Phylogenetic signal, evolutionary process, and rate.

A recent advance in the phylogenetic comparative analysis of continuous traits has been explicit, model-based measurement of "phylogenetic signal" in data sets composed of observations collected from species related by a phylogenetic tree. Phylogenetic signal is a measure of the statistical dependence among species' trait values due to their phylogenetic relationships. Although phylogenetic signal is a measure of pattern (statistical dependence), there has nonetheless been a widespread propensity in the literature to attribute this pattern to aspects of the evolutionary process or rate. This may be due, in part, to the perception that high evolutionary rate necessarily results in low phylogenetic signal; and, conversely, that low evolutionary rate or stabilizing selection results in high phylogenetic signal (due to the resulting high resemblance between related species). In this study, we use individual-based numerical simulations on stochastic phylogenetic trees to clarify the relationship between phylogenetic signal, rate, and evolutionary process. Under the simplest model for quantitative trait evolution, homogeneous rate genetic drift, there is no relation between evolutionary rate and phylogenetic signal. For other circumstances, such as functional constraint, fluctuating selection, niche conservatism, and evolutionary heterogeneity, the relationship between process, rate, and phylogenetic signal is complex. For these reasons, we recommend against interpretations of evolutionary process or rate based on estimates of phylogenetic signal.

Discordance between morphological and mechanical diversity in the feeding mechanism of centrarchid fishes.

Morphological diversity is routinely used to infer ecological variation among species because differences in form underlie variation in functional performance of ecological tasks like capturing prey, avoiding predators, or defending territories. However, many functions have complex morphological bases that can weaken associations between morphological and functional diversification. We investigate the link between these levels of diversity in a mechanically explicit model of fish suction-feeding performance, where the map of head morphology to feeding mechanics is many-to-one: multiple, alternative forms can produce the same mechanical property. We show that many-to-one mapping leads to discordance between morphological and mechanical diversity in the freshwater fish family, the Centrarchidae, despite close associations between morphological changes and their mechanical effects. We find that each of the model's five morphological variables underlies evolution of suction capacity. Yet, the major centrarchid clades exhibit an order of magnitude range in diversity of suction mechanics in the absence of any clear difference in diversity of the morphological variables. This cryptic pattern of mechanical diversity suggests an evolutionary history for suction performance that is unlike the one inferred from comparisons of morphological diversity. Because many-to-one mapping is likely to be common in functional systems, this property of design may lead to widespread discordance between functional and morphological diversity. Although we focus on the interaction between morphology and mechanics, many-to-one mapping can decouple diversity between levels of organization in any hierarchical system.

Body shape transformation along a shared axis of anatomical evolution in labyrinth fishes (Anabantoidei).

Major morphological transformations, such as the evolution of elongate body shape in vertebrates, punctuate evolutionary history. A fundamental step in understanding the processes that give rise to such transformations is identification of the underlying anatomical changes. But as we demonstrate in this study, important insights can also be gained by comparing these changes to those that occur in ancestral and closely related lineages. In labyrinth fishes (Anabantoidei), rapid evolution of a highly derived torpedo-shaped body in the common ancestor of the pikehead (Luciocephalus aura and L. pulcher) occurred primarily through exceptional elongation of the head, with secondary contributions involving reduction in body depth and lengthening of the precaudal vertebral region. This combination of changes aligns closely with the primary axis of anatomical diversification in other anabantoids, revealing that pikehead evolution involved extraordinarily rapid change in structures that were ancestrally labile. Finer-scale examination of the anatomical components that determine head elongation also shows alignment between the pikehead evolutionary trajectory and the primary axis of cranial diversification in anabantoids, with much higher evolutionary rates leading to the pikehead. Altogether, our results show major morphological transformation stemming from extreme change along a shared morphological axis in labyrinth fishes.

Ecological specialization and morphological diversification in Greater Antillean boas.

