Fins,limbs, and tails: outgrowths and axial patterning in vertebrate evolution

Current phylogenies show that paired fins and limbs are unique to jawed vertebrates and their immediate ancestry. Such fins evolved first as a single pair extending from an anterior location, and later stabilized as two pairs at pectoral and pelvic levels. Fin number, identity, and position are therefore key issues in vertebrate developmental evolution. Localization of the AP levels at which developmental signals initiate outgrowth from the body wall may be determined by Hox gene expression patterns along the lateral plate mesoderm. This regionalization appears to be regulated independently of that in the paraxial mesoderm and axial skeleton. When combined with current hypotheses of Hox gene phylogenetic and functional diversity, these data suggest a new model of fin/limb developmental evolution. This coordinates body wall regions of outgrowth with primitive boundaries established in the gut, as well as the fundamental nonequivalence of pectoral and pelvic structures. BioEssays 20 :371–381, 1998. © 1998 John Wiley & Sons Inc.     

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.     

Trophic convergence drives morphological convergence in marine tetrapods

Marine tetrapod clades (e.g. seals, whales) independently adapted to marine life through the Mesozoic and Caenozoic, and provide iconic examples of convergent evolution. Apparent morphological convergence is often explained as the result of adaptation to similar ecological niches. However, quantitative tests of this hypothesis are uncommon. We use dietary data to classify the feeding ecology of extant marine tetrapods and identify patterns in skull and tooth morphology that discriminate trophic groups across clades. Mapping these patterns onto phylogeny reveals coordinated evolutionary shifts in diet and morphology in different marine tetrapod lineages. Similarities in morphology between species with similar diets—even across large phylogenetic distances—are consistent with previous hypotheses that shared functional constraints drive convergent evolution in marine tetrapods.     

Patterns of correlation and covariation of anthropoid distal forelimb segments correspond to Hoxd expression territories

Anthropoids in general and hominoids in particular exhibit differential adaptations in forearm and digital skeletal proportions to a diverse array of locomotor modes. Hox genes act as selector genes with spatially regulated expression patterns during development. Their expression in the forelimb appears to define modules that specify differential skeletal growth. Here we explore forelimb skeletal proportions in a large sample of anthropoids from a background provided by Hoxd expression patterns in late-stage murine embryonic forelimbs. Interspecific correlation and principal components analyses of primate forelimb data indicate that morphological variation in anthropoids reflects well-defined developmental modules downstream of Hoxd expression. The phalanges of digit one appear to represent a single growth module, whereas the metacarpals and manual phalanges of the posterior digits correspond to a second, independent, expression territory that extends proximally into the distal zeugopod. In particular, hominoids show very high correlations among the posterior digits and the independence of digit one. In addition, the distal radius is generally highly correlated with the posterior digits and not digit one. Relying on established functional differences among Hox paralogs, we present a model that parsimoniously explains hominoid forearm and digital proportions as a consequence of downstream effects of Hox. We, therefore, suggest that Hox-defined developmental modules have served as evolutionary modules during manual evolution in anthropoids.     

Timing of organogenesis support basal position of turtles in the amniote tree of life

Background  

The phylogenetic position of turtles is the most disputed aspect in the reconstruction of the land vertebrate tree of life. This controversy has arisen after many different kinds and revisions of investigations of molecular and morphological data. Three main hypotheses of living sister-groups of turtles have resulted from them: all reptiles, crocodiles + birds or squamates + tuatara. Although embryology has played a major role in morphological studies of vertebrate phylogeny, data on developmental timing have never been examined to explore and test the alternative phylogenetic hypotheses. We conducted a comprehensive study of published and new embryological data comprising 15 turtle and eight tetrapod species belonging to other taxa, integrating for the first time data on the side-necked turtle clade.     

The evolution of paired fins

Summary The Archipterygium is Gegenbaur’s most lasting contribution to the study of vertebrate limb evolution. This transformational hypothesis of gill arches to limb girdles, rays to fins, and proposal of a vertebrate fin-limb groundplan, is generally treated as a flawed alternative to the more widely accepted lateral fin-fold hypothesis of vertebrate limb evolution. When compared to the phylogenetic distribution and diversity of fins and limbs, both hypotheses fail. Dermal skeletal lateral folds, spines and keels originate repeatedly in vertebrate evolution, but paired fins with girdles originate at pectoral level and are anteroposteriorly restricted. Pelvic fins emerge later in phylogeny; pectoral and pelvic appendages primitively differ. Endoskeletal girdles never exhibit characteristics of gill arches. The emergent sequence of paired fin evolution depends upon phylogenetic hypotheses within which extant agnathan interrelationships are uncertain; positions of jawless fossil fish along the gnathostome stem are insecure; the fossil data set is patchy. However, certain features of the data set are robust. This has prompted a reconsideration of Gegenbaur’s hypothesized arch-girdle relationship, and an iterative homology between scapulocoracoid and extrabranchial cartilages is suggested. No transformation of arch to girdle is necessarily implied, but some signal of developmental relatedness is predicted.     

Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development

The stratigraphically earliest and the most primitive examples of vertebrate skeletal mineralization belong to lineages that are entirely extinct. Therefore, palaeontology offers a singular opportunity to address the patterns and mechanisms of evolution in the vertebrate mineralized skeleton. We test the two leading hypotheses for the emergence of the four skeletal tissue types (bone, dentine, enamel, cartilage) that define the present state of skeletal tissue diversity in vertebrates. Although primitive vertebrate skeletons demonstrate a broad range of tissues that are difficult to classify, the first hypothesis maintains that the four skeletal tissue types emerged early in vertebrate phylogeny and that the full spectrum of vertebrate skeletal tissue diversity is explained by the traditional classification system. The opposing hypothesis suggests that the early evolution of the mineralized vertebrate skeleton was a time of plasticity and that the four tissue types did not emerge until later. On the basis of a considerable, and expanding, palaeontological dataset, we track the stratigraphic and phylogenetic histories of vertebrate skeletal tissues. With a cladistic perspective, we present findings that differ substantially from long-standing models of tissue evolution. Despite a greater diversity of skeletal tissues early in vertebrate phylogeny, our synthesis finds that bone, dentine, enamel and cartilage do appear to account for the full extent of this variation and do appear to be fundamentally distinct from their first inceptions, although why a higher diversity of tissue structural grades exists within these types early in vertebrate phylogeny is a question that remains to be addressed. Citing recent evidence that presents a correlation between duplication events in secretory calcium-binding phosphoproteins (SCPPs) and the structural complexity of mineralized tissues, we suggest that the high diversity of skeletal tissues early in vertebrate phylogeny may result from a low diversity of SCPPs and a corresponding lack of constraints on the mineralization of these tissues.     

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.     

The phylogenetic placement of Chondrichthyes: inferences from analysis of multiple genes and implications for comparative studies

Elasmobranch fishes (sharks and rays) have proven valuable for inferring general and specific properties of molecular evolution through comparative studies with crown group vertebrates because they are the most ancient group of gnathostomes. Recent studies have questioned the conventional phylogenetic placement of sharks in the vertebrate tree, however. In this paper I review the importance of the basal position of Chondrichthyes for comparative biology and compile evidence from multiple, independent genes to evaluate the phylogenetic placement of sharks. The results suggests that alternative phylogenetic hypotheses of the relationships among the Chondrichthyes, Actinopterygii and Sarcopterygii can not be refuted with available data, implying that the assumption of the basal placement of sharks in the vertebrate tree is suspect. Resolving the phylogeny of basal vertebrates is important for testing hypotheses about the evolution of vertebrates, and the current lack of a robust phylogeny limits evolutionary inferences that can be gained from comparative studies that include sharks and rays.     

Genome Duplications and Accelerated Evolution of Hox Genes and Cluster Architecture in Teleost Fishes

The early origin of four vertebrate Hox gene clusters duringthe evolution of gnathostomes was likely caused by two consecutiveduplications of the entire genome and the subsequent loss ofindividual genes. The presumed conserved and important rolesof these genes in tetrapods during development led to the generalassumption that Hox cluster architecture had remained unchangedsince the last common ancestor of all jawed vertebrates. Butrecent data from teleost fishes reveals that this is not thecase. Here, we present an analysis of the evolution of vertebrateHox genes and clusters, with emphasis on the differences betweenthe Hox A clusters of fish (actinopterygian) and tetrapod (sarcopterygian)lineages. In contrast to the general conservation of genomicarchitecture and gene sequence observed in sarcopterygians,the evolutionary history of actinopterygian Hox clusters likelyincludes an additional (third) genome duplication that initiallyincreased the number of clusters from four to eight. We document,for the first time, higher rates of gene loss and gene sequenceevolution in the Hox genes of fishes compared to those of landvertebrates. These two observations might suggest that two differentmolecular evolutionary strategies exist in the two major vertebratelineages. Preliminary data from the African cichlid fish Oreochromisniloticus compared to those of the pufferfish and zebrafishreveal important differences in Hox cluster architecture amongfishes and, together with genetic mapping data from Medaka,indicate that the third genome duplication was not zebrafish-specific,but probably occurred early in the history of fishes. Each descendingfish lineage that has been characterized so far, distinctivelymodified its Hox cluster architecture through independent secondarylosses. This variation is related to the large body plan differencesobserved among fishes, such as the loss of entire sets of appendagesand ribs in some lineages.     

