Comparative Developmental Data Research Articles

Molecular Evolution across Mouse Spermatogenesis.

Genes involved in spermatogenesis tend to evolve rapidly, but we lack a clear understanding of how protein sequences and patterns of gene expression evolve across this complex developmental process. We used fluorescence-activated cell sorting (FACS) to generate expression data for early (meiotic) and late (postmeiotic) cell types across 13 inbred strains of mice (Mus) spanning ∼7 My of evolution. We used these comparative developmental data to investigate the evolution of lineage-specific expression, protein-coding sequences, and expression levels. We found increased lineage specificity and more rapid protein-coding and expression divergence during late spermatogenesis, suggesting that signatures of rapid testis molecular evolution are punctuated across sperm development. Despite strong overall developmental parallels in these components of molecular evolution, protein and expression divergences were only weakly correlated across genes. We detected more rapid protein evolution on the X chromosome relative to the autosomes, whereas X-linked gene expression tended to be relatively more conserved likely reflecting chromosome-specific regulatory constraints. Using allele-specific FACS expression data from crosses between four strains, we found that the relative contributions of different regulatory mechanisms also differed between cell types. Genes showing cis-regulatory changes were more common late in spermatogenesis, and tended to be associated with larger differences in expression levels and greater expression divergence between species. In contrast, genes with trans-acting changes were more common early and tended to be more conserved across species. Our findings advance understanding of gene evolution across spermatogenesis and underscore the fundamental importance of developmental context in molecular evolutionary studies.

Conserved Mechanisms, Novel Anatomies: The Developmental Basis of Fin Evolution and the Origin of Limbs

The transformation of paired fins into tetrapod limbs is one of the most intensively scrutinized events in animal evolution. Early anatomical and embryological datasets identified distinctive morphological regions within the appendage and posed hypotheses about how the loss, gain, and transformation of these regions could explain the observed patterns of both extant and fossil appendage diversity. These hypotheses have been put to the test by our growing understanding of patterning mechanisms that regulate formation of the appendage axes, comparisons of gene expression data from an array of phylogenetically informative taxa, and increasingly sophisticated and elegant experiments leveraging the latest molecular approaches. Together, these data demonstrate the remarkable conservation of developmental mechanisms, even across phylogenetically and morphologically disparate taxa, as well as raising new questions about the way we view homology, evolutionary novelty, and the often non-linear connection between morphology and gene expression. In this review, we present historical hypotheses regarding paired fin evolution and limb origins, summarize key aspects of central appendage patterning mechanisms in model and non-model species, address how modern comparative developmental data interface with our understanding of appendage anatomy, and highlight new approaches that promise to provide new insight into these well-traveled questions.

Homology conundrum among foreguts of caenogastropod molluscs: A view from comparative patterns of development

AbstractEvolution of two novel feeding strategies among caenogastropod molluscs, suspension feeding in calyptraeids such as Crepidula fornicata and predatory feeding with a pleurembolic proboscis among neogastropods, may have both involved elongation of the anterior esophagus. Emergence of predatory feeding with a proboscis is particularly significant because it correlates with the rapid adaptive radiation of buccinoidean and muricoidean neogastropods during the Cretaceous. However, the notion that this important evolutionary transition involved elongation of the anterior esophagus to extend down a long proboscis has been disputed by evidence that it may have been the wall of the buccal cavity that elongated. We undertook a comparative study on foregut morphogenesis during larval and metamorphic development in C. fornicata and in three species of neogastropods with a pleurembolic proboscis to examine the hypothesis that the same region of foregut has elongated in all. We approached this by identifying a conserved marker for the boundary between buccal cavity and anterior esophagus, which was recognizable before the developing foregut showed regional differences in length. A survey of four species of littorinimorph caenogastropods suggested that the site of neurogenic placodes for the buccal ganglia could serve as this marker. Results showed that foregut lengthening in C. fornicata involved elongation posterior to neurogenic placodes for buccal ganglia, an area that corresponded to the anterior esophagus in the other littorinimorphs. However, foregut elongation occurred anterior to neurogenic placodes for buccal ganglia in two buccinoidean and one muricoidean neogastropod. The elongated foregut within the pleurembolic proboscis of these neogastropods qualifies as anterior esophagus only if the definition of the anterior esophagus is expanded to include the dorsal folds that run down the roof of the buccal cavity. Regardless of how the anterior esophagus is defined, comparative developmental data do not support the hypothesis of homology between the elongated adult foregut regions in C. fornicata and in neogastropods with a pleurembolic proboscis.