Colonization of islands can dramatically influence the evolutionary trajectories of organisms, with both deterministic and stochastic processes driving adaptation and diversification. Some island colonists evolve extremely large or small body sizes, presumably in response to unique ecological circumstances present on islands. One example of this phenomenon, the Greater Antillean boas, includes both small (<90 cm) and large (4 m) species occurring on the Greater Antilles and Bahamas, with some islands supporting pairs or trios of body-size divergent species. These boas have been shown to comprise a monophyletic radiation arising from a Miocene dispersal event to the Greater Antilles, though it is not known whether co-occurrence of small and large species is a result of dispersal or in situ evolution. Here, we provide the first comprehensive species phylogeny for this clade combined with morphometric and ecological data to show that small body size evolved repeatedly on separate islands in association with specialization in substrate use. Our results further suggest that microhabitat specialization is linked to increased rates of head shape diversification among specialists. Our findings show that ecological specialization following island colonization promotes morphological diversity through deterministic body size evolution and cranial morphological diversification that is contingent on island- and species-specific factors.

Comparative analysis of morphological diversity: does disparity accumulate at the same rate in two lineages of centrarchid fishes?

Evolutionary lineages differ with regard to the variety of forms they exhibit. We investigated whether comparisons of morphological diversity can be used to identify differences in ecological diversity in two sister clades of centrarchid fishes. Species in the Lepomis clade (sunfishes) feed on a wider range of prey items than species in the Micropterus clade (black basses). We quantified disparity in morphology of the feeding apparatus as within-clade variance on principal components and found that Lepomis exhibits 4.4 and 7.4 times more variance than Micropterus on the first two principal components. However, lineages are expected to diversify morphologically and ecologically given enough time, and this pattern could have arisen due to differences in the amount of time each clade has had to accumulate variance. Despite being sister groups, the age of the most recent common ancestor of Lepomis is approximately 14.6 million years ago and its lineages have a total length of 86.4 million years while the age of the most recent common ancestor of Micropterus is only about 8.4 million years ago, and it has a total branch length of 42.9 million years. We used the Brownian motion model of character evolution to test the hypothesis that time of independent evolution of each clade's lineages accounts for differences in morphological disparity and determined that the rates of evolution of the first two principal components are 4.4 and 7.7 times greater in Lepomis. Thus, time and phylogeny do not account for the differences in morphological disparity observed in Lepomis and Micropterus, and other diversity-promoting mechanisms should be investigated.

Biting disrupts integration to spur skull evolution in eels.

The demand that anatomical structures work together to perform biological functions is thought to impose strong limits on morphological evolution. Breakthroughs in diversification can occur, however, when functional integration among structures is relaxed. Although such transitions are expected to generate variation in morphological diversification across the tree of life, empirical tests of this hypothesis are rare. Here we show that transitions between suction-based and biting modes of prey capture, which require different degrees of coordination among skull components, are associated with shifts in the pattern of skull diversification in eels (Anguilliformes). Biting eels have experienced greater independence of the jaws, hyoid and operculum during evolution and exhibit more varied morphologies than closely related suction feeders, and this pattern reflects the weakened functional integration among skull components required for biting. Our results suggest that behavioural transitions can change the evolutionary potential of the vertebrate skeleton by altering functional relationships among structures.

A revised metric for quantifying body shape in vertebrates.

Vertebrates exhibit tremendous diversity in body shape, though quantifying this variation has been challenging. In the past, researchers have used simplified metrics that either describe overall shape but reveal little about its anatomical basis or that characterize only a subset of the morphological features that contribute to shape variation. Here, we present a revised metric of body shape, the vertebrate shape index (VSI), which combines the four primary morphological components that lead to shape diversity in vertebrates: head shape, length of the second major body axis (depth or width), and shape of the precaudal and caudal regions of the vertebral column. We illustrate the usefulness of VSI on a data set of 194 species, primarily representing five major vertebrate clades: Actinopterygii, Lissamphibia, Squamata, Aves, and Mammalia. We quantify VSI diversity within each of these clades and, in the course of doing so, show how measurements of the morphological components of VSI can be obtained from radiographs, articulated skeletons, and cleared and stained specimens. We also demonstrate that head shape, secondary body axis, and vertebral characteristics are important independent contributors to body shape diversity, though their importance varies across vertebrate groups. Finally, we present a functional application of VSI to test a hypothesized relationship between body shape and the degree of axial bending associated with locomotor modes in ray-finned fishes. Altogether, our study highlights the promise VSI holds for identifying the morphological variation underlying body shape diversity as well as the selective factors driving shape evolution.

Evolution of extreme body size disparity in monitor lizards (Varanus).

