Recombination rate and protein evolution in yeast

Background

Tetrapods exhibit great diversity in limb structures among species and also between forelimbs and hindlimbs within species, diversity which frequently correlates with locomotor modes and life history. We aim to examine the potential relation of changes in developmental timing (heterochrony) to the origin of limb morphological diversity in an explicit comparative and quantitative framework. In particular, we studied the relative time sequence of development of the forelimbs versus the hindlimbs in 138 embryos of 14 tetrapod species spanning a diverse taxonomic, ecomorphological and life-history breadth. Whole-mounts and histological sections were used to code the appearance of 10 developmental events comprising landmarks of development from the early bud stage to late chondrogenesis in the forelimb and the corresponding serial homologues in the hindlimb.

Results

An overall pattern of change across tetrapods can be discerned and appears to be relatively clade-specific. In the primitive condition, as seen in Chondrichthyes and Osteichthyes, the forelimb/pectoral fin develops earlier than the hindlimb/pelvic fin. This pattern is either retained or re-evolved in eulipotyphlan insectivores (= shrews, moles, hedgehogs, and solenodons) and taken to its extreme in marsupials. Although exceptions are known, the two anurans we examined reversed the pattern and displayed a significant advance in hindlimb development. All other species examined, including a bat with its greatly enlarged forelimbs modified as wings in the adult, showed near synchrony in the development of the fore and hindlimbs.

Conclusion

Major heterochronic changes in early limb development and chondrogenesis were absent within major clades except Lissamphibia, and their presence across vertebrate phylogeny are not easily correlated with adaptive phenomena related to morphological differences in the adult fore- and hindlimbs. The apparently conservative nature of this trait means that changes in chondrogenetic patterns may serve as useful phylogenetic characters at higher taxonomic levels in tetrapods. Our results highlight the more important role generally played by allometric heterochrony in this instance to shape adult morphology.     

On homology

The currently most widely used definitions of homology, which concentrate exclusively on what I call phylogenetic homology, involve comparisons between taxa. Although they share important conceptual relationships with phylogenetic homology and their role in evolutionary biology is significant, serial and other forms of iterative homology have been, by comparison, overlooked. There is need for a more inclusive definition of homology. I propose that the basis of homology in the broad sense is the sharing of pathways of development, which are controlled by genealogically-related genes. Using this definition, one can construct hierarchies of homology, and recognize different degrees or strengths of homology. Because different aspects of structures are controlled by distinct developmental programs, it is sometimes necessary to speak of homologies of different attributes of specific structures, rather than to homologize the structures per se. For good biological reasons, parallelism may be difficult to distinguish from homology, and one must in practice be willing to tolerate some ambiguity between them. The formulation I present leads to some unorthodox conclusions about homology in mammalian dentitions and homology between the fore-and hindlimbs of tetrapods.     

Developmental genetic basis for the evolution of pelvic fin loss in the pufferfish Takifugu rubripes

Paired appendages were a key developmental innovation among vertebrates and they eventually evolved into limbs. Ancient developmental control systems for paired fins and limbs are broadly conserved among gnathostome vertebrates. Some lineages including whales, some salamanders, snakes, and many ray-fin fish, independently lost the pectoral, pelvic, or both appendages over evolutionary time. When different taxa independently evolve similar developmental morphologies, do they use the same molecular genetic mechanisms? To determine the developmental genetic basis for the evolution of pelvis loss in the pufferfish Takifugu rubripes (fugu), we isolated fugu orthologs of genes thought to be essential for limb development in tetrapods, including limb positioning (Hoxc6, Hoxd9), limb bud initiation (Pitx1, Tbx4, Tbx5), and limb bud outgrowth (Shh, Fgf10), and studied their expression patterns during fugu development. Results showed that bud outgrowth and initiation fail to occur in fugu, and that pelvis loss is associated with altered expression of Hoxd9a, which we show to be a marker for pelvic fin position in three-spine stickleback Gasterosteus aculeatus. These results rule out changes in appendage outgrowth and initiation genes as the earliest developmental defect in pufferfish pelvic fin loss and suggest that altered Hoxd9a expression in the lateral mesoderm may account for pelvis loss in fugu. This mechanism appears to be different from the mechanism for pelvic loss in stickleback, showing that different taxa can evolve similar phenotypes by different mechanisms.     

