Synchronized swimming: coordination of pelvic and pectoral fins during augmented punting by the freshwater stingray Potamotrygon orbignyi

Benthic animals live at the juncture of fluid and solid environments, an interface that shapes many aspects of their behavior, including their means of locomotion. Aquatic walking and similar substrate-dependent forms of underwater propulsion have evolved multiple times in benthic invertebrate and vertebrate taxa, including batoid elasmobranchs. Skates (Rajidae) use the pelvic fins to punt across the substrate, keeping the pectoral fin disc still. Other batoids combine pelvic fin motions with pectoral fin undulation in augmented punting, but the coordination of these two modes has not been described. In this study of an augmented punter, the freshwater stingray Potamotrygon orbignyi, we demonstrate the synchrony of pelvic and pectoral fin cycles. The punt begins as the pelvic fins, held in an anterior position, are planted into the substrate and used to push the body forward. Meanwhile, a wave of pectoral fin undulation begins, increasing to maximum height just before the cycle's halfway point, when the pelvic fins reach their furthest posterior extension. The pectoral fin wave subsides as the pelvic fins return to their starting position for subsequent punts. Despite definitive links between pectoral and pelvic fin activity, we find no significant relationship between pectoral fin kinematics (frequency, wave height, and wave speed) and punt performance. However, slip calculations indicate that pectoral undulation can produce thrust and augment punting. Pelvic fin kinematics (frequency and duty factor) have significant effects, suggesting that while both sets of fins contribute to thrust generation, the pelvic fins likely determine punt performance.     

Fossil fishes from china provide first evidence of dermal pelvic girdles in osteichthyans

Background

The pectoral and pelvic girdles support paired fins and limbs, and have transformed significantly in the diversification of gnathostomes or jawed vertebrates (including osteichthyans, chondrichthyans, acanthodians and placoderms). For instance, changes in the pectoral and pelvic girdles accompanied the transition of fins to limbs as some osteichthyans (a clade that contains the vast majority of vertebrates – bony fishes and tetrapods) ventured from aquatic to terrestrial environments. The fossil record shows that the pectoral girdles of early osteichthyans (e.g., Lophosteus, Andreolepis, Psarolepis and Guiyu) retained part of the primitive gnathostome pectoral girdle condition with spines and/or other dermal components. However, very little is known about the condition of the pelvic girdle in the earliest osteichthyans. Living osteichthyans, like chondrichthyans (cartilaginous fishes), have exclusively endoskeletal pelvic girdles, while dermal pelvic girdle components (plates and/or spines) have so far been found only in some extinct placoderms and acanthodians. Consequently, whether the pectoral and pelvic girdles are primitively similar in osteichthyans cannot be adequately evaluated, and phylogeny-based inferences regarding the primitive pelvic girdle condition in osteichthyans cannot be tested against available fossil evidence.

Methodology/Principal Findings

Here we report the first discovery of spine-bearing dermal pelvic girdles in early osteichthyans, based on a new articulated specimen of Guiyu oneiros from the Late Ludlow (Silurian) Kuanti Formation, Yunnan, as well as a re-examination of the previously described holotype. We also describe disarticulated pelvic girdles of Psarolepis romeri from the Lochkovian (Early Devonian) Xitun Formation, Yunnan, which resemble the previously reported pectoral girdles in having integrated dermal and endoskeletal components with polybasal fin articulation.

Conclusions/Significance

The new findings reveal hitherto unknown similarity in pectoral and pelvic girdles among early osteichthyans, and provide critical information for studying the evolution of pelvic girdles in osteichthyans and other gnathostomes.     

