Elongation of the body in eels

The shape of the body affects how organisms move, where they live, and how they feed. One body plan that has long engaged the interest of both evolutionary biologists and functional morphologists is axial elongation. There is a growing interest in the correlates and evolution of elongation within different terrestrial and aquatic vertebrate clades. At first glance, Anguilliformes may appear to exhibit a single cylindrical form but there is considerable diversity underlying this seemingly simplified body plan. Here, we explore evolution of the axial skeleton in 54 anguilliform taxa and some close relatives. We describe the diversity of axial elongation as well as investigate how characters such as head length, branchial-arch length, and shape of the pectoral fins correlate with vertebral number to possibly facilitate changes in absolute diameter of the body. Overall, we find that precaudal vertebral numbers and caudal vertebral numbers are evolving independently across elopomorph fishes. We also find that precaudal and caudal vertebral aspect ratios are evolving together across elopomorph fishes. When focusing within Anguilliformes we find striking diversity in the mechanisms of elongation of the body, including almost every trend for axial elongation known within actinopterygian fishes. The three major clades of eels we examined have slightly different mechanisms of elongation. We also find a suite of morphological characters associated with elongation in anguilliform fishes that appears to coincide with a more fossorial lifestyle such as high elongation ratios, a more posteriorly extended-branchial region, and a reduction in the size of the pectoral fins. Lastly, we point out that a diverse range of derived behaviors such as head- and tail-first burrowing, rotational feeding, and knotting around prey are only found in long cylindrical vertebrates.     

Head‐turning morphologies: Evolution of shape diversity in the mammalian atlas–axis complex

Mammals flex, extend, and rotate their spines as they perform behaviors critical for survival, such as foraging, consuming prey, locomoting, and interacting with conspecifics or predators. The atlas–axis complex is a mammalian innovation that allows precise head movements during these behaviors. Although morphological variation in other vertebral regions has been linked to ecological differences in mammals, less is known about morphological specialization in the cervical vertebrae, which are developmentally constrained in number but highly variable in size and shape. Here, we present the first phylogenetic comparative study of the atlas–axis complex across mammals. We used spherical harmonics to quantify 3D shape variation of the atlas and axis across a diverse sample of species, and performed phylogenetic analyses to investigate if vertebral shape is associated with body size, locomotion, and diet. We found that differences in atlas and axis shape are partly explained by phylogeny, and that mammalian subclades differ in morphological disparity. Atlas and axis shape diversity is associated with differences in body size and locomotion; large terrestrial mammals have craniocaudally elongated vertebrae, whereas smaller mammals and aquatic mammals have more compressed vertebrae. These results provide a foundation for investigating functional hypotheses underlying the evolution of neck morphologies across mammals.     

Vertebral evolution and the diversification of squamate reptiles

Taxonomic, morphological, and functional diversity are often discordant and independent components of diversity. A fundamental and largely unanswered question in evolutionary biology is why some clades diversify primarily in some of these components and not others. Dramatic variation in trunk vertebral numbers (14 to >300) among squamate reptiles coincides with different body shapes, and snake-like body shapes have evolved numerous times. However, whether increased evolutionary rates or numbers of vertebrae underlie body shape and taxonomic diversification is unknown. Using a supertree of squamates including 1375 species, and corresponding vertebral and body shape data, we show that increased rates of evolution in vertebral numbers have coincided with increased rates and disparity in body shape evolution, but not changes in rates of taxonomic diversification. We also show that the evolution of many vertebrae has not spurred or inhibited body shape or taxonomic diversification, suggesting that increased vertebral number is not a key innovation. Our findings demonstrate that lineage attributes such as the relaxation of constraints on vertebral number can facilitate the evolution of novel body shapes, but that different factors are responsible for body shape and taxonomic diversification.     