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.     

Limbs in whales and limblessness in other vertebrates: mechanisms of evolutionary and developmental transformation and loss

We address the developmental and evolutionary mechanisms underlying fore- and hindlimb development and progressive hindlimb reduction and skeletal loss in whales and evaluate whether the genetic, developmental, and evolutionary mechanisms thought to be responsible for limb loss in snakes "explain" loss of the hindlimbs in whales. Limb loss and concurrent morphological and physiological changes associated with the transition from land to water are discussed within the context of the current whale phylogeny. Emphasis is placed on fore- and hindlimb development, how the forelimbs transformed into flippers, and how the hindlimbs regressed, leaving either no elements or vestigial skeletal elements. Hindlimbs likely began to regress only after the ancestors of whales entered the aquatic environment: Hindlimb function was co-opted by the undulatory vertical axial locomotion made possible by the newly evolved caudal flukes. Loss of the hindlimbs was associated with elongation of the body during the transition from land to water. Limblessness in most snakes is also associated with adoption of a new (burrowing) lifestyle and was driven by developmental changes associated with elongation of the body. Parallels between adaptation to burrowing or to the aquatic environment reflect structural and functional changes associated with the switch to axial locomotion. Because they are more fully studied and to determine whether hindlimb loss in lineages that are not closely related could result from similar genetically controlled developmental pathways, we discuss developmental (cellular and genetic) processes that may have driven limb loss in snakes and leg-less lizards and compare these processes to the loss of hindlimbs in whales. In neither group does ontogenetic or phylogenetic limb reduction result from failure to initiate limb development. In both groups limb loss results from arrested development at the limb bud stage, as a result of inability to maintain necessary inductive tissue interactions and enhanced cell death over that seen in limbed tetrapods. An evolutionary change in Hox gene expression--as occurs in snakes--or in Hox gene regulation--as occurs in some limbless mutants--is unlikely to have initiated loss of the hindlimbs in cetaceans. Selective pressures acting on a wide range of developmental processes and adult traits other than the limbs are likely to have driven the loss of hindlimbs in whales.     

Expression of Hoxa-11 and Hoxa-13 in the pectoral fin of a basal ray-finned fish, Polyodon spathula: implications for the origin of tetrapod limbs

Summary Paleontological and anatomical evidence suggests that the autopodium (hand or foot) is a novel feature that distinguishes limbs from fins, while the upper and lower limb (stylopod and zeugopod) are homologous to parts of the sarcopterygian paired fins. In tetrapod limb development Hoxa-11 plays a key role in differentiating the lower limb and Hoxa-13 plays a key role in differentiating the autopodium. It is thus important to determine the ancestral functions of these genes in order to understand the developmental genetic changes that led to the origin of the tetrapod autopodium. In particular it is important to understand which features of gene expression are derived in tetrapods and which are ancestral in bony fishes. To address these questions we cloned and sequenced the Hoxa-11 and Hoxa-13 genes from the North American paddlefish, Polyodon spathula, a basal ray-finned fish that has a pectoral fin morphology resembling that of primitive bony fishes ancestral to the tetrapod lineage. Sequence analysis of these genes shows that they are not orthologous to the duplicated zebrafish and fugu genes. This implies that the paddlefish has not duplicated its HoxA cluster, unlike zebrafish and fugu. The expression of Hoxa-11 and Hoxa-13 in the pectoral fins shows two main phases: an early phase in which Hoxa-11 is expressed proximally and Hoxa-13 is expressed distally, and a later phase in which Hoxa-11 and Hoxa-13 broadly overlap in the distal mesenchyme of the fin bud but are absent in the proximal fin bud. Hence the distal polarity of Hoxa-13 expression seen in tetrapods is likely to be an ancestral feature of paired appendage development. The main difference in HoxA gene expression between fin and limb development is that in tetrapods (with the exception of newts) Hoxa-11 expression is suppressed by Hoxa-13 in the distal limb bud mesenchyme. There is, however, a short period of limb bud development where Hoxa-11 and Hoxa-13 overlap similarly to the late expression seen in zebrafish and paddlefish. We conclude that the early expression pattern in tetrapods is similar to that seen in late fin development and that the local exclusion by Hoxa-13 of Hoxa-11 from the distal limb bud is a derived feature of limb developmental regulation.     

