The convergent evolution of snake‐like forms by divergent evolutionary pathways in squamate reptiles*

Convergent evolution of phenotypes is considered evidence that evolution is deterministic. Establishing if such convergent phenotypes arose through convergent evolutionary pathways is a stronger test of determinism. We studied the evolution of snake‐like body shapes in six clades of lizards, each containing species ranging from short‐bodied and pentadactyl to long‐bodied and limbless. We tested whether body shapes that evolved in each clade were convergent, and whether clades evolved snake‐like body shapes following convergent evolutionary pathways. Our analyses showed that indeed species with the same numbers of digits in each clade evolved convergent body shapes. We then compared evolutionary pathways among clades by considering patterns of evolutionary integration and shape of relationship among body parts, patterns of vertebral evolution, and models of digit evolution. We found that all clades elongated their bodies through the addition, not elongation, of vertebrae, and had similar patterns of integration. However, patterns of integration, the body parts that were related by a linear or a threshold model, and patterns of digit evolution differed among clades. These results showed that clades followed different evolutionary pathways. This suggests an important role of historical contingency as opposed to determinism in the convergent evolution of snake‐like body shapes.     

Comparative limb bone scaling in turtles: Phylogenetic transitions with changes in functional demands?

Several terrestrial vertebrate clades include lineages that have evolved nearly exclusive use of aquatic habitats. In many cases, such transitions are associated with the evolution of flattened limbs that are used to swim via dorsoventral flapping. Such changes in shape may have been facilitated by changes in limb bone loading in novel aquatic environments. Studies on limb bone loading in turtles found that torsion is high relative to bending loads on land, but reduced compared to bending during aquatic rowing. Release from torsion among rowers could have facilitated the evolution of hydrodynamically advantageous flattened limbs among aquatic species. Because rowing is regarded as an intermediate locomotor stage between walking and flapping, rowing species might show limb bone flattening intermediate between the tubular shapes of walkers and the flattened shapes of flappers. We collected measurements of humeri and femora from specimens representing four functionally divergent turtle clades: sea turtles (marine flappers), softshells (specialized freshwater rowers), emydids (generalist semiaquatic rowers), and tortoises (terrestrial walkers). Patterns of limb bone scaling with size were compared across lineages using phylogenetic comparative methods. Although rowing taxa did not show the intermediate scaling patterns we predicted, our data provide other functional insights. For example, flattening of sea turtle humeri was associated with positive allometry (relative to body mass) for the limb bone diameter perpendicular to the flexion-extension plane of the elbow. Moreover, softshell limb bones exhibit positive allometry of femoral diameters relative to body mass, potentially helping them maintain their typical benthic position in water by providing additional weight to compensate for shell reduction. Tortoise limb bones showed positive allometry of diameters, as well as long humeri, relative to body mass, potentially reflecting specializations for resisting loads associated with digging. Overall, scaling patterns of many turtle lineages appear to correlate with distinctive behaviors or locomotor habits.     

Are there general laws for digit evolution in squamates? The loss and re‐evolution of digits in a clade of fossorial lizards (Brachymeles,Scincinae)

Evolutionary simplification of autopodial structures is a major theme in studies of body‐form evolution. Previous studies on amniotes have supported Morse's law, that is, that the first digit reduced is Digit I, followed by Digit V. Furthermore, the question of reversibility for evolutionary digit loss and its implications for “Dollo's law” remains controversial. Here, we provide an analysis of limb and digit evolution for the skink genus Brachymeles. Employing phylogenetic, morphological, osteological, and myological data, we (a) test the hypothesis that digits have re‐evolved, (b) describe patterns of morphological evolution, and (c) investigate whether patterns of digit loss are generalizable across taxa. We found strong statistical support for digit, but not limb re‐evolution. The feet of pentadactyl species of Brachymeles are very similar to those of outgroup species, while the hands of these lineages are modified (2‐3‐3‐3‐2) and a have a reduced set of intrinsic hand muscles. Digit number variation suggests a more labile Digit V than Digit I, contrary to Morse's law. The observed pattern of digit variation is different from that of other scincid lizards (Lerista, Hemiergis, Carlia). Our results present the first evidence of clade‐specific modes of digit reduction.     