Developmental and Evolutionary Perspectives on the Origin and Diversification of Arthropod Appendages.

Jointed, segmented appendages are a key innovation of arthropods. The subsequent diversification of these appendages, both along the body axis and across taxa, has contributed to the evolutionary success of arthropods. Both developmental and fossil data are informative for understanding how these transitions occurred. Comparative analyses help to pinpoint the developmental novelties that distinguish arthropod appendages from the lobopodous appendages of other panarthropods, and that distinguish different appendage types. The fossil record of stem group arthropods is diverse and preserves intermediate steps in these evolutionary transitions, including some that cannot be directly inferred based on extant taxa. These lead to hypotheses that can be tested with comparative developmental data, as well as to reinterpretations of developmental results. One developmental novelty of arthropods is the reiterated deployment of the joint formation network, which divides the appendages into segments. The fossil record raises questions about how this joint formation network was first deployed, given the contrasting morphologies of appendages in stem group versus extant arthropods. The fossil record supports a character tree for appendage diversification showing progressive individuation of appendages in an anterior-to-posterior sequence. However, to date, developmental evidence provides at best limited support for this character tree. Recent interpretations of the fossil record suggest that the labrum of extant arthropods is a greatly reduced protocerebral appendage pair; this hypothesis is consistent with the extensive shared developmental patterning of the labrum and jointed appendages. Reciprocal illumination from fossils and developmental patterning in a phylogenetic context both makes sense of some results and helps motivates questions for future research.

Sexual reproduction, sporophyte development and molecular variation in the model moss Physcomitrella patens: introducing the ecotype Reute

Rich ecotype collections are used for several plant models to unravel the molecular causes of phenotypic differences, and to investigate the effects of environmental adaption and acclimation. For the model moss Physcomitrella patens collections of accessions are available, and have been used for phylogenetic and taxonomic studies, for example, but few have been investigated further for phenotypic differences. Here, we focus on the Reute accession and provide expression profiling and comparative developmental data for several stages of sporophyte development, as well as information on genetic variation via genomic sequencing. We analysed cross-technology and cross-laboratory data to define a confident set of 15 mature sporophyte-specific genes. We find that the standard laboratory strain Gransden produces fewer sporophytes than Reute or Villersexel, although gametangia develop with the same time course and do not show evident morphological differences. Reute exhibits less genetic variation relative to Gransden than Villersexel, yet we found variation between Gransden and Reute in the expression profiles of several genes, as well as variation hot spots and genes that appear to evolve under positive Darwinian selection. We analyzed expression differences between the ecotypes for selected candidate genes in the GRAS transcription factor family, the chalcone synthase family and in genes involved in cell wall modification that are potentially related to phenotypic differences. We confirm that Reute is a P.patens ecotype, and suggest its use for reverse-genetics studies that involve progression through the life cycle and multiple generations.

Building brains that can evolve: Challenges and prospects for evo-devo neurobiology

Evo-devo biology involves cross-species comparisons of entire developmental trajectories, not just of adult forms. This approach has proven very successful in general morphology, but its application to neurobiological problems is still relatively new. To date, the most successful area of evo-devo neurobiology has been the use of comparative developmental data to clarify adult homologies. The most exciting future prospect is the use of comparative developmental data to understand the formation of species differences in adult structure and function. An interesting «model system» for this kind of research is the quest to understand why the neocortex folds in some species but not others.

Gene Expression Data from the Moon Jelly, Aurelia, Provide Insights into the Evolution of the Combinatorial Code Controlling Animal Sense Organ Development.