Many features of species' biology, including life history, physiology, morphology, and ecology are tightly linked to body size. Investigation into the causes of size divergence is therefore critical to understanding the factors shaping phenotypic diversity within clades. In this study, we examined size evolution in monitor lizards (Varanus), a clade that includes the largest extant lizard species, the Komodo dragon (V. komodoensis), as well as diminutive species that are nearly four orders of magnitude smaller in adult body mass. We demonstrate that the remarkable body size disparity of this clade is a consequence of different selective demands imposed by three major habitat use patterns-arboreality, terrestriality, and rock-dwelling. We reconstructed phylogenetic relationships and ancestral habitat use and applied model selection to determine that the best-fitting evolutionary models for species' adult size are those that infer oppositely directed adaptive evolution associated with terrestriality and rock-dwelling, with terrestrial lineages evolving extremely large size and rock-dwellers becoming very small. We also show that habitat use affects the evolution of several ecologically important morphological traits independently of body size divergence. These results suggest that habitat use exerts a strong, multidimensional influence on the evolution of morphological size and shape disparity in monitor lizards.

Functional innovations and morphological diversification in parrotfish.

The association between diversification and evolutionary innovations has been well documented and tested in studies of taxonomic richness but the impact that such innovations have on the diversity of form and function is less well understood. Using phylogenetically rigorous techniques, we investigated the association between morphological diversity and two design breakthroughs within the jaws of parrotfish. Similar intramandibular joints and other modifications of the pharyngeal jaws have evolved repeatedly in teleost fish and are frequently hypothesized to promote diversity. We quantified morphological diversity within six functionally important oral jaw traits using the Brownian motion rate of evolution to correct for phylogenetic and time-related biases and compared these rates across clades that did and did not possess the intramandibular joint and the parrotfish pharyngeal jaw. No change in morphological diversity was associated with the pharyngeal jaw modification alone but rates of oral jaw diversification were up to 8× faster in parrotfish species that possessed both innovations. Interestingly, this morphological diversity may not have led to differential resource uses as available data suggest that members of this clade show remarkable homogeneity of diet.

Phylogenetic analysis of the evolutionary correlation using likelihood.

Many evolutionary processes can lead to a change in the correlation between continuous characters over time or on different branches of a phylogenetic tree. Shifts in genetic or functional constraint, in the selective regime, or in some combination thereof can influence both the evolution of continuous traits and their relation to each other. These changes can often be mapped on a phylogenetic tree to examine their influence on multivariate phenotypic diversification. We propose a new likelihood method to fit multiple evolutionary rate matrices (also called evolutionary variance-covariance matrices) to species data for two or more continuous characters and a phylogeny. The evolutionary rate matrix is a matrix containing the evolutionary rates for individual characters on its diagonal, and the covariances between characters (of which the evolutionary correlations are a function) elsewhere. To illustrate our approach, we apply the method to an empirical dataset consisting of two features of feeding morphology sampled from 28 centrarchid fish species, as well as to data generated via phylogenetic numerical simulations. We find that the method has appropriate type I error, power, and parameter estimation. The approach presented herein is the first to allow for the explicit testing of how and when the evolutionary covariances between characters have changed in the history of a group.

Piscivory limits diversification of feeding morphology in centrarchid fishes.

Proximity to an adaptive peak influences a lineage's potential to diversify. We tested whether piscivory, a high quality but functionally demanding trophic strategy, represents an adaptive peak that limits morphological diversification in the teleost fish clade, Centrarchidae. We synthesized published diet data and applied a well-resolved, multilocus and time-calibrated phylogeny to reconstruct ancestral piscivory. We measured functional features of the skull and performed principal components analysis on species' values for these variables. To assess the role of piscivory on morphological diversification, we compared the fit of several models of evolution for each principal component (PC), where model parameters were allowed to vary between lineages that differed in degree of piscivory. According to the best-fitting model, two adaptive peaks influenced PC 1 evolution, one peak shared between highly and moderately piscivorous lineages and another for nonpiscivores. Brownian motion better fit PCs 2, 3, and 4, but the best Brownian models infer a slow rate of PC 2 evolution shared among all piscivores and a uniquely slow rate of PC 4 evolution in highly piscivorous lineages. These results suggest that piscivory limits feeding morphology diversification, but this effect is most severe in lineages that exhibit an extreme form of this diet.