Evolutionary history of elongation and maximum body length in moray eels (Anguilliformes: Muraenidae)

Body shape and size are important axes of organismal diversification. The elongate body form has evolved repeatedly in disparate vertebrate clades, and is associated with a variety of maximum body lengths. We used a time‐calibrated phylogeny for 40 species of moray eels to analyse the evolution of elongation and the morphological mechanisms underlying variation in body shape and maximum body length. We find that body elongation in morays evolves independently of elongation of the vertebral column. In contrast, maximum body length evolves by a different mechanism: through region‐specific increases in vertebral number, elongation of individual vertebral centra, and postembryonic somatic growth. We reconstruct an ancestral moray eel and provide evidence for accelerated morphological evolution in three highly elongate species that are associated with a burrowing lifestyle. We compare these patterns with those described for other vertebrates, and show that body shape and body length may evolve independently of each other and (in the case of shape) of the vertebral column. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 861–875.     

A Morphospace for Reef Fishes: Elongation Is the Dominant Axis of Body Shape Evolution

Tropical reef fishes are widely regarded as being perhaps the most morphologically diverse vertebrate assemblage on earth, yet much remains to be discovered about the scope and patterns of this diversity. We created a morphospace of 2,939 species spanning 56 families of tropical Indo-Pacific reef fishes and established the primary axes of body shape variation, the phylogenetic consistency of these patterns, and whether dominant patterns of shape change can be accomplished by diverse underlying changes. Principal component analysis showed a major axis of shape variation that contrasts deep-bodied species with slender, elongate forms. Furthermore, using custom methods to compare the elongation vector (axis that maximizes elongation deformation) and the main vector of shape variation (first principal component) for each family in the morphospace, we showed that two thirds of the families diversify along an axis of body elongation. Finally, a comparative analysis using a principal coordinate analysis based on the angles among first principal component vectors of each family shape showed that families accomplish changes in elongation with a wide range of underlying modifications. Some groups such as Pomacentridae and Lethrinidae undergo decreases in body depth with proportional increases in all body regions, while other families show disproportionate changes in the length of the head (e.g., Labridae), the trunk or caudal region in all combinations (e.g., Pempheridae and Pinguipedidae). In conclusion, we found that evolutionary changes in body shape along an axis of elongation dominates diversification in reef fishes. Changes in shape on this axis are thought to have immediate implications for swimming performance, defense from gape limited predators, suction feeding performance and access to some highly specialized habitats. The morphological modifications that underlie changes in elongation are highly diverse, suggesting a role for a range of developmental processes and functional consequences.     

Differential occupation of axial morphospace

The postcranial system is composed of the axial and appendicular skeletons. The axial skeleton, which consists of serially repeating segments commonly known as vertebrae, protects and provides leverage for movement of the body. Across the vertebral column, much numerical and morphological diversity can be observed, which is associated with axial regionalization. The present article discusses this basic diversity and the early developmental mechanisms that guide vertebral formation and regionalization. An examination of vertebral numbers across the major vertebrate clades finds that actinopterygian and chondrichthyan fishes tend to increase vertebral number in the caudal region whereas Sarcopterygii increase the number of vertebrae in the precaudal region, although exceptions to each trend exist. Given the different regions of axial morphospace that are occupied by these groups, differential developmental processes control the axial patterning of actinopterygian and sarcopterygian species. It is possible that, among a variety of factors, the differential selective regimes for aquatic versus terrestrial locomotion have led to the differential use of axial morphospace in vertebrates.     

Shared extremes by ectotherms and endotherms: Body elongation in mustelids is associated with small size and reduced limbs

An elongate body with reduced or absent limbs has evolved independently in many ectothermic vertebrate lineages. While much effort has been spent examining the morphological pathways to elongation in these clades, quantitative investigations into the evolution of elongation in endothermic clades are lacking. We quantified body shape in 61 musteloid mammals (red panda, skunks, raccoons, and weasels) using the head‐body elongation ratio. We also examined the morphological changes that may underlie the evolution toward more extreme body plans. We found that a mustelid clade comprised of the subfamilies Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae exhibited an evolutionary transition toward more elongate bodies. Furthermore, we discovered that elongation of the body is associated with the evolution of other key traits such as a reduction in body size and a reduction in forelimb length but not hindlimb length. This relationship between body elongation and forelimb length has not previously been quantitatively established for mammals but is consistent with trends exhibited by ectothermic vertebrates and suggests a common pattern of trait covariance associated with body shape evolution. This study provides the framework for documenting body shapes across a wider range of mammalian clades to better understand the morphological changes influencing shape disparity across all vertebrates.     