CONVERGENT EVOLUTION OF SEXUAL DIMORPHISM IN SKULL SHAPE USING DISTINCT DEVELOPMENTAL STRATEGIES

Studies integrating evolutionary and developmental analyses of morphological variation are of growing interest to biologists as they promise to shed fresh light on the mechanisms of morphological diversification. Sexually dimorphic traits tend to be incredibly divergent across taxa. Such diversification must arise through evolutionary modifications to sex differences during development. Nevertheless, few studies of dimorphism have attempted to synthesize evolutionary and developmental perspectives. Using geometric morphometric analysis of head shape for 50 Anolis species, we show that two clades have converged on extreme levels of sexual dimorphism through similar, male‐specific changes in facial morphology. In both clades, males have evolved highly elongate faces whereas females retain faces of more moderate proportion. This convergence is accomplished using distinct developmental mechanisms; one clade evolved extreme dimorphism through the exaggeration of a widely shared, potentially ancestral, developmental strategy whereas the other clade evolved a novel developmental strategy not observed elsewhere in the genus. Together, our analyses indicate that both shared and derived features of development contribute to macroevolutionary patterns of morphological diversity among Anolis lizards.     

Body-form Evolution in the Scincid Lizard Clade <Emphasis Type="Italic">Lerista</Emphasis> and the Mode of Macroevolutionary Transitions

The scincid lizard clade Lerista provides an exceptional model for studying the mode of substantial evolutionary transformations, comprising more than 90 species displaying a remarkable variety of body forms. Patterns of character evolution in this clade, inferred from reconstructed ancestral states, are at least partly consistent with the correlated progression model of macroevolutionary change. At each stage in the transition to a highly elongate, limb-reduced body plan, alterations to the lengths of the forelimb and hind limb are accompanied by compensatory changes in snout-vent length (or vice versa), preserving locomotory ability. Nonetheless, there is evidence for moderate dissociation of hind limb evolution in some lineages, while tail length has evolved effectively independently of the substantial alterations to the lengths of the body and limbs. This indicates a significant role of evolutionary and developmental modularity in the divergence of body form within Lerista, and emphasises the potential variability of the strength of functional constraints within organisms and among lineages. Trends toward a highly elongate, functionally limbless body plan may be attributed primarily to a combination of the interdependence of changes in snout-vent length and limb lengths and the very low probability of re-elaborating structurally reduced limbs. Similar asymmetries in the probabilities of interrelated phenotypic changes may be a significant cause of evolutionary trends resulting in the emergence of higher taxa. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

LOCOMOTOR MODULES AND THE EVOLUTION OF AVIAN FLIGHT

The evolution of avian flight can be interpreted by analyzing the sequence of modifications of the primitive tetrapod locomotor system through time. Herein, we introduce the term “locomotor module” to identify anatomical subregions of the musculoskeletal system that are highly integrated and act as functional units during locomotion. The first tetrapods, which employed lateral undulations of the entire body and appendages, had one large locomotor module. Basal dinosaurs and theropods were bipedal and possessed a smaller locomotor module consisting of the hind limb and tail. Bird flight evolved as the superimposition of a second (aerial) locomotor capability onto the ancestral (terrestrial) theropod body plan. Although the origin of the wing module was the primary innovation, alterations in the terrestrial system were also significant. We propose that the primitive theropod locomotor module was functionally and anatomically subdivided into separate pelvic and caudal locomotor modules. This decoupling freed the tail to attain a new and intimate affiliation with the forelimb during flight, a configuration unique to birds. Thus, the evolution of flight can be viewed as the origin and novel association of locomotor modules. Differential elaboration of these modules in various lineages has produced the diverse locomotor abilities of modern birds.     

THE EVOLUTION OF BIPEDALISM IN JERBOAS (RODENTIA: DIPODOIDEA): ORIGIN IN HUMID AND FORESTED ENVIRONMENTS

Mammalian bipedalism has long been thought to have arisen in response to arid and open environments. Here, we tested whether bipedalism coevolved with environmental changes using molecular and paleontological data from the rodent superfamily Dipodoidea and statistical methods for reconstructing ancestral characteristics and past climates. Our results show that the post‐Late Miocene aridification exerted selective pressures on tooth shape, but not on leg length of bipedal jerboas. Cheek tooth crown height has increased since the Late Miocene, but the hind limb/head‐body length ratios remained stable and high despite the environmental change from humid and forested to arid and open conditions, rather than increasing from low to high as predicted by the arid‐bipedalism hypothesis. The decoupling of locomotor and dental character evolution indicates that bipedalism evolved under selective pressure different from that of dental hypsodonty in jerboas. We reconstructed the habitats of early jerboas using floral and faunal data, and the results show that the environments in which bipedalism evolved were forested. Our results suggest that bipedalism evolved as an adaptation to humid woodlands or forests for vertical jumping. Running at high speeds is likely a by‐product of selection for jumping, which became advantageous in open environments later on.     

