Evolutionary and developmental origins of the cardiac neural crest: Building a divided outflow tract

The cardiac neural crest cells (CNCCs) have played an important role in the evolution and development of the vertebrate cardiovascular system: from reinforcement of the developing aortic arch arteries early in vertebrate evolution, to later orchestration of aortic arch artery remodeling into the great arteries of the heart, and finally outflow tract septation in amniotes. A critical element necessary for the evolutionary advent of outflow tract septation was the co‐evolution of the cardiac neural crest cells with the second heart field. This review highlights the major transitions in vertebrate circulatory evolution, explores the evolutionary developmental origins of the CNCCs from the third stream cranial neural crest, and explores candidate signaling pathways in CNCC and outflow tract evolution drawn from our knowledge of DiGeorge Syndrome. Birth Defects Research (Part C) 102:309–323, 2014. © 2014 Wiley Periodicals, Inc.     

Teleost fish with specific genome duplication as unique models of vertebrate evolution

Whole-genome duplication (WGD) is believed to be one of the major evolutionary events that shaped the genome organization of vertebrates. Here, we review recent research on vertebrate genome evolution, specifically on WGD and its consequences for gene and genome evolution in teleost fishes. Recent genome analyses confirmed that all vertebrates experienced two rounds of WGD early in their evolution, and that teleosts experienced a subsequent additional third-round (3R)-WGD. The 3R-WGD was estimated to have occurred 320–400 million years ago in a teleost ancestor, but after its divergence from a common ancestor with living non-teleost actinopterygians (Bichir, Sturgeon, Bowfin, and Gar) based on the analyses of teleost-specific duplicate genes. This 3R-WGD was confirmed by synteny analysis and ancestral karyotype inference using the genome sequences of Tetraodon and medaka. Most of the tetrapods, on the other hand, have not experienced an additional WGD; however, they have experienced repeated chromosomal rearrangements throughout the whole genome. Therefore, different types of chromosomal events have characterized the genomes of teleosts and tetrapods, respectively. The 3R-WGD is useful to investigate the consequences of WGD because it is an evolutionarily recent WGD and thus teleost genomes retain many more WGD-derived duplicates and “traces” of their evolution. In addition, the remarkable morphological, physiological, and ecological diversity of teleosts may facilitate understanding of macrophenotypic evolution on the basis of genetic/genomic information. We highlight the teleosts with 3R-WGD as unique models for future studies on ecology and evolution taking advantage of emerging genomics technologies and systems biology environments.     

Evolution of sarcomeric myosin heavy chain genes: evidence from fish

Myosin heavy chain (MYH) is a major structural protein, integral to the function of sarcomeric muscles. We investigated both exon-intron organization and amino acid sequence of sarcomeric MYH genes to infer their evolutionary history in vertebrates. Our results were consistent with the hypothesis that a multigene family encoded MYH proteins in the ancestral chordate, one gene ancestral to human MYH16 and its homologues and another ancestral to all other vertebrate sarcomeric MYH genes. We identified teleost homologues of mammalian skeletal and cardiac MYH genes, indicating that the ancestors of those genes were present before the divergence of actinopterygians and sarcopterygians. Indeed, the ancestral skeletal genes probably duplicated at least once before the divergence of teleosts and tetrapods. Fish homologues of mammalian skeletal MYH are expressed in skeletal tissue and homologues of mammalian cardiac genes are expressed in the heart but, unlike mammals, there is overlap between these expression domains. Our analyses inferred two other ancestral vertebrate MYH genes, giving rise to human MYH14 and MYH15 and their homologues. Relative to the skeletal and cardiac genes, MYH14 and MYH15 homologues are characterized by evolution of intron position, differences in evolutionary rate between the functionally differentiated head and rod of the myosin protein, and possible evolution of function among vertebrate classes. Tandem duplication and gene conversion appear to have played major roles in the evolution of at least cardiac and skeletal MYH genes in fish. One outcome of this high level of concerted evolution is that different fish taxa have different suites of MYH genes, i.e., true orthologs do not exist.     