In Bilateria, Pax6, Six, Eya and Dach families of transcription factors underlie the development and evolution of morphologically and phyletically distinct eyes, including the compound eyes in Drosophila and the camera-type eyes in vertebrates, indicating that bilaterian eyes evolved under the strong influence of ancestral developmental gene regulation. However the conservation in eye developmental genetics deeper in the Eumetazoa, and the origin of the conserved gene regulatory apparatus controlling eye development remain unclear due to limited comparative developmental data from Cnidaria. Here we show in the eye-bearing scyphozoan cnidarian Aurelia that the ectodermal photosensory domain of the developing medusa sensory structure known as the rhopalium expresses sine oculis (so)/six1/2 and eyes absent/eya, but not optix/six3/6 or pax (A&B). In addition, the so and eya co-expression domain encompasses the region of active cell proliferation, neurogenesis, and mechanoreceptor development in rhopalia. Consistent with the role of so and eya in rhopalial development, developmental transcriptome data across Aurelia life cycle stages show upregulation of so and eya, but not optix or pax (A&B), during medusa formation. Moreover, pax6 and dach are absent in the Aurelia genome, and thus are not required for eye development in Aurelia. Our data are consistent with so and eya, but not optix, pax or dach, having conserved functions in sensory structure specification across Eumetazoa. The lability of developmental components including Pax genes relative to so-eya is consistent with a model of sense organ development and evolution that involved the lineage specific modification of a combinatorial code that specifies animal sense organs.

Body plan of turtles: an anatomical, developmental and evolutionary perspective

The evolution of the turtle shell has long been one of the central debates in comparative anatomy. The turtle shell consists of dorsal and ventral parts: the carapace and plastron, respectively. The basic structure of the carapace comprises vertebrae and ribs. The pectoral girdle of turtles sits inside the carapace or the rib cage, in striking contrast to the body plan of other tetrapods. Due to this topological change in the arrangement of skeletal elements, the carapace has been regarded as an example of evolutionary novelty that violates the ancestral body plan of tetrapods. Comparing the spatial relationships of anatomical structures in the embryos of turtles and other amniotes, we have shown that the topology of the musculoskeletal system is largely conserved even in turtles. The positional changes seen in the ribs and pectoral girdle can be ascribed to turtle-specific folding of the lateral body wall in the late developmental stages. Whereas the ribs of other amniotes grow from the axial domain to the lateral body wall, turtle ribs remain arrested axially. Marginal growth of the axial domain in turtle embryos brings the morphologically short ribs in to cover the scapula dorsocaudally. This concentric growth appears to be induced by the margin of the carapace, which involves an ancestral gene expression cascade in a new location. These comparative developmental data allow us to hypothesize the gradual evolution of turtles, which is consistent with the recent finding of a transitional fossil animal, Odontochelys, which did not have the carapace but already possessed the plastron.

Ever Since Owen: Changing Perspectives on the Early Evolution of Tetrapods

The traditional notion of a gap between fishes and amphibians has been closed by a wealth of fish-like fossil tetrapods, many discovered since the mid 1980s. This review summarizes these discoveries and explores their significance relative to changing ideas about early tetrapod phylogeny, biogeography, and ecology. Research emphasis can now shift to broader-based questions, including the whole of the early tetrapod radiation, from the divergence from other lobed-finned fishes to the origins of modern amphibians and amniotes. The fish-to-tetrapod morphological transition occurred within the Upper Devonian; the divergence of modern tetrapod groups is an Early Carboniferous event. Modern tetrapods emerged in the aftermath of one of the five major extinction episodes in the fossil record, but the earlier Devonian tetrapod radiation is not well understood. Tetrapod limbs, paired fins, and comparative developmental data are reviewed; again, research emphasis needs to change to explore the origins of tetrapod diversity.