MORPHOLOGICAL RATES OF ANGIOSPERM SEED SIZE EVOLUTION

The evolution of seed size among angiosperms reflects their ecological diversification in a complex fitness landscape of life‐history strategies. The lineages that have evolved seeds beyond the upper and lower boundaries that defined nonflowering seed plants since the Paleozoic are more dispersed across the angiosperm phylogeny than would be expected under a neutral model of phenotypic evolution. Morphological rates of seed size evolution estimated for 40 clades based on 17,375 species ranged from 0.001 (Garryales) to 0.207 (Malvales). Comparative phylogenetic analysis indicated that morphological rates are not associated with the clade's seed size but are negatively correlated with the clade's position in the overall distribution of angiosperm seed sizes; clades with seed sizes closer to the angiosperm mean had significantly higher morphological rates than clades with extremely small or extremely large seeds. Likewise, per‐clade taxonomic diversification rates are not associated with the seed size of the clade but with where the clade falls within the angiosperm seed size distribution. These results suggest that evolutionary rates (morphological and taxonomic) are elevated in densely occupied regions of the seed morphospace relative to lineages whose ecophenotypic innovations have moved them toward the edges.     

CONVERGENT AND CORRELATED EVOLUTION OF MAJOR LIFE‐HISTORY TRAITS IN THE ANGIOSPERM GENUS LEUCADENDRON (PROTEACEAE)

Natural selection is expected to cause convergence of life histories among taxa as well as correlated evolution of different life‐history traits. Here, we quantify the extent of convergence of five key life‐history traits (adult fire survival, seed storage, degree of sexual dimorphism, pollination mode, and seed‐dispersal mode) and test hypotheses about their correlated evolution in the genus Leucadendron (Proteaceae) from the fire‐prone South African fynbos. We reconstructed a new molecular phylogeny of this highly diverse genus that involves more taxa and molecular markers than previously. This reconstruction identifies new clades that were not detected by previous molecular study and morphological classifications. Using this new phylogeny and robust methods that account for phylogenetic uncertainty, we show that the five life‐history traits studied were labile during the evolutionary history of the genus. This diversity allowed us to tackle major questions about the correlated evolution of life‐history strategies. We found that species with longer seed‐dispersal distances tended to evolve lower pollen‐dispersal distance, that insect‐pollinated species evolved decreased sexual dimorphism, and that species with a persistent soil seed‐bank evolved toward reduced fire‐survival ability of adults.     

Understanding hind limb weight support in chimpanzees with implications for the evolution of primate locomotion

Most quadrupedal mammals support a larger amount of body weight on their forelimbs compared with their hind limbs during locomotion, whereas most primates support more of their body weight on their hind limbs. Increased hind limb weight support is generally interpreted as an adaptation that reduces stress on primates' highly mobile forelimb joints. Thus, increased hind limb weight support was likely vital for the evolution of primate arboreality. Despite its evolutionary importance, the mechanism used by primates to achieve this important kinetic pattern remains unclear. Here, we examine weight support patterns in a sample of chimpanzees (Pan troglodytes) to test the hypothesis that limb position, combined with whole body center of mass position (COM), explains increased hind limb weight support in this taxon. Chimpanzees have a COM midway between their shoulders and hips and walk with a relatively protracted hind limb and a relatively vertical forelimb, averaged over a step. Thus, the limb kinematics of chimpanzees brings their feet closer to the COM than their hands, generating greater hind limb weight support. Comparative data suggest that these same factors likely explain weight support patterns for a broader sample of primates. It remains unclear whether primates use these limb kinematics to increase hind limb weight support, or whether they are byproducts of other gait characteristics. The latter hypothesis raises the intriguing possibility that primate weight support patterns actually evolved as byproducts of other traits, or spandrels, rather than as adaptations to increase forelimb mobility. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Influence of body mass on the shape of forelimb in musteloid carnivorans