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.     

Vertebrate Axial and Appendicular Patterning: The Early Development of Paired Appendages

Determination of paired fin or limb number, identity and positionare key issues in vertebrate development and evolution. Phylogeniesincluding fossil data show that paired appendages are uniqueto jawed vertebrates and their immediate ancestry; that suchfins evolved first as a single pair in an anterior location;that appendicular endoskeletons are primitively AP asymmetric;and that pectoral and pelvic fins primitively differ. It isconjectured that Hox gene expression patterns along the lateralplate mesoderm establish boundaries that contribute to localisationof AP levels at which signals initiate outgrowth from the bodywall. Such regionalisation may be regulated independently ofthat in the paraxial mesoderm and axial skeleton. When combinedwith current hypotheses of Hox gene phylogenetic and functionaldiversity, these data suggest a new model of fin/limb developmentalevolution. This coordinates body wall outgrowth regions withprimitive boundaries established in the gut, and the fundamentalnon-equivalence of pectoral and pelvic structures.     

Primitive versus derived traits in the developmental program of the vertebrate head: views from cyclostome developmental studies

Evolution can be viewed as a series of changes in the developmental program along the phylogenetic tree. To better understand the early evolution of the vertebrate skull, we can use the embryos of the cyclostome species as models. By comparing the cyclostome developmental patterns with those of gnathostomes, it becomes possible to distinguish the primitive and derived parts of the developmental program as taxon-specific traits. These traits are often recognizable as developmental constraints that define taxa by biasing the developmental trajectories within a certain limited range, resulting in morphological homologies in adults. These developmental constraints are distributed on the phylogenetic tree like the morphological character states of adult animals and are associated with specific regions of the tree. From this perspective, we emphasize the importance of considering gene expression and embryonic anatomy as the mechanistic bases that can result in homologous or nonhomologous morphological patterns at later developmental stages. Taking the acquisition of the jaw and trabecula cranii as examples, we demonstrate that a set of embryonic features can be coupled or decoupled during evolution and development. When they are coupled, they exert an ancestral developmental constraint that results in homologous morphological patterns, and when they are decoupled, the ancestral constraints tend to be abandoned, generating a new body plan. The heterotopy behind the specification of the oral domain is an example of decoupling, based on shifted tissue interactions. We also stress the importance of "developmental burden" in determining the sequential order of changes through evolution.     

The mitochondrial phylogeny of an ancient lineage of ray-finned fishes (Polypteridae) with implications for the evolution of body elongation,pelvic fin loss,and craniofacial morphology in Osteichthyes

Background  

The family Polypteridae, commonly known as "bichirs", is a lineage that diverged early in the evolutionary history of Actinopterygii (ray-finned fish), but has been the subject of far less evolutionary study than other members of that clade. Uncovering patterns of morphological change within Polypteridae provides an important opportunity to evaluate if the mechanisms underlying morphological evolution are shared among actinoptyerygians, and in fact, perhaps the entire osteichthyan (bony fish and tetrapods) tree of life. However, the greatest impediment to elucidating these patterns is the lack of a well-resolved, highly-supported phylogenetic tree of Polypteridae. In fact, the interrelationships of polypterid species have never been subject to molecular phylogenetic analysis. Here, we infer the first molecular phylogeny of bichirs, including all 12 recognized species and multiple subspecies using Bayesian analyses of 16S and cyt-b mtDNA. We use this mitochondrial phylogeny, ancestral state reconstruction, and geometric morphometrics to test whether patterns of morphological evolution, including the evolution of body elongation, pelvic fin reduction, and craniofacial morphology, are shared throughout the osteichthyan tree of life.     

Molecular data indicate the protostome affinity of brachiopods

Although the phylogenetic position of brachiopods has always been subject to debate, many authors place them as a sister group to deuterostomes on the basis of morphological and developmental characters. However, molecular phylogeny consistently places them among protostomes. More precisely, brachiopods are predicted to branch inside the lophotrochozoan assemblage, together with annelids, molluscs, nemerteans, flatworms, and others. That result has been criticized on the basis of (1) prior knowledge of brachiopod morphology and (2) the known limitations of molecular phylogenies. Here I review recent data of molecular origin, particularly those displaying qualitative properties close to those of morphological characters. The complement of Hox genes present in all metazoa tested to date has proved to be a powerful tool for broad phylogenetic reconstruction. The mitochondrial genome also provides qualitative characters, showing discrete events of gene rearrangements. After discussing the data and the way they should be interpreted in the perspective of several hypotheses for metazoan phylogeny, I conclude that they argue strongly in favor of the protostome (and lophotrochozoan) affinity of the brachiopods. There is therefore a need for a reinterpretation of brachiopod morphological and developmental characters. I also identify some research axes on brachiopod morphology.     

HOW LIZARDS TURN INTO SNAKES: A PHYLOGENETIC ANALYSIS OF BODY-FORM EVOLUTION IN ANGUID LIZARDS

Abstract One of the most striking morphological transformations in vertebrate evolution is the transition from a lizardlike body form to an elongate, limbless (snakelike) body form. Despite its dramatic nature, this transition has occurred repeatedly among closely related species (especially in squamate reptiles), making it an excellent system for studying macroevolutionary transformations in body plan. In this paper, we examine the evolution of body form in the lizard family Anguidae, a clade in which multiple independent losses of limbs have occurred. We combine a molecular phylogeny for 27 species, our morphometric data, and phylogenetic comparative methods to provide the first statistical phylogenetic tests of several long‐standing hypotheses for the evolution of snakelike body form. Our results confirm the hypothesized relationships between body elongation and limb reduction and between limb reduction and digit reduction. However, we find no support for the hypothesized sequence going from body elongation to limb reduction to digit loss, and we show that a burrowing lifestyle is not a necessary correlate of limb loss. We also show that similar degrees of overall body elongation are achieved in two different ways in anguids, that these different modes of elongation are associated with different habitat preferences, and that this dichotomy in body plan and ecology is widespread in limb‐reduced squamates. Finally, a recent developmental study has proposed that the transition from lizardlike to snakelike body form involves changes in the expression domains of midbody Hox genes, changes that would link elongation and limb loss and might cause sudden transformations in body form. Our results reject this developmental model and suggest that this transition involves gradual changes occurring over relatively long time scales.     

Hox, ParaHox, ProtoHox: facts and guesses

The Hox gene cluster has captivated the imagination of evolutionary and developmental biologists worldwide. In this review, the origin of the Hox and ParaHox gene clusters by duplication of a ProtoHox gene cluster, and the changes in their gene numbers in major Metazoan Transitions are reviewed critically. Re-evaluation of existing data and recent findings in Cnidarians, Acoels, and critical stages of vertebrate evolution suggest alternative scenarios for the origin, structure, and changes in Hox gene numbers in relevant events of Metazoan evolution. I discuss opposing views and propose that (i) the ProtoHox cluster had only two genes, and not four as commonly believed: a corollary is that the origin of Bilaterians was coincident with the invention of new Hox and ParaHox gene classes, which may have facilitated such a transition; (ii) the ProtoHox cluster duplication was a cis duplication event, rather than a trans duplication event, as previously suggested, and (iii) the ancestral vertebrate cluster possessed 14 Hox genes, and not the 13 generally assumed. These hypotheses could be verified or refuted in the near future, but they may help critical discussion of the evolution of the Hox/ParaHox family in the metazoan kingdom.     

A Brief Review of Metazoan Phylogeny and Future Prospects in Hox-Research

Underlying any analysis on the evolution of development is aphylogenetic framework, whether explicitly stated or implied.As such, differing views on phylogenetic relationships leadto variable interpretations of how developmental mechanismshave changed through time. Over the past decade, many long-standinghypotheses about animal evolution have been questioned causingsubstantial changes in the assumed phylogenetic framework underlyingcomparative developmental studies. Current hypotheses aboutearly metazoan history suggest that three, not two, major lineagesof bilateral animals originated in the Precambrian: the Deuterostomes(e.g., seastars, acorn worms, and vertebrates), the Ecdysozoans(e.g., nematodes and arthropods), and the Lophotrochozoans (e.g.,annelids, mollusks, and lophophorates). Although informationin Hox-genes bears directly on our understanding of early metazoanevolution and the formation of body plans, research effort hasbeen focused primarily on two taxa, insects and vertebrates.By sampling a greater diversity of metazoan taxa and takingadvantage of biotechnological advances in genomics, we willnot only learn more about metazoan phylogeny, but will alsogain valuable insight as to the key evolutionary forces thatestablished and maintained metazoan bauplans.