Variation in morphology and functional performance across distinct evolutionary lineages of the Moorish gecko (Tarentola mauritanica) from the Iberian Peninsula

Deciphering the mechanisms that underlie morphological and functional diversity is essential for understanding how organisms adapt to their environment. Interestingly, phenotypic divergence does not necessarily correspond to the geographic and genetic separation between populations. Here, we explored the morphological and functional divergence among populations of two genetically differentiated clades of the Moorish gecko, Tarentola mauritanica. We used linear and geometric morphometrics to quantify morphological variation and investigated how it translates into biting and CLIMBING PERFORMANCE, to better understand the mechanisms potentially underlying population and lineage divergence. We found marked morphological differences between clades, both in body size and head shape. However, much of this differentiation is more strongly related to local variation between populations of the same clade, suggesting that recent ecological events may be more influential than deep evolutionary history in shaping diversity patterns in this group. Despite a lack of association between morphology and functional diversification in the locomotor system of the Moorish gecko, straightforward links are observed between head morphology and biting performance, providing more hints on the possible underlying causes. Indeed, variation in bite force is mostly determined by size variation and sexual dimorphism, and differences between the two clades concern how sexual variation is expressed, reinforcing the idea that both social and ecological factors contribute in shaping differentiation. Interestingly, the individuals from the islets off the coast of Murcia exhibit particular morphological and functional traits, which suggests that the ecological conditions related to insularity may drive the phenotypic differentiation of this population.     

What explains patterns of species richness? The relative importance of climatic‐niche evolution,morphological evolution,and ecological limits in salamanders

A major goal of evolutionary biology and ecology is to understand why species richness varies among clades. Previous studies have suggested that variation in richness among clades might be related to variation in rates of morphological evolution among clades (e.g., body size and shape). Other studies have suggested that richness patterns might be related to variation in rates of climatic‐niche evolution. However, few studies, if any, have tested the relative importance of these variables in explaining patterns of richness among clades. Here, we test their relative importance among major clades of Plethodontidae, the most species‐rich family of salamanders. Earlier studies have suggested that climatic‐niche evolution explains patterns of diversification among plethodontid clades, whereas rates of morphological evolution do not. A subsequent study stated that rates of morphological evolution instead explained patterns of species richness among plethodontid clades (along with “ecological limits” on richness of clades, leading to saturation of clades with species, given limited resources). However, they did not consider climatic‐niche evolution. Using phylogenetic multiple regression, we show that rates of climatic‐niche evolution explain most variation in richness among plethodontid clades, whereas rates of morphological evolution do not. We find little evidence that ecological limits explain patterns of richness among plethodontid clades. We also test whether rates of morphological and climatic‐niche evolution are correlated, and find that they are not. Overall, our results help explain richness patterns in a major amphibian group and provide possibly the first test of the relative importance of climatic niches and morphological evolution in explaining diversity patterns.     