In the majority of mammals, the limbs are positioned under the body and play an important role in gravitational support, allowing the transfer of the load and providing stability to the animal. For this reason, an animal's body mass likely has a significant effect on the shape of its limb bones. In the present study, we investigate the influence of body mass variation on the shape of the three long bones of the forelimb in a group of closely‐related species of mammals: the musteloid carnivorans. We use geometric morphometric techniques to quantify forelimb shape; then estimate phylogenetic signal in the shape of each long bone; and, finally, we apply an independent contrasts approach to assess evolutionary associations between forelimb shape and body mass. The results obtained show that body mass evolution is tightly coordinated with the evolution of forelimb shape, although not equally in all elements. In particular, the humeral and radial shapes of heavier species appear better suited for load bearing and load transmission than the ulna. Nevertheless, our results also show that body mass influences only part of forelimb long bone shape and that other factors, such as locomotor ecology, must be considered to fully understand forelimb evolution. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 91–103.     

Adaptive processes drive ecomorphological convergent evolution in antwrens (Thamnophilidae)

Phylogenetic niche conservatism (PNC) and convergence are contrasting evolutionary patterns that describe phenotypic similarity across independent lineages. Assessing whether and how adaptive processes give origin to these patterns represent a fundamental step toward understanding phenotypic evolution. Phylogenetic model‐based approaches offer the opportunity not only to distinguish between PNC and convergence, but also to determine the extent that adaptive processes explain phenotypic similarity. The Myrmotherula complex in the Neotropical family Thamnophilidae is a polyphyletic group of sexually dimorphic small insectivorous forest birds that are relatively homogeneous in size and shape. Here, we integrate a comprehensive species‐level molecular phylogeny of the Myrmotherula complex with morphometric and ecological data within a comparative framework to test whether phenotypic similarity is described by a pattern of PNC or convergence, and to identify evolutionary mechanisms underlying body size and shape evolution. We show that antwrens in the Myrmotherula complex represent distantly related clades that exhibit adaptive convergent evolution in body size and divergent evolution in body shape. Phenotypic similarity in the group is primarily driven by their tendency to converge toward smaller body sizes. Differences in body size and shape across lineages are associated to ecological and behavioral factors.     

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.     

SEX‐SPECIFIC PATTERNS OF MORPHOLOGICAL DIVERSIFICATION: EVOLUTION OF REACTION NORMS AND STATIC ALLOMETRIES IN NERIID FLIES

The consequences of sex‐specific selection for patterns of diversification remain poorly known. Because male secondary sexual traits are typically costly to express, and both costs and benefits are likely to depend on ambient environment and individual condition, such traits may be expected to diversify via changes in reaction norms as well as the scaling of trait size with body size (static allometry). We investigated morphological diversification within two species of Australian neriid flies (Telostylinus angusticollis, Telostylinus lineolatus) by rearing larvae from several populations on larval diets varying sixfold in nutrient concentration. Mean body size varied among populations of T. angusticollis, but body size reaction norms did not vary within either species. However, we detected diversification of reaction norms for body shape in males and females within both species. Moreover, unlike females, males also diversified in static allometry slope and reaction norms for static allometry slope of sexual and nonsexual traits. Our findings reveal qualitative sex differences in patterns of morphological diversification, whereby shape–size relationships diversify extensively in males, but remain conserved in females despite extensive evolution of trait means. Our results highlight the importance of incorporating plasticity and allometry in studies of adaptation and diversification.     

Optimal shape and motion of undulatory swimming organisms

Undulatory swimming animals exhibit diverse ranges of body shapes and motion patterns and are often considered as having superior locomotory performance. The extent to which morphological traits of swimming animals have evolved owing to primarily locomotion considerations is, however, not clear. To shed some light on that question, we present here the optimal shape and motion of undulatory swimming organisms obtained by optimizing locomotive performance measures within the framework of a combined hydrodynamical, structural and novel muscular model. We develop a muscular model for periodic muscle contraction which provides relevant kinematic and energetic quantities required to describe swimming. Using an evolutionary algorithm, we performed a multi-objective optimization for achieving maximum sustained swimming speed U and minimum cost of transport (COT)--two conflicting locomotive performance measures that have been conjectured as likely to increase fitness for survival. Starting from an initial population of random characteristics, our results show that, for a range of size scales, fish-like body shapes and motion indeed emerge when U and COT are optimized. Inherent boundary-layer-dependent allometric scaling between body mass and kinematic and energetic quantities of the optimal populations is observed. The trade-off between U and COT affects the geometry, kinematics and energetics of swimming organisms. Our results are corroborated by empirical data from swimming animals over nine orders of magnitude in size, supporting the notion that optimizing U and COT could be the driving force of evolution in many species.     