Reconstructing pectoral appendicular muscle anatomy in fossil fish and tetrapods over the fins‐to‐limbs transition

The question of how tetrapod limbs evolved from fins is one of the great puzzles of evolutionary biology. While palaeontologists, developmental biologists, and geneticists have made great strides in explaining the origin and early evolution of limb skeletal structures, that of the muscles remains largely unknown. The main reason is the lack of consensus about appendicular muscle homology between the closest living relatives of early tetrapods: lobe‐finned fish and crown tetrapods. In the light of a recent study of these homologies, we re‐examined osteological correlates of muscle attachment in the pectoral girdle, humerus, radius, and ulna of early tetrapods and their close relatives. Twenty‐nine extinct and six extant sarcopterygians were included in a meta‐analysis using information from the literature and from original specimens, when possible. We analysed these osteological correlates using parsimony‐based character optimization in order to reconstruct muscle anatomy in ancestral lobe‐finned fish, tetrapodomorph fish, stem tetrapods, and crown tetrapods. Our synthesis revealed that many tetrapod shoulder muscles probably were already present in tetrapodomorph fish, while most of the more‐distal appendicular muscles either arose later from largely undifferentiated dorsal and ventral muscle masses or did not leave clear correlates of attachment in these taxa. Based on this review and meta‐analysis, we postulate a stepwise sequence of specific appendicular muscle acquisitions, splits, and fusions that led from the ancestral sarcopterygian pectoral fin to the ancestral tetrapod forelimb. This sequence largely agrees with previous hypotheses based on palaeontological and comparative work, but it is much more comprehensive in terms of both muscles and taxa. Combined with existing information about the skeletal system, our new synthesis helps to illuminate the genetic, developmental, morphological, functional, and ecological changes that were key components of the fins‐to‐limbs transition.     

Morphogenetic approach to the formation of paired limbs in the course of tetrapodization

Transition from sarcopterygians to tetrapods is analyzed based on new paleontological, ontogenetic, and molecular data. It is shown that transformation of skeletal fin elements into the tetrapod limb followed the patterns of divergent, parallel, and mosaic development. Morphogenetic plasticity and autonomy of these processes as well as the same developmental bauplan for the limbs of Urodela and Anura are proposed. Variations observed in these processes are regarded as a result of larval adaptations and heterochronies. The latter excludes recapitulation of successive archetypical states (transformation-development of the fish fin into tetrapod limb). The idea that the digits are a novelty relative to the distal radials of the fin is supported.     

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.     