Comparative morphology and osteology of pelvic fin‐derived midline suckers in lumpfishes,snailfishes and gobies

Some fishes use modified body structures – including pelvic fins – to produce suction to facilitate stability in turbulent environments. This study compares the morphology and osteology of the pelvic suckers of representative lumpfishes (Cyclopteridae), snailfishes (Liparidae) and gobies (Gobiidae). In all species studied the midline sucker (pelvic suctorial organ [PSO]) is formed from the pelvic girdle and fin rays I and 5 of the pelvic fins, comprised of similar osteological elements to those found in the pelvic girdle and pelvic fin rays although the morphology of the bony elements is species‐specific. Pelvic suctorial organs in those fishes that lack pelvic girdles are therefore homologous to pelvic girdles. The phenotypic diversity seen in so few species indicates that many sucker morphologies have arisen, origination depending on the concerted development of muscular, skeletal, nervous, and skin body tissues. The structure of the soft rays of the pelvic fins in the liparids and cyclopterids is unusual and indicative of unconventional developmental patterning of fin ray halves and of evolution in the underlying mechanisms responsible for the development of midline suckers.     

Paired fin skeletons and relationships of the fossil group Porolepiformes (Osteichthyes: Sardcopterygii)

The endoskeletal girdles, anocleithrum and paired fin supports of the porolepiform fish Glyptolepis (Osteichthyes: Sarcopterygii: Porolepiformes) are figured and described. The pectoral fin skeleton is known from the proximal part only and the pelvic fin skeleton is fragmentary, but the scapulocoracoid, anocleithrum and pelvic girdle can be reconstructed in their entirety. The anocleithrum is entirely subdermal. The pectoral fin skeleton in shown to be biserial, with a large number of axial mesomeres, whereas the pelvic fin contains fewer mesomeres and is strongly asymmetrical with very few postaxial radials. The scapulocoracoid is essentially similar to a reconstruction figured by Jarvik (1980), but has a more elongate glenoid; this has functional implications. The pelvic girdle consists of two separate halves as in Eusthenopteron, but differs from that genus in lacking dorsolateral rami. A brief survey of the evidence of paired fin structure in other porolepiform genera is carried out to establish whether the structures seen in Glyptolepis are likely to be representative for the Porolepiformes. A study of the morphology and muscle attachments of the paired fin skeletons indicates that the pattern of fin movement was significantly different from that in Neoceratodus. The fin supports and girdles of Glyptolepis are compared with those of other sarcopterygian groups as well as with actinopterygians, placoderms and sharks, in order to establish evolutionary polarities. Glyptolepis is shown to display a number of derived characters. The information gained from the comparison is used to construct a maximum parsimony cladogram, which places coelacanths as the sister group of porolepiforms + lungfishes, with the rhizodonts + tetrapods and osteolepiforms as successive sister groups of this clade. Characters of uncertain polarity are considered in the light of this cladogram. A comparison with recently published cladograms shows that none are completely compatible with the results from this study.     

Pectoral fin morphology of batoid fishes (Chondrichthyes: Batoidea): Explaining phylogenetic variation with geometric morphometrics

The diverse cartilaginous fish lineage, Batoidea (rays, skates, and allies), sister taxon to sharks, comprises a huge range of morphological diversity which to date remains unquantified and unexplained in terms of evolution or locomotor style. A recent molecular phylogeny has enabled us to confidently assess broadscale aspects of morphology across Batoidea. Geometric morphometrics quantifies the major aspects of shape variation, focusing on the enlarged pectoral fins which characterize batoids, to explore relationships between ancestry, locomotion and habitat. A database of 253 specimens, encompassing 60 of the 72 batoid genera, reveals that the majority of morphological variation across Batoidea is attributable to fin aspect‐ratio and the chordwise location of fin apexes. Both aspect‐ratio and apex location exhibit significant phylogenetic signal. Standardized independent linear contrast analysis reveals that fin aspect‐ratio can predict locomotor style. This study provides the first evidence that low aspect‐ratio fins are correlated with undulatory‐style locomotion in batoids, whereas high aspect‐ratio fins are correlated with oscillatory locomotion. We also show that it is phylogeny that determines locomotor style. In addition, body‐ and caudal fin‐locomotors are shown to exhibit low aspect‐ratio fins, whereas a pelagic lifestyle correlates with high aspect‐ratio fins. These results emphasize the importance of phylogeny in determining batoid pectoral fin shape, however, interactions with other constraints, most notably locomotor style, are also highlighted as significant. J. Morphol. 275:1173–1186, 2014. © 2014 Wiley Periodicals, Inc.     