Correlated evolution of body and fin morphology in the cichlid fishes

Body and fin shapes are chief determinants of swimming performance in fishes. Different configurations of body and fin shapes can suit different locomotor specializations. The success of any configuration is dependent upon the hydrodynamic interactions between body and fins. Despite the importance of body–fin interactions for swimming, there are few data indicating whether body and fin configurations evolve in concert, or whether these structures vary independently. The cichlid fishes are a diverse family whose well‐studied phylogenetic relationships make them ideal for the study of macroevolution of ecomorphology. This study measured body, and caudal and median fin morphology from radiographs of 131 cichlid genera, using morphometrics and phylogenetic comparative methods to determine whether these traits exhibit correlated evolution. Partial least squares canonical analysis revealed that body, caudal fin, dorsal fin, and anal fin shapes all exhibited strong correlated evolution consistent with locomotor ecomorphology. Major patterns included the evolution of deep body profiles with long fins, suggestive of maneuvering specialization; and the evolution of narrow, elongate caudal peduncles with concave tails, a combination that characterizes economical cruisers. These results demonstrate that body shape evolution does not occur independently of other traits, but among a suite of other morphological changes that augment locomotor specialization.     

EVOLUTION OF SCAPULA SIZE AND SHAPE IN DIDELPHID MARSUPIALS (DIDELPHIMORPHIA: DIDELPHIDAE)

The New World family Didelphidae, the basal lineage within marsupials, is commonly viewed as morphologically conservative, yet includes aquatic, terrestrial, scansorial, and arboreal species. Here, I quantitatively estimated the existing variability in size and shape of the Didelphidae scapula (1076 specimens from 56 species) using geometric morphometrics, and compared size and shape differences to evolutionary and ecologic distances. I found considerable variation in the scapula morphology, most of it related to size differences between species. This results in morphologic divergence between different locomotor habits in larger species (resulting from increased mechanical loads), but most smaller species present similarly shaped scapulae. The only exceptions are the water opossum and the short-tailed opossums, and the functional explanations for these differences remain unclear. Scapula size and shape were mapped onto a molecular phylogeny for 32 selected taxa and ancestral size and shapes were reconstructed using squared-changed parsimony. Results indicate that the Didelphidae evolved from a medium- to small-sized ancestor with a generalized scapula, slightly more similar to arboreal ones, but strikingly different from big-bodied present arboreal species, suggesting that the ancestral Didelphidae was a small scansorial animal with no particular adaptations for arboreal or terrestrial habits, and these specializations evolved only in larger-bodied clades.     

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.     

ASYNCHRONOUS EVOLUTION OF PHYSIOLOGY AND MORPHOLOGY IN ANOLIS LIZARDS

Species‐rich adaptive radiations typically diversify along several distinct ecological axes, each characterized by morphological, physiological, and behavioral adaptations. We test here whether different types of adaptive traits share similar patterns of evolution within a radiation by investigating patterns of evolution of morphological traits associated with microhabitat specialization and of physiological traits associated with thermal biology in Anolis lizards. Previous studies of anoles suggest that close relatives share the same “structural niche” (i.e., use the same types of perches) and are similar in body size and shape, but live in different “climatic niches” (i.e., use habitats with different insolation and temperature profiles). Because morphology is closely tied to structural niche and field active body temperatures are tied to climatic niches in Anolis, we expected phylogenetic analyses to show that morphology is more evolutionarily conservative than thermal physiology. In support of this hypothesis, we find (1) that thermal biology exhibits more divergence among recently diverged Anolis taxa than does morphology; and (2) diversification of thermal biology among all species often follows diversification in morphology. These conclusions are remarkably consistent with predictions made by anole biologists in the 1960s and 1970s.