New,puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma

Most textbooks and research reports state that the structures of the tetrapod forelimbs and hindlimbs are serial homologues. From this view, the main challenge of evolutionary biologists is not to explain the similarity between tetrapod limbs, but instead to explain why and how they have diverged. However, these statements seem to be related to a confusion between the serial homology of the vertebrate pelvic and pectoral appendages as a whole, and the serial homology of the specific soft‐ and hard‐tissue structures of the tetrapod forelimbs and hindlimbs, leading to an even more crucial and puzzling question being overlooked: why are the skeletal and particularly the muscle structures of the forelimb and hindlimb actually so strikingly similar to each other? Herein we provide an updated discussion of these questions and test two main hypotheses: (i) that the similarity of the limb muscles is due to serial homology; and (ii) that tetrapods that use hindlimbs for a largely exclusive function (e.g. bipedalism in humans) exhibit fewer cases of similarity between forelimbs and hindlimbs than do quadrupedal species. Our review shows that of the 23 arm, forearm and hand muscles/muscle groups of salamanders, 18 (78%) have clear ‘topological equivalents' in the hindlimb; in lizards, 14/24 (58%); in rats, 14/35 (40%); and in modern humans, 19/37 (51%). These numbers seem to support the idea that there is a plesiomorphic similarity and subsequent evolutionary divergence, but this tendency actually only applies to the three former quadrupedal taxa. Moreover, if one takes into account the total number of ‘correspondences’, one comes to a surprising and puzzling conclusion: in modern humans the number of forelimb muscles/muscle groups with clear ‘equivalents’ in the hindlimb (19) is substantially higher than in quadrupedal mammals such as rats (14), lizards (14) and even salamanders (18). These data contradict the hypothesis that divergent functions lead to divergent morphological structures. Furthermore, as we show that at least five of the 19 modern human adult forelimb elements that have a clear hindlimb ‘equivalent’ derive from embryonic anlages that are very different from the ones giving rise to their adult hindlimb ‘equivalents’, they also contradict the hypothesis that the similarity in muscle structures between the forelimb and hindlimb of tetrapods such as modern humans are due to their origin as serial homologues. This similarity is instead the result of phylogenetically independent evolutionary changes leading to a parallelism/convergence due to: (i) developmental constraints, i.e. similar molecular mechanisms are involved (particularly in the formation of the neomorphic hand), but this does not necessarily mean that similar anlages are used to form the similar adult structures; (ii) functional constraints, related to similar adaptations; (iii) topological constraints, i.e. limited physical possibilities; and even (iv) phylogenetic constraints, which tend to prevent/decrease the occurrence of new homoplasic similarities, but also help to keep older, ancestral homoplasic resemblances.     

Branching,segmentation and the metapterygial axis: pattern versus process in the vertebrate limb

Explanations of the patterns of vertebrate fin and limb evolution are improving as specific hypotheses based on molecular and developmental data are proposed and tested. Comparative analyses of gene expression patterns and functions in developing limbs, and morphological patterns in embryonic, adult and fossil limbs point to digit specification as a key developmental innovation associated with the origin of tetrapods. Digit development during the fin-to-limb transition involved sustained proximodistal outgrowth and a new phase of Hox gene expression in the distal fin bud. These patterning changes in the distal limb have been explained by the linked concepts of the metapterygial axis and the digital arch. These have been proposed to account for the generation of limb pattern by sequential branching and segmentation of precartilagenous elements along the proximodistal axis of the limb. While these ideas have been very fruitful, they have become increasingly difficult to reconcile with experimental and comparative studies of fin and limb development. Here we argue that limb development does not involve a branching mechanism, and reassess the concept of a metapterygial axis in limb development and evolution.     

Two Perspectives on the Evolution of the Tetrapod Limb

SYNOPSIS. The evolution of the tetrapod limb is examined fromtwo perspectives: structural and functional. Rosen et al. (1981)argued that lungfishes are the sister group of tetrapods, withlimb characteristics comprising an important subset of theirevidence. A re-analysis of the limb characters advocated byRosen et al. does not support their contention, but insteadsuggests that rhipidistian fishes of the family Osteolepidaeare the closest relatives of the tetrapods. In order to understandthe probable selective pressures leading to evolution of thetetrapod limb, a functional analysis of the fins of antennariidanglerfishes was performed. Antennariids use their limb-likefins to traverse underwater substrates. The analysis revealsa large number of functional and morphological convergencesbetween antennariid fins and tetrapod limbs. It is suggestedthat tetrapod limbs were evolved for underwater transport ratherthan for locomotion on dry land.     