TESTING FOR ANCIENT ADAPTIVE RADIATIONS IN NEOTROPICAL CICHLID FISHES

Most contemporary studies of adaptive radiation focus on relatively recent and geographically restricted clades. It is less clear whether diversification of ancient clades spanning entire continents is consistent with adaptive radiation. We used novel fossil calibrations to generate a chronogram of Neotropical cichlid fishes and to test whether patterns of lineage and morphological diversification are congruent with hypothesized adaptive radiations in South and Central America. We found that diversification in the Neotropical cichlid clade and the highly diverse tribe Geophagini was consistent with diversity‐dependent, early bursts of divergence followed by decreased rates of lineage accumulation. South American Geophagini underwent early rapid differentiation in body shape, expanding into novel morphological space characterized by elongate‐bodied predators. Divergence in head shape attributes associated with trophic specialization evolved under strong adaptive constraints in all Neotropical cichlid clades. The South American Cichlasomatini followed patterns consistent with constant rates of morphological divergence. Although morphological diversification in South American Heroini was limited, Eocene invasion of Central American habitats was followed by convergent diversification mirroring variation observed in Geophagini. Diversification in Neotropical cichlids was influenced by the early adaptive radiation of Geophagini, which potentially limited differentiation in other cichlid clades.     

Primate cranial diversity

Many studies in primate and human evolution focus on aspects of cranial morphology to address issues of systematics, phylogeny, and functional anatomy. However, broad analyses of cranial diversity within Primates as an Order are notably absent. In this study, we present a 3D geometric morphometric analysis of primate cranial morphology, providing a multivariate comparison of the major patterns of cranial shape change during primate evolution and quantitative assessments of cranial diversity among different clades. We digitized a set of 18 landmarks designed to capture overall cranial shape on male and female crania representing 66 genera of living primates. The landmark data were aligned using a Generalized Procrustes Analysis and then subjected to a principal components analysis to identify the major axes of cranial variation. Cranial diversity among clades was compared using multivariate measurements of variance. The first principal component axis reflects differences in cranial flexion, orbit size and orientation, and relative neurocranial volume. In general, it separates strepsirrhines from anthropoids. The second axis reflects differences in relative cranial height and snout length and primarily describes differences among anthropoids. Eulemur, Mandrillus, Pongo, and Homo are among the extremes in cranial shape. Anthropoids, catarrhines, and haplorhines show a higher variance than prosimians or strepsirrhines. Hominoids show the highest variance in cranial shape among extant primate clades, and much of this diversity is driven by the unique cranium of Homo sapiens. Am J Phys Anthropol 142:565–578, 2010. © 2010 Wiley‐Liss, Inc.     

Head shape evolution in monitor lizards (Varanus): interactions between extreme size disparity,phylogeny and ecology

Characterizing patterns of observed current variation, and testing hypotheses concerning the potential drivers of this variation, is fundamental to understanding how morphology evolves. Phylogenetic history, size and ecology are all central components driving the evolution of morphological variation, but only recently have methods become available to tease these aspects apart for particular body structures. Extant monitor lizards (Varanus) have radiated into an incredible range of habitats and display the largest body size range of any terrestrial vertebrate genus. Although their body morphology remains remarkably conservative, they have obvious head shape variation. We use two‐dimensional geometric morphometric techniques to characterize the patterns of dorsal head shape variation in 36 species (375 specimens) of varanid, and test how this variation relates to size, phylogenetic history and ecology as represented by habitat. Interspecific head shape disparity is strongly allometric. Once size effects are removed, principal component analysis shows that most shape variation relates to changes in the snout and head width. Size‐corrected head shape variation has strong phylogenetic signal at a broad level, but habitat use is predictive of shape disparity within phylogenetic lineages. Size often explains shape disparity among organisms; however, the ability to separate size and shape variation using geometric morphometrics has enabled the identification of phylogenetic history and habitat as additional key factors contributing to the evolution of head shape disparity among varanid lizards.     

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.     

MORPHOLOGICAL DIVERSIFICATION AND ADAPTIVE RADIATION: A COMPARISON OF TWO DIVERSE LIZARD CLADES

We compared the morphological diversity (i.e., the amount of morphological space occupied) of two similar clades, the lizard genera Anolis and Sceloporus. These species-rich monophyletic clades are similar in body size, age of origin, and many aspects of their natural history. We examined a number of morphological traits whose variation is likely to represent adaptation to different aspects of the environment, including body size, limb proportions, head dimensions, and tail length. Examination of the position of species in multidimensional space, based on a principal components analysis, indicates that the morphological diversity of Anolis, which we refer to as disparity, is significantly greater than that of Sceloporus. One potential explanation for this pattern is that morphological diversification in Anolis was facilitated by the evolution of subdigital toe-pads, which allow anoles to use the environment in ways not available to Sceloporus. The geographic location of diversification (tropical and subtropical for Anolis, arid for Sceloporus) may also have been important.     