Lessons from parasitic flatworms about evolution and historical biogeography of their vertebrate hosts

Cophylogenetic studies investigate the evolutionary trends within host-parasite associations. Examination of the different levels of fidelity between host and parasite phylogenies provides a powerful tool to inspect patterns and processes of parasite diversification over host evolution and geological times. Within the phylum Platyhelminthes, the monogeneans are mainly fish parasites. The Polystomatidae, however, are known from the sarcopterygian Australian lungfish and tetrapods such as amphibians, freshwater turtles, and the African hippopotamus. Cophylogenetic and biogeographic vicariance analyses, supplemented by molecular calibrations, showed that the Polystomatidae may track the evolutionary history of the first aquatic tetrapods in the Palaeozoic age. Evolutionary lines of the major polystome lineages would also be intimately related to the evolution of their hosts over hundreds of millions years. Since the Mesozoic, evolution of polystomes would have been shaped mainly by plate tectonics during the break-up of Gondwanaland and subsequent dispersal of ancestral neobatrachian host lineages. Therefore the Polystomatidae could serve as a novel model to improve cophylogenetic tools and to inspect a suite of questions about the evolution of vertebrate hosts. To cite this article: O. Verneau et al., C. R. Biologies 332 (2009).     

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.     

A Standard System to Study Vertebrate Embryos

Staged embryonic series are important as reference for different kinds of biological studies. I summarise problems that occur when using ‘staging tables’ of ‘model organisms’. Investigations of developmental processes in a broad scope of taxa are becoming commonplace. Beginning in the 1990s, methods were developed to quantify and analyse developmental events in a phylogenetic framework. The algorithms associated with these methods are still under development, mainly due to difficulties of using non-independent characters. Nevertheless, the principle of comparing clearly defined newly occurring morphological features in development (events) in quantifying analyses was a key innovation for comparative embryonic research. Up to date no standard was set for how to define such events in a comparative approach. As a case study I compared the external development of 23 land vertebrate species with a focus on turtles, mainly based on reference staging tables. I excluded all the characters that are only identical for a particular species or general features that were only analysed in a few species. Based on these comparisons I defined 104 developmental characters that are common either for all vertebrates (61 characters), gnathostomes (26), tetrapods (3), amniotes (7), or only for sauropsids (7). Characters concern the neural tube, somite, ear, eye, limb, maxillary and mandibular process, pharyngeal arch, eyelid or carapace development. I present an illustrated guide listing all the defined events. This guide can be used for describing developmental series of any vertebrate species or for documenting specimen variability of a particular species. The guide incorporates drawings and photographs as well as consideration of species identifying developmental features such as colouration. The simple character-code of the guide is extendable to further characters pertaining to external and internal morphological, physiological, genetic or molecular development, and also for other vertebrate groups not examined here, such as Chondrichthyes or Actinopterygii. An online database to type in developmental events for different stages and species could be a basis for further studies in comparative embryology. By documenting developmental events with the standard code, sequence heterochrony studies (i.e. Parsimov) and studies on variability can use this broad comparative data set.     

Zebrafish models in cardiac development and congenital heart birth defects

The zebrafish has become an ideal vertebrate animal system for investigating cardiac development due to its genetic tractability, external fertilization, early optical clarity and ability to survive without a functional cardiovascular system during development. In particular, recent advances in imaging techniques and the creation of zebrafish transgenics now permit the in vivo analysis of the dynamic cellular events that transpire during cardiac morphogenesis. As a result, the combination of these salient features provides detailed insight as to how specific genes may influence cardiac development at the cellular level. In this review, we will highlight how the zebrafish has been utilized to elucidate not only the underlying mechanisms of cardiac development and human congenital heart diseases (CHDs), but also potential pathways that may modulate cardiac regeneration. Thus, we have organized this review based on the major categories of CHDs-structural heart, functional heart, and vascular/great vessel defects, and will conclude with how the zebrafish may be further used to contribute to our understanding of specific human CHDs in the future.     