CHARACTER DIAGNOSIS, FOSSILS AND THE ORIGIN OF TETRAPODS

I. The traditional view of the origin of tetrapod vertebrates is that they are descendants of fossil osteolepiform fish, of which Eusthenopteron is best known. In recent years both that conclusion and the methodology by which it has been reached have been challenged by practitioners of cladistic analysis. Particularly a recent review by Rosen et al. (1981) claims that Dipnoi (lungfish) are the sister-group of the Tetrapoda, that Osteolepiformes is a non-taxon and that Eusthenopteron is more distant from tetrapods than are Dipnoi, coelacanths and probably the fossil Porolepiformes. We attempt to refute all these concludions by use of the same cladistic technique. 2. We accept that all the above-mentioned groups, together with some less well-known taxa, can be united as Sarcopterygii by means of shared derived (apomorph) characters. We also agree that Porolepiformes and Actinistia (coelacanths) can be characterized as valid taxa. The primitive and enigmatic fossil fish Powichthys is accepted as representing the plesiomorph sister-group of true porolepiforms. 3. Only two apomorph features, the course of the jaw adductor muscles and the position of incurrent and excurrent nostrils, appear to unite all the fish, living and fossil, currently regarded as Dipnoi. The characteristic tooth plates and the presence of petrodentine both exclude important primitive fossil forms. 4. Contrary to the opinion of Rosen et al., Osteolepiformes can be characterized — by the arrangement of bones forming the cheek plate, the presence of basal scutes to the fins and by the unjointed radials of the median fins. However, if these are true autapomorphies they exclude any osteolepiform from direct tetrapod ancestry. 5. Tetrapoda is a monophyletic group characterized by ten or more autapomorphies, including the bones of the cheek plate, a stapes and fenestra ovalis, and a series of characters of the appendicular skeleton. 6. Tetrapods have a true choana (internal nostril). We accept that the posterior (excurrent) nostril of Dipnoi is the homologue of the tetrapod choana. However, we assert that the posterior nostril of all bony fish is the homologue of the choana. This assertion would be refuted if any fish showed separate posterior nostril and choana. We reject the claim that this ‘three nostril condition’ occurred in porolepiforms and osteolepiforms. The evidence for a choana in porolepiforms is inadequate. Osteolepiforms had a true choana, characterized as in tetrapods by its relationship to the bones of the palate, but no third nostril. Dipnoans are not choanate. 7. Following cladistic practice, the relationship of the extant taxa is established first. Dipnoi are thus shown to be the living sister-group of tetrapods, but only on ‘soft anatomy’ characters unavailable in fossils. Coelacanths are the living sister-group of the taxon so formed. 8. The relationship of the fossil taxa to the extant sarcopterygians is then considered. The synapomorphy scheme proposed by Rosen et al. is discussed at length. Virtually all the characters they use to exclude close relationship of Eusthenopteron (and hence all osteolepiforms) to tetrapods, in favour of coelacanths and dipnoans, are invalid. 9. A series of synapomorphies uniting osteolepiforms and tetrapods is proposed, including a true choana (hence the taxon Choanata), the histology of the teeth, and a number of characters of the humerus. The recently discovered fossil Youngolepis, which lacks a choana, represents the sister-group of the Choanata, and is not uniquely close to Powichthys. The latter, as a porolepiform (s.l.) is a member of the sister-group to Choanata plus Youngolepis. 10. Our cladistic analysis suggests that all the extinct taxa considered are more closely related to tetrapods than are the Dipnoi. Moreover fossil evidence suggests that Dipnoi, considered as an extant taxon, may not even be the living sister-group of Tetrapoda. Early fossil dipnoans appear to have been marine fish without specific adaptations for air breathing. If so the apparent synapomorphies of Dipnoi and Tetrapoda may be homoplastic — the insistence on grouping extant taxa first would then have yielded an invalid inference.     

Are lungfishes the sister group of tetrapods?