Growth and Regeneration of the Second Antennae of Asellus Aquaticus (Isopoda) in the Context of Arthropod Antennal Segmentation

The production of new articles in the flagellum of the second antennae of Asellus aquaticus was studied in both undamaged and regenerating antennae. Segmentation is an iterative process in two phases: 1) the first proximal flagellomere (the meristematic article) repeatedly gives off distally a new primary article; 2) each primary article divides into four secondary articles (a quartet). To a certain extent, production and development of different quartets are independent processes. Evidence is provided that the formation of new articles and their setae are partly decoupled. During regeneration from the preferred breakage point (the so-called ‘autotomy plane’), the flagellum is generated by the same mechanism of two-phase segmentation. The regenerated flagellum has a normal segmental composition, except for the tip (the apical complex), which has four flagellomeres rather than the normal five. The similar segmental pattern observed also in other malacostracan crustaceans and in insects, supports a close phylogenetic relationship among the two groups; if the latter proves not to hold, that similarity would provide an example of parallel evolution of developmental mechanism. The difference between ‘true’ articles and annulations, defined on the structure of the muscular system, is discussed on the basis of comparative developmental data. In general, annulations are produced more sequentially, compared with the almost simultaneous emergence of true articles.

Modern insights on gastropod development: Reevaluation of the evolution of a novel body plan

More than a century of speculation about the evolutionary origin of the contorted gastropod body plan has been inspired by adult anatomy and by long-standing developmental observations. The result has been a concept of gastropod torsion that I call the "rotation hypothesis." Under the rotation hypothesis, gastropods originated when all components of the visceropallium (shell, mantle, mantle cavity with contained structures, and viscera) rotated by 180° relative to the head and foot. This evolutionary rotation is echoed during early development of patellogastropods and vetigastropods and occurs to some extent during development of more derived clades. However, comparative developmental data on ontogenetic torsion are minimal and I argue that the rotation hypothesis is a tautological argument. More recent studies on representatives from 3 major clades of gastropods suggest that the highly conserved aspect of gastropod development is not synchronous rotation of all components of the visceropallium relative to the head and foot but rather a state of anatomical organization in which the developing mantle cavity is on the right but the shell coil is posterior (endogastric orientation). This conserved state of developmental anatomy has inspired an alternative hypothesis for the evolutionary origin of the gastropod body plan, the "asymmetry hypothesis." Under the asymmetry hypothesis, the gastropod mantle cavity originated from 1 side only of a bilateral set of mantle cavities. The asymmetry hypothesis does not require a saltation event to explain the origin of gastropods, nor does it require that the ancient molluscan precursor of gastropods carried the shell coil over the head (exogastric orientation).

Confocal imaging of sensory organ formation during Xenopus inner ear development

During Xenopus larval development, the otic vesicle gradually gives rise to several auditory and vestibular sensory organs that are innervated by the eighth cranial nerve. Confocal imaging methods were used to examine the appearance of stereociliary bundles in the various sensory epithelia during Xenopus development (stages 28–50), and to gather comparative developmental data that show how the inner ear gradually forms distinct auditory and vestibular compartments discernable by larval stage 50. A BioRad MRC-1024 confocal microscope was used to collect digitized images from inner ears labeled with Alexa 488 phalloidin to detect the actin cytoskeleton, and propidium iodide to highlight DNA in cell nuclei. Confocal images from whole inner ears clearly show the developmental emergence of uniquely organized sensory epithelia populated by hair cell bundles of varying morphology, as well as the position of the sensory ganglia relative to the endorgans. Images from sectioned tissue provide additional information about cell morphology and the arrangement of the sensory epithelium in relation to neural innervation. Taken together, the image data illustrate the complex structural changes that underlie inner ear organogenesis and morphogenesis. [Work supported by grants to EES (NIH NIGMS, NASA) and awards to QQ (NASA NMSGC Fellowship, NIGMS RISE).]

Molecular strategies in the evolution of mammalian dental patterning

The acquisition of masticatory capability by mammals allowed a better processing of food and a consequent increase in the efficiency of nutrients intake by the digestive system. The development of tooth classes and variations in tooth number can be considered intrinsic characteristics of mammalian dentition. These features allowed species to develop specialized dentitions, creating new adaptive zones. Comparative developmental data from knockout mutant mice and human tooth agenesis present new insights on the