Comparative punting kinematics and pelvic fin musculature of benthic batoids

Although the majority of batoid elasmobranchs, skates and rays, are benthically associated, benthic locomotion has been largely overlooked in this group. Only skates have been previously described to perform a form of benthic locomotion termed “punting.” While keeping the rest of the body motionless, the skate's pelvic fins are planted into the substrate and then retracted caudally, which thrusts the body forward. In this study, we demonstrate that this form of locomotion is not confined to the skates, but is found across a range of phylogenetically and morphologically diverse batoid species. However, only the clearnose skate, Raja eglanteria, and the lesser electric ray, Narcine brasiliensis, performed “true punting,” in which only the pelvic fins were engaged. The yellow stingray, Urobatis jamaicensis, and the Atlantic stingray, Dasyatis sabina, performed “augmented punting,” in which pectoral fin movement was also used to generate thrust. Despite this supplemental use of pectoral fins, the augmented punters failed to exceed the punting capabilities of the true punters. The urobatid and the true punters all punted approximately half their disc length per punt, whereas the dasyatid punted a significantly shorter distance. The skate punted significantly faster than the other species. Examination of the pelvic fin musculature revealed more specialized muscles in the true punters than in the augmented punters. This concordance of musculature with punting ability provides predictive power regarding the punting kinematics of other elasmobranchs based upon gross muscular examinations. In contrast to previous assumptions, our results suggest that benthic locomotion is widespread among batoids. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Re‐evaluation of batoid pectoral morphology reveals novel patterns of diversity among major lineages

Batoids (Chondrichthyes: Batoidea) are a diverse group of cartilaginous fishes which comprise a monophyletic sister lineage to all neoselachians or modern sharks. All species in this group possess anteroposteriorly expanded‐pectoral fins, giving them a unique disc‐like body form. Reliance on pectoral fins for propulsion ranges from minimal (sawfish) to almost complete dependence (skates and rays). A recent study on the diversity of planform pectoral fin shape in batoids compared overall patterns of morphological variation within the group. However, inconsistent pectoral homology prevented the study from accurately representing relationships within and among major batoid taxa. With previous work in mind, we undertook an independent investigation of pectoral form in batoids and evaluated the implications of shape diversity on locomotion and lifestyle, particularly in the skates (Rajoidei) and rays (Myliobatoidei). We used geometric morphometrics with sliding semilandmarks to analyze pectoral fin outlines and also calculate fin aspect ratios (AR), a functional trait linked to locomotion. In agreement with previous work, our results indicated that much of the evolution of batoid pectoral shape has occurred along a morphological axis that is closely related to AR. For species where kinematic data were available, both shape and AR were associated with swimming mode. This work further revealed novel patterns of shape variation among batoids, including strong bimodality of shape in rays, an intermediate location of skate species in the morphospace between benthic/demersal and pelagic rays, and approximately parallel shape trajectories in the benthic/demersal rays and skates. Finally, manipulation of landmarks verified the need for a consistent and accurate definition of homology for the outcome and efficacy of analyses of pectoral form and function in batoids. J. Morphol. 277:482–493, 2016. © 2016 Wiley Periodicals, Inc.     

Skeletal and muscular pelvic morphology of hillstream loaches (Cypriniformes: Balitoridae)

The rheophilic hillstream loaches (Balitoridae) of South and Southeast Asia possess a range of pelvic girdle morphologies, which may be attributed to adaptations for locomotion against rapidly flowing water. Specifically, the connectivity of the pelvic plate (basipterygium) to the vertebral column via a sacral rib, and the relative size and shape of the sacral rib, fall within a spectrum of three discrete morphotypes: long, narrow rib that meets the basipterygium; thicker, slightly curved rib meeting the basipterygium; and robust crested rib interlocking with the basipterygium. Species in this third category with more robust sacral rib connections between the basipterygium and vertebral column are capable of walking out of water with a tetrapod-like lateral-sequence, diagonal-couplet gait. This behavior has not been observed in species lacking direct skeletal connection between the vertebrae and the pelvis. The phylogenetic positions of the morphotypes were visualized by matching the morphological features onto a novel hypothesis of relationships for the family Balitoridae. The morphotypes determined through skeletal morphology were correlated with patterns observed in the pelvic muscle morphology of these fishes. Transitions towards increasingly robust pelvic girdle attachment were coincident with a more anterior origin on the basipterygium and more lateral insertion of the muscles on the fin rays, along with a reduction of the superficial abductors and adductors with more posterior insertions. These modifications are expected to provide a mechanical advantage for generating force against the ground. Inclusion of the enigmatic cave-adapted balitorid Cryptotora thamicola into the most data-rich balitorid phylogeny reveals its closest relatives, providing insight into the origin of the skeletal connection between the axial skeleton and basipterygium.     