Evolution of Cranial Shape in Caecilians (Amphibia: Gymnophiona)

Insights into morphological diversification can be obtained from the ways the species of a clade occupy morphospace. Projecting a phylogeny into morphospace provides estimates of evolutionary trajectories as lineages diversified information that can be used to infer the dynamics of evolutionary processes that produced patterns of morphospace occupation. We present here a large-scale investigation into evolution of morphological variation in the skull of caecilian amphibians, a major clade of vertebrates. Because caecilians are limbless, predominantly fossorial animals, diversification of their skull has occurred within a framework imposed by the functional demands of head-first burrowing. We examined cranial shape in 141 species, over half of known species, using X-ray computed tomography and geometric morphometrics. Mapping an existing phylogeny into the cranial morphospace to estimate the history of morphological change (phylomorphospace), we find a striking pattern: most species occupy distinct clusters in cranial morphospace that closely correspond to the main caecilian clades, and each cluster is separated by unoccupied morphospace. The empty spaces in shape space are unlikely to be caused entirely by extinction or incomplete sampling. The main caecilian clades have different amounts of morphological disparity, but neither clade age nor number of species account for this variation. Cranial shape variation is clearly linked to phyletic divergence, but there is also homoplasy, which is attributed to extrinsic factors associated with head-first digging: features of caecilian crania that have been previously argued to correlate with differential microhabitat use and burrowing ability, such as subterminal and terminal mouths, degree of temporal fenestration (stegokrotaphy/zygokrotaphy), and eyes covered by bone, have evolved and many combinations occur in modern species. We find evidence of morphological convergence in cranial shape, among species that have eyes covered by bone, resulting in a narrow bullet-shaped head. These results reveal a complex history, including early expansion of morphospace and both divergent and convergent evolution resulting in the diversity we observe today.     

Postmetamorphic ontogenetic allometry and the evolution of skull shape in Nest‐building frogs Leptodactylus (Anura: Leptodactylidae)

Allometry constitutes an important source of morphological variation. However, its influence in head development in anurans has been poorly explored. By using geometric morphometrics followed by statistical and comparative methods we analyzed patterns of allometric change during cranial postmetamorphic ontogeny in species of Nest‐building frogs Leptodactylus (Leptodactylidae). We found that the anuran skull is not a static structure, and allometry plays an important role in defining its shape in this group. Similar to other groups with biphasic life‐cycle, and following a general trend in vertebrates, ontogenetic changes mostly involve rearrangement in rostral, otoccipital, and suspensorium regions. Ontogenetic transformations are paralleled by shape changes associated with evolutionary change in size, such that the skulls of species of different intrageneric groups are scaled to each other, and small and large species show patterns of paedomorphic/peramorphic features, respectively. Allometric trajectories producing those phenotypes are highly evolvable though, with shape change direction and magnitude varying widely among clades, and irrespective of changes in absolute body size. These results reinforce the importance of large‐scale comparisons of growth patterns to understand the plasticity, evolution, and polarity of morphological changes in different clades.     