It is generally accepted that rhipaidistian crossopterygians are the closest relatives of tetrapods. Rosen, Forey, Gardiner & Patterson (1981) challenge this view and contend that lungfishes are the sister group of tetrapods. They present a detailed cladistic analysis and claim to identify a large number of synapomorphies shared by lungfishes and tetrapods but not by rhipidistians. Their analysis is faulty. Although Rosen et al. (1981) correctly emphasize that cladistic relationships must be based on shared derived characters, they often fail to take intragroup variation into account in postulating synapomorphies. They also use evidence inconsistently by attributing greater significance to similarities between lungfishes and tetrapods than to even more detailed similarities between rhipidistians and tetrapods. They misinterpret the skeletal pattern of the paired appendages. The many synapomorphies that they claim to have identified are either invalid, irrelevant, or are characters involving reduction or loss (which have a high probability of convergence). Consequently, they make an unconvincing case for a sister-group relationship between lungfishes and tetrapods. On the other hand, Rosen et al. (1981) do show that evidence for the orthodox view of rhipidistian-tetrapod relationships is not as strong as generally believed. The uncertain interrelationships among rhipidistians is a major problem. Tetrapod-fish relationships need to be re-examined by means of a properly conducted cladistic analysis.     

Ossification patterns in the tetrapod limb – conservation and divergence from morphogenetic events

Two different patterns of the condensation and chondrification of the limbs of tetrapods are known from extensive studies on their early skeletal development. These are on the one hand postaxial dominance in the sequential formation of skeletal elements in amniotes and anurans, and on the other, preaxial dominance in urodeles. The present study investigates the relative sequence of ossification in the fore‐ and hindlimbs of selected tetrapod taxa based on a literature survey in comparison to the patterns of early skeletal development, i.e. mesenchymal condensation and chondrification, representing essential steps in the late stages of tetrapod limb development. This reveals the degree of conservation and divergence of the ossification sequence from early morphogenetic events in the tetrapod limb skeleton. A step‐by‐step recapitulation of condensation and chondrification during the ossification of limbs can clearly be refuted. However, some of the deeper aspects of early skeletal patterning in the limbs, i.e. the general direction of development and sequence of digit formation are conserved, particularly in anamniotes. Amniotes show a weaker coupling of the ossification sequence in the limb skeleton with earlier condensation and chondrification events. The stronger correlation between the sequence of condensation/chondrification and ossification in the limbs of anamniotes may represent a plesiomorphic trait of tetrapods. The pattern of limb ossification across tetrapods also shows that some trends in the sequence of ossification of their limb skeleton are shared by major clades possibly representing phylogenetic signals. This review furthermore concerns the ossification sequence of the limbs of the Palaeozoic temnospondyl amphibian Apateon sp. For the first time this is described in detail and its patterns are compared with those observed in extant taxa. Apateon sp. shares preaxial dominance in limb development with extant salamanders and the specific order of ossification events in the fore‐ and hindlimb of this fossil dissorophoid is almost identical to that of some modern urodeles.     

Of chicken wings and frog legs: a smorgasbord of evolutionary variation in mechanisms of tetrapod limb development

The tetrapod limb, which has served as a paradigm for the study of development and morphological evolution, is becoming a paradigm for developmental evolution as well. In its origin and diversification, the tetrapod limb has undergone a great deal of remodeling. These morphological changes and other evolutionary phenomena have produced variation in mechanisms of tetrapod limb development. Here, we review that variation in the four major clades of limbed tetrapods. Comparisons in a phylogenetic context reveal details of development and evolution that otherwise may have been unclear. Such details include apparent differences in the mechanisms of dorsal-ventral patterning and limb identity specification between mouse and chick and mechanistic novelties in amniotes, anurans, and urodeles. As we gain a better understanding of the details of limb development, further differences among taxa will be revealed. The use of appropriate comparative techniques in a phylogenetic context thus sheds light on evolutionary transitions in limb morphology and the generality of developmental models across species and is therefore important to both evolutionary and developmental biologists.     

Why is limb regeneration possible in amphibians but not in reptiles,birds, and mammals?