The structure and function of the dermal pectoral girdle in bony fishes with particular reference to ostariophysines

The structure of the dermal pectoral girdle of teleostean fishes is analyzed in relation to its functions. In bony fishes the vertebral column, with a horizontal axis, and the pectoral girdle, with a basically vertical axis, form the only skeletal links between the head and the body. The individual bones of the dermal girdle are considered as supporting units joined by a series of articulations that permit differential movement between adjacent bones. The movements mediated by this linkage system are: lateral swinging of the head relative to the body, expansion of the distance between the central areas of the two pectoral girdles to permit passage of large food items, and fore-and-aft movements of the anteroventral ends of the cleithra relative to the skull. Among other factors affecting the structure of the dermal pectoral girdle are the provision for the support of the pectoral fin base and the requirement for the effective operation of a sleeve valve between the girdle and the opercular cover.
Modifications of the dermal pectoral girdle in ostariophysine fishes are discussed. A brief history of the bony fish girdle in terms of its functional components is postulated.     

Comparative anatomy and development of pectoral and pelvic girdles in hylid anurans

The development of the tetrapod pectoral and pelvic girdles is intimately linked to the proximal segments of the fore‐ and hindlimbs. Most studies on girdles are osteological and provide little information about soft elements such as muscles and tendons. Moreover, there are few comparative developmental studies. Comparative data gleaned from cleared‐and‐stained whole mounts and serial histological sections of 10 species of hylid frogs are presented here. Adult skeletal morphology, along with bones, muscles, and connective tissue of both girdles and their association with the proximal portions of the anuran fore‐ and hindlimbs are described. The data suggest that any similarity could be attributable to the constraints of their ball‐and‐socket joints, including incorporation of the girdle and stylopodium into a single developmental module. An ancestral state reconstruction of key structures and developmental episodes reveals that several development events occur at similar stages in different species, thereby preventing heterochronic changes. The medial contact of the halves of the pectoral girdle coincides with the emergence of the forelimbs from the branchial chamber and with the total differentiation of the linkage between the axial skeleton and the girdles. The data suggest that morphogenic activity in the anterior dorsal body region is greater than in the posterior one, reflecting the evolutionary sequence of the development of the two girdles in ancient tetrapods. The data also document the profound differences in the anatomy and development of the pectoral and pelvic girdles, supporting the proposal that the pectoral and pelvic girdles are not serially homologous, as was long presumed.     

Moving in two worlds: aquatic and terrestrial locomotion in sea snakes (Laticauda colubrina,Laticaudidae)

Yellow‐lipped sea kraits (Laticauda colubrina) are amphibious in their habits. We measured their locomotor speeds in water and on land to investigate two topics: (1) to what degree have adaptations to increase swimming speed (paddle‐like tail etc.) reduced terrestrial locomotor ability in sea kraits?; and (2) do a sea krait’s sex and body size influence its locomotor ability in these two habitats, as might be expected from the fact that different age and sex classes of sea kraits use the marine and terrestrial environments in different ways? To estimate ancestral states for locomotor performance, we measured speeds of three species of Australian terrestrial elapids that spend part of their time foraging in water. The evolutionary modifications of Laticauda for marine life have enhanced their swimming speeds by about 60%, but decreased their terrestrial locomotor speed by about 80%. Larger snakes moved faster than smaller individuals in absolute terms but were slower in terms of body lengths travelled per second, especially on land. Male sea kraits were faster than females (independent of the body‐size effect), especially on land. Prey items in the gut reduced locomotor speeds both on land and in water. Proteroglyphous snakes may offer exceptional opportunities to study phylogenetic shifts in locomotor ability, because (1) they display multiple independent evolutionary shifts from terrestrial to aquatic habits, and (2) one proteroglyph lineage (the laticaudids) displays considerable intraspecific and interspecific diversity in terms of the degree to which they use terrestrial vs. aquatic habitats.     