Morphological differentiation among populations of Rhinella marina (Amphibia: Anura) in western Mexico

Conspecific populations inhabiting different environments may exhibit morphological differences, potentially reflecting differential local adaptation. In anuran amphibians, morphology of the pelvis and hindlimbs may often experience strong selection due to effects on locomotion. In this study, we used the cane toad Rhinella marina to test the hypothesis that populations experiencing a higher abundance of predators should suffer higher mortality rates and exhibit morphological traits associated with enhanced locomotor performance (narrower pelvis and head, longer pelvis and hindlimbs, shorter presacral vertebral column). We investigated inter-population variation in survival rate, abundance of predators, and body shape across five populations in rivers in western Mexico. We conducted (1) mark-recapture experiments to calculate survival rates, (2) linear transects with point counts to estimate abundance of predatory spiders, snakes, and birds, and (3) geometric morphometric analyses to investigate body shape variation. We found significant differences among populations in survival rates, abundance of predators, and body shape. However, these three variables were not necessarily inter-related. Increased predator abundance did not result in decreased survival rates, suggesting other causes of mortality affect these populations. While some morphological differences supported our predictions (trend for longer pelvis, shorter presacral vertebral column, and narrower head in sites with increased abundance of spiders and snakes), other aspects of morphology did not. We discuss alternative explanations for the lack of clear associations between predation, survival, and morphology.     

Predictors of body shape among populations of a stream fish (Cyprinella venusta,Cypriniformes: Cyprinidae)

Performance‐related variation in fitness can manifest as morphological responses to ecological and evolutionary pressures. Eco‐morphological studies often utilize stark binary comparisons, such as lentic to lotic populations of freshwater fishes, to characterize relationships between form and function despite possible complications from confounding factors. In the present study, we compared body shape variation among lotic populations of a stream fish (Cyprinella venusta Girard) to disentangle the influence of ecological and evolutionary drivers of phenotypic change. We assessed the extent to which body shape corresponded to three key environmental factors (mean channel velocity, mean discharge, and mean annual run‐off), phylogeny (mitochondrial DNA divergence), and body size (centroid size). We also examined relationships between these parameters and a fineness index, which is a measure of streamlining and morphological optimization for steady swimming performance. All three environmental variables had some explanatory power, although morphological characteristics were predominantly associated with variation in mean annual run‐off. Phylogeny was also a strong predictor of morphological variation, whereas body size had little predictive power. Populations experiencing higher mean annual run‐off exhibited a shorter base of the dorsal fin, a more slender body and caudal peduncle, a smaller head in both horizontal and vertical dimensions, and a more anterior placement of the eye. With some exceptions, such as variation in jaw length, differences in body shape associated with phylogenetic history were similar to those associated with run‐off. Notably, all clades exhibited parallel responses to variation in run‐off. Populations experiencing high mean annual run‐off approached a hydrodynamic optimum, suggesting a morphology optimized for steady swimming performance. In contrast to previous studies that emphasize the importance of average water velocity, the findings of the present study indicate that morphological variation among populations of stream fishes is tightly linked to more complex aspects of hydrology and evolutionary history. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, ●● , ●●–●●.     

Evolutionary trends in Tetrastigma (Vitaceae): Morphological diversity and taxonomic implications

Tetrastigma (Miq.) Planch. (Vitaceae) is a genus with ca. 100 species showing great morphological diversity. Previous molecular phylogenetic studies suggested that traditional classification systems are not consistent with the molecular phylogeny, and Tetrastigma is undergoing further systematic investigation. We traced the evolutionary trends of 20 morphological characters within a robust phylogenetic framework. Our results revealed that many morphological characters show either multiple transitions or few state changes, however, some characters show distinct variation. The two subgenera in Tetrastigma (subgen. Tetrastigma and subgen. Palmicirrata) based on unbranched/bifurcate versus digitately branched tendrils are not supported because subgen. Tetrastigma is paraphyletic. However, the unbranched versus bifurcate/digitately branched tendril is of taxonomic utility to characterize some of the major clades. Inflorescences in Tetrastigma appear axillary, but are leaf‐opposed on a compressed axillary shoot. We found most of the species in Tetrastigma retained the ancestral compound dichasial inflorescence, except those of clade IV that have derived pseudo‐umbellate inflorescences. Other characters including habit, leaf organization, and berry shape provide additional morphological support for the major clades. Our morphological analysis and recent molecular study suggest each of the five major clades within Tetrastigma be treated as distinct taxonomic sections (five sections in the genus).