The capacity to regenerate limbs is very high in amphibians and practically absent in other tetrapods despite the similarities in developmental pathways and ultimate morphology of tetrapod limbs. We propose that limb regeneration is only possible when the limb develops as a semiautonomous module and is not involved in interactions with transient structures. This hypothesis is based on the following two assumptions: To an important extent, limb development uses the same developmental mechanisms as normal limb development and developmental mechanisms that require interactions with transient structures cannot be recapitulated later. In amniotes limb development is early, shortly after neurulation, and requires inductive interactions with transient structures such as somites. In amphibians limb development is delayed relative to amniotes and has become decoupled from interactions with somites and other transient structures that are no longer present at this stage. The limb develops as a semi-independent module. A comparison of the autonomy and timing of limb development in different vertebrate taxa supports our hypothesis and its assumptions. The data suggest a good correlation between self-organizing and regenerative capacity. Furthermore, they suggest that whatever barriers amphibians overcame in the evolution of metamorphosis, they are the same barriers that need to be overcome to make limb regeneration possible in other taxa.     

Patterns of fluctuating asymmetry in the limbs of anurans

It has been hypothesized that fluctuating asymmetry (FA) may provide an indication of the functional importance of structures within an organism, with structures that more strongly impact fitness being more symmetric. Based on this idea, we predicted that for tetrapods in which the forelimbs and hindlimbs play an unequal role in locomotion, the less functionally important limb set should display higher levels of FA. We conducted a multispecies test of this hypothesis in anurans (frogs and toads), whose saltatory locomotor mode is powered by the hindlimbs. We also tested whether FA in the forelimbs, which play a more important role during landing, differed between families that differ in the degree of forelimb use in locomotion (Bufonidae vs. Ranidae). We calculated FA from the lengths of humeri and femora measured from disarticulated skeletal specimens of four anuran taxa (Bufonidae: Anaxyrus americanus, Rhinella marina; Ranidae: Lithobates catesbeianus, Lithobates clamitans). Our findings were consistent with the hypothesis that natural selection for increased locomotor performance may influence patterns of FA seen in vertebrate limbs, with all species displaying lower mean FA in the hindlimbs. More subtle functional roles between the forelimbs of bufonids and ranids, however, did not elicit different levels of FA.     

Musculoskeletal morphology of the pelvis and pelvic fins in the lungfish Protopterus annectens

The West African lungfish (Protopterus annectens) performs benthic, pelvic fin‐driven locomotion with gaits common to tetrapods, the sister group of the lungfishes. Features of P. annectens movement are similar to those of modern tetrapods and include use of the distal region of the pelvic fin as a “foot,” use of the fin to lift the body above the substrate and rotation of the fin around the joint with the pelvis. In contrast to these similarities in movement, the pelvic fins of P. annectens are long, slender structures that are superficially very different from tetrapod limbs. Here, we describe the musculoskeletal anatomy of the pelvis and pelvic fins of P. annectens with dissection, magnetic resonance imaging, histology and 3D‐reconstruction methods. We found that the pelvis is embedded in the hypaxial muscle by a median rostral and two dorsolateral skeletal projections. The protractor and retractor muscles at the base of the pelvic fin are fan‐shaped muscles that cup the femur. The skeletal elements of the fin are serially repeating cartilage cylinders. Along the length of the fin, repeating truncated cones of muscles, the musculus circumradialis pelvici, are separated by connective tissue sheets that connect the skeletal elements to the skin. The simplicity of the protractor and retractor muscles at the base of the fin is surprising, given the complex rotational movement those muscles generate. In contrast, the series of many repeating segmental muscles along the length of the fin is consistent with the dexterity of bending of the distal limb. P. annectens can provide a window into soft‐tissue anatomy and sarcopterygian fish fin function that complements the fossil data from related taxa. This work, combined with previous behavioral examination of P. annectens, illustrates that fin morphologies that do not appear to be capable of walking can accomplish that function, and may inform the interpretation of fossil anatomical evidence. J. Morphol. 275:431–441, 2014. © 2013 Wiley Periodicals, Inc.