Development and evolution of the muscles of the pelvic fin

Locomotor strategies in terrestrial tetrapods have evolved from the utilisation of sinusoidal contractions of axial musculature, evident in ancestral fish species, to the reliance on powerful and complex limb muscles to provide propulsive force. Within tetrapods, a hindlimb-dominant locomotor strategy predominates, and its evolution is considered critical for the evident success of the tetrapod transition onto land. Here, we determine the developmental mechanisms of pelvic fin muscle formation in living fish species at critical points within the vertebrate phylogeny and reveal a stepwise modification from a primitive to a more derived mode of pelvic fin muscle formation. A distinct process generates pelvic fin muscle in bony fishes that incorporates both primitive and derived characteristics of vertebrate appendicular muscle formation. We propose that the adoption of the fully derived mode of hindlimb muscle formation from this bimodal character state is an evolutionary innovation that was critical to the success of the tetrapod transition.     

Genetic analysis of punt,a type II Dpp receptor that functions throughout the Drosophila melanogaster life cycle.

TGF-beta (transforming growth factor-beta-) mediated signal transduction affects growth and patterning in a variety of organisms. Here we report a genetic characterization of the Drosophila punt gene that encodes a type II serine/threonine kinase TGF-beta/Dpp (Decapentaplegic) receptor. Although the punt gene was originally identified based on its requirement for embryonic dorsal closure, we have documented multiple periods of punt activity throughout the Drosophila life cycle. We demonstrate that potentially related embryonic punt phenotypes, defects in dorsoventral patterning and dorsal closure, correspond to distinct maternal and zygotic requirements for punt. In addition, we document postembryonic requirements for punt activity. The tight correspondence between both embryonic and postembryonic loss-of-function punt and dpp phenotypes implicates a role for Punt in mediating virtually all Dpp signaling events in Drosophila. Finally, our comparison of punt homoallelic and heteroallelic phenotypes provides direct evidence for interallelic complementation. Taken together, these results suggest that the Punt protein functions as a dimer or higher order multimer throughout the Drosophila life cycle.     

The evolution of jumping in frogs: Morphological evidence for the basal anuran locomotor condition and the radiation of locomotor systems in crown group anurans

Our understanding of the evolution of frog locomotion follows from the work of Emerson in which anurans are proposed to possess one of three different iliosacral configurations: 1) a lateral‐bending system found in walking and hopping frogs; 2) a fore‐aft sliding mechanism found in several locomotor modes; and 3) a sagittal‐hinge‐type pelvis posited to be related to long‐distance jumping performance. The most basal living (Ascaphus) and fossil (Prosalirus) frogs are described as sagittal‐hinge pelvic types, and it has been proposed that long‐distance jumping with a sagittal‐hinge pelvis arose early in frog evolution. We revisited osteological traits of the pelvic region to conduct a phylogenetic analysis of the relationships between pelvic systems and locomotor modes in frogs. Using two of Emerson's diagnostic traits from the sacrum and ilium and two new traits from the urostyle, we resampled the taxa originally studied by Emerson and key paleotaxa and conducted an analysis of ancestral‐character state evolution in relation to locomotor mode. We present a new pattern for the evolution of pelvic systems and locomotor modes in frogs. Character analysis shows that the lateral‐bender, walker/hopper condition is both basal and generally conserved across the Anura. Long‐distance jumping frogs do not appear until well within the Neobatrachia. The sagittal‐hinge morphology is correlated with long‐distance jumping in terrestrial frogs; however, it evolved convergently multiple times in crown group anurans with the same four pelvic traits described herein. Arboreal jumping has appeared in multiple crown lineages as well, but with divergent patterns of evolution involving each of the three pelvic types. The fore‐aft slider morph appears independently in three different locomotor modes and, thus, is a more complex system than previously thought. Finally, it appears that the advent of a bicondylar sacro‐urostylic articulation was originally related to providing axial rigidity to lateral‐bending behaviors rather than sagittal bending. J. Morphol., 2011. © 2010 Wiley‐Liss, Inc.     