The multifaceted role of Notch in cardiac development and disease

Notch receptors and their cognate ligands transduce crucial signals between cells in various tissues, and have been conserved across millions of years of evolution. Mutations in Notch signalling components result in congenital heart defects in humans and mice, demonstrating an essential role for Notch in cardiovascular development. The results of recent experiments implicate this signalling pathway in many stages of heart development, and provide mechanistic insight into the vital functions of Notch in the aetiology of several common forms of paediatric and adult cardiac disease.     

Developmental Data and Phylogenetic Systematics: Evolution of the Vertebrate Limb

Among the primary contributions of phylogenetic systematicsto the synthesis of developmental biology and evolution arephylogenetic hypotheses. Phylogenetic hypotheses are criticalin interpreting the patterns of evolution of developmental genesand processes, as are morphological data. Using a robust phylogeny,the evolutionary history of individual morphological or developmentalfeatures can be traced and ancestral conditions inferred. Multiplecharacters (e.g., morphological and developmental) can be mappedtogether on the phylogeny, and patterns of character associationcan be quantified and tested for correlation. Using the vertebrate forelimb as an example, I show that bymapping accurate morphological data (homologous skeletal elementsof the vertebrate forelimb) onto a phylogeny, an alternativeinterpretation of Hox gene expression emerges. Teleost fishesand tetrapods may share no homologous skeletal elements in theirforelimbs, and thus similarities and differences in Hox patternsduring limb development must be reinterpreted. Specifically,the presence of the phase III Hox pattern in tetrapods may notbe correlated with digits but rather may simply be the normalexpression pattern of a metapterygium in fishes. This exampleillustrates the rigorous hypotheses that can be developed usingmorphological data and phylogenetic methods. "Creating a general reference system and investigating the relationsthat extend from it to all other possible and necessary systemsin biology is the task of systematics." (Hennig, 1966, p.7)     

Evolution of neurohypophyseal hormones and their receptors.

Nine active neurohypophyseal principles have been isolated and identified among the vertebrates. Arginine-vasotocin is the most ubiquitous, occurring in pituitary glands from representatives of all the major vertebrate groups. There is much more variation in structure among the principles that resemble oxytocin. The manner in which these evolved remains unclear. Arginine-vasotocin stimulates smooth muscles from a wide variety of vertebrate species. It can stimulate contraction of oviducts from many jawed fishes and tetrapods. The oxytocin-like peptides are usually less active in this respect. Among adult mammals arginine-vasotocin is replaced by arginine-vasopressin which has much less oxytocin activity. Thus, although arginine-vasotocin may both stimulate oviducts and cause water retention in nonmammalian tetrapods, oxytocic and antidiuretic functions can be regulated independently by oxytocin and vasopressin in mammals. Arginine-vasotocin elicits vasoconstrictor responses in even the most primitive vertebrates. These may be systemic or regional. Their distribution may determine whether arginine-vasotocin acts as a diuretic or an antidiuretic agent. It is possible that the most primitive neurohypophyseal functions were related to cardiovascular regulation and that the neurohypophysis acquired its osmoregulatory functions later in vertebrate evolution.     

The corticostriatal junction: a crucial region for forebrain development and evolution

Most parts of the brain are conserved across reptiles and birds (sauropsids) and mammals. Two major qualitative differences occur in the upper part, or pallium, of the telencephalon, the most rostral part of the brain. Mammals have a six-layered neocortex and also exhibit a different morphological organization in the lateral half, or sector, of their pallium than do sauropsids. These differences of lateral pallial construction may derive from small but crucial differences in migration patterns of neuronal precursors generated at or above the corner of the lateral ventricle, the corticostriatal junction (CS). Sauropsids have a large structure, the dorsal ventricular ridge, that is proliferated from this region, and its anterior part (ADVR) receives ascending projections from the dorsal thalamus. Mammals have multiple structures in this same region-the lateral part of neocortex, amygdala, and claustrum-endopiriform formation. We propose here that, as the degree of development of structures that form the deeper tier of the pallium varies across the stages of embryology and across phylogeny, mutations may have occurred during evolution at the origin of mammals that had profound consequences for the fate of neural populations generated in the region of the CS and its neighboring pallial germinal zone.     

Development of mandibular,hyoid and hypobranchial muscles in the zebrafish: homologies and evolution of these muscles within bony fishes and tetrapods

Background  

During vertebrate head evolution, muscle changes accompanied radical modification of the skeleton. Recent studies have suggested that muscles and their innervation evolve less rapidly than cartilage. The freshwater teleostean zebrafish (Danio rerio) is the most studied actinopterygian model organism, and is sometimes taken to represent osteichthyans as a whole, which include bony fishes and tetrapods. Most work concerning zebrafish cranial muscles has focused on larval stages. We set out to describe the later development of zebrafish head muscles and compare muscle homologies across the Osteichthyes.     

Human cardiomyocyte progenitor cells: a short history of nearly everything

The high occurrence of cardiac disease in the Western world has driven clinicians and cardiovascular biologists to look for alternative strategies to treat patients. A challenging approach is the use of stem cells to repair the heart, in itself an inspiring thought. In the past 10 years, stem cells from different sources have been under intense investigation and, as a result, a multitude of studies have been published on the identification, isolation, and characterization, of cardiovascular progenitor cells and repair in different animal models. However, relatively few cardiovascular progenitor populations have been identified in human hearts, including, but not limited to, cardiosphere-derived cells, cKit+ human cardiac stem cells , Isl1+ cardiovascular progenitors, and, in our lab, cardiomyocyte progenitor cells (CMPCs). Here, we aim to provide a comprehensive summary of the past findings and present challenges for future therapeutic potential of CMPCs.     

Dermal bone in early tetrapods: a palaeophysiological hypothesis of adaptation for terrestrial acidosis

The dermal bone sculpture of early, basal tetrapods of the Permo-Carboniferous is unlike the bone surface of any living vertebrate, and its function has long been obscure. Drawing from physiological studies of extant tetrapods, where dermal bone or other calcified tissues aid in regulating acid-base balance relating to hypercapnia (excess blood carbon dioxide) and/or lactate acidosis, we propose a similar function for these sculptured dermal bones in early tetrapods. Unlike the condition in modern reptiles, which experience hypercapnia when submerged in water, these animals would have experienced hypercapnia on land, owing to likely inefficient means of eliminating carbon dioxide. The different patterns of dermal bone sculpture in these tetrapods largely correlates with levels of terrestriality: sculpture is reduced or lost in stem amniotes that likely had the more efficient lung ventilation mode of costal aspiration, and in small-sized stem amphibians that would have been able to use the skin for gas exchange.     

The representation of heart development in the gene ontology

An understanding of heart development is critical in any systems biology approach to cardiovascular disease. The interpretation of data generated from high-throughput technologies (such as microarray and proteomics) is also essential to this approach. However, characterizing the role of genes in the processes underlying heart development and cardiovascular disease involves the non-trivial task of data analysis and integration of previous knowledge. The Gene Ontology (GO) Consortium provides structured controlled biological vocabularies that are used to summarize previous functional knowledge for gene products across all species. One aspect of GO describes biological processes, such as development and signaling.In order to support high-throughput cardiovascular research, we have initiated an effort to fully describe heart development in GO; expanding the number of GO terms describing heart development from 12 to over 280. This new ontology describes heart morphogenesis, the differentiation of specific cardiac cell types, and the involvement of signaling pathways in heart development. This work also aligns GO with the current views of the heart development research community and its representation in the literature. This extension of GO allows gene product annotators to comprehensively capture the genetic program leading to the developmental progression of the heart. This will enable users to integrate heart development data across species, resulting in the comprehensive retrieval of information about this subject.The revised GO structure, combined with gene product annotations, should improve the interpretation of data from high-throughput methods in a variety of cardiovascular research areas, including heart development, congenital cardiac disease, and cardiac stem cell research. Additionally, we invite the heart development community to contribute to the expansion of this important dataset for the benefit of future research in this area.     

Perspectives on the convergent evolution of tetrapod salt glands

Since their discovery in 1958, the function of specialized salt-secreting glands in tetrapods has been studied in great detail, and such studies continue to contribute to a general understanding of transport mechanisms of epithelial water and ions. Interestingly, during that same time period, there have been only few attempts to understand the convergent evolution of this tissue, likely as a result of the paucity of taxonomic, embryological, and molecular data available. In this review, we synthesize the available data regarding the distribution of salt glands across extant and extinct tetrapod lineages and the anatomical position of the salt gland in each taxon. Further, we use these data to develop hypotheses about the various factors that have influenced the convergent evolution of salt glands across taxa with special focus on the variation in the anatomical position of the glands and on the molecular mechanisms that may have facilitated the development of a salt gland by co-option of a nonsalt-secreting ancestral gland. It is our hope that this review will stimulate renewed interest in the topic of the convergent evolution of salt glands and inspire future empirical studies aimed at evaluating the hypotheses we lay out herein.     

Oropharyngeal morphology in the basal tortoise Manouria emys emys with comments on form and function of the testudinid tongue

In tetrapods, the ability to ingest food on land is based on certain morphological features of the oropharynx in general and the feeding apparatus in particular. Recent paleoecological studies imply that terrestrial feeding has evolved secondarily in turtles, so they had to meet the morphological oropharyngeal requirements independently to other amniotes. This study is designed to improve our limited knowledge about the oropharyngeal morphology of tortoises by analyzing in detail the oropharynx in Manouria emys emys. Special emphasis is placed on the form and function of the tongue. Even if Manouria is considered a basal member of the only terrestrial turtle clade and was hypothesized to have retained some features reflecting an aquatic ancestry, Manouria shows oropharyngeal characteristics found in more derived testudinids. Accordingly, the oropharyngeal cavity in Manouria is richly structured and the glands are large and complexly organized. The tongue is large and fleshy and bears numerous slender papillae lacking lingual muscles. The hyolingual skeleton is mainly cartilaginous, and the enlarged anterior elements support the tongue and provide insertion sides for the well‐developed lingual muscles, which show striking differences to other reptiles. We conclude that the oropharyngeal design in Manouria differs clearly from semiaquatic and aquatic turtles, as well as from other reptilian sauropsids. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Induction and patterning of the cardiac conduction system

The cardiac conduction system (CCS) is the component of the heart that initiates and maintains a rhythmic heartbeat. As the embryonic heart forms, the CCS must continue to develop and mature in a coordinated manner to ensure that proper pace making potential and distribution of action potential is maintained at all stages. This requires not only the formation of distinct and disparate components of the CCS, but the integration of these components into a functioning whole as the heart matures. Though research in this area of development may have lagged behind other areas of heart development, in recent years there has been much progress in understanding the ontogeny of the CCS and the developmental cues that drive its formation. This is largely due to studies on the avian heart as well as the use of molecular biology approaches. This review gives a perspective on advances in understanding the development of the vertebrate CCS, and reports new data illuminating the mechanism of conduction cell determination and maintenance in the mammalian heart. As much of our knowledge about the development of the CCS has been derived from the chick embryo, one important area facing the field is the relationship and similarities between the structure and development of avian and mammalian conduction systems. Specifically, the morphology of the distal elements of the mammalian CCS and the manner in which its components are recruited from working cardiomyocytes are areas of research that will, hopefully, receive more attention in the near future. A more general and outstanding question is how the disparate components of all vertebrate conduction systems integrate into a functional entity during embryogenesis. There is mounting evidence linking the patterning and formation of the CCS to instructive cues derived from the cardiac vasculature and, more specifically, to hemodynamic-responsive factors produced by cardiac endothelia. This highlights the need for a greater understanding of the biophysical forces acting on, and created by, the cardiovascular system during embryonic development. A better understanding of these processes will be necessary if therapeutics are to be developed that allow the regeneration of damaged cardiac tissues or the construction of biologically engineered heart tissues.     

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.