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.     

On the serial homology of the pectoral and pelvic girdles of tetrapods

While fore‐ and hindlimbs are commonly assumed to be serially homologous, the serial homology of the pectoral and pelvic girdles is more ambiguous. We investigate the degree to which a common history, developmental program, and gene network are shared between the girdles relative to the rest of the appendicular skeleton. Paleontological data indicate that pectoral appendages arose millions of years before pelvic appendages. Recent embryological and genetic data suggest that the anatomical similarity between the fore‐ and hindlimbs arose through the sequential, derived deployment of similar developmental programs and gene networks, and is therefore not due to ancestral serial homology. Much less developmental work has however been published about the girdles. Here, we provide the first detailed review of the developmental programs and gene networks of the pectoral and pelvic girdles. Our review shows that, with respect to these programs and networks, there are fewer similarities between pelvic and pectoral girdles than there are between the limbs. The available data therefore support recent hypotheses that the anatomical similarities between the fore‐ and hindlimbs arose during the fin‐to‐limb transition through the derived co‐option of similar developmental mechanisms, while the phylogenetically older pectoral and pelvic girdles have remained more distinct since their evolutionary origin.     

Walking in skates (Chondrichthyes, Rajidae): anatomy, behaviour and analogies to tetrapod locomotion

Pelvic fin walking in skates is common. However, the structure and function of pelvic fins have not been analysed. Pelvic fins of skates of the genus Psammobatis and Rioraja agassizi are externally divided into an anterior leg-like lobe and a posterior fin-like lobe. Internally, the anterior lobes are supported by a compound radial, a proximal radial and distal radials that resemble a thigh, a calf and a foot, respectively, and three associated radials arising from the pelvic girdle. A highly developed radial condyle on the pelvic girdle enables broad 'limb' movements. The muscular arrangement of the anterior lobes is formed by protractor, retractor, flexor and extensor muscles, clearly departing from the generalized fin muscle arrangement of elasmobranchs. Walking is composed of propulsion and recovery phases. A backward movement of the compound radial in the horizontal plane characterizes the propulsive phase. The proximal radial connects vertically the compoundradial with the foot-like distal radials, which are anchored on the bottom. During the recovery phase, the foot-like structure is lifted off the bottom and the entire limb-like anterior lobe is moved forwards for starting a new cycle. Walking in skates resembles the ancestral tetrapod sprawling locomotion seen in many salamanders and lizards. Pelvic fin anatomy and walking behaviour in skates and hemiscylliid sharksare compared. Ecological and evolutionary implications of walking locomotion in skates are also discussed.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 35–41.     

The effect of parity on morphological evolution among phrynosomatid lizards

The shift from egg laying to live‐bearing is one of the most well‐studied transitions in evolutionary biology. Few studies, however, have assessed the effect of this transition on morphological evolution. Here, we evaluated the effect of reproductive mode on the morphological evolution of 10 traits, among 108 species of phrynosomatid lizards. We assess whether the requirement for passing shelled eggs through the pelvic girdle has led to morphological constraints in oviparous species and whether long gestation times in viviparous species have led to constraints in locomotor morphology. We fit models to the data that vary both in their tempo (strength and rate of selection) and mode of evolution (Brownian or Ornstein‐Uhlenbeck) and estimates of trait optima. We found that most traits are best fit by a generalized multipeak OU model, suggesting differing trait optima for viviparous vs. oviparous species. Additionally, rates (σ²) of both pelvic girdle and forelimb trait evolution varied with parity; viviparous species had higher rates. Hindlimb traits, however, exhibited no difference in σ² between parity modes. In a functional context, our results suggest that the passage of shelled eggs constrains the morphology of the pelvic girdle, but we found no evidence of morphological constraint of the locomotor apparatus in viviparous species. Our results are consistent with recent lineage diversification analyses, leading to the conclusion that transitions to viviparity increase both lineage and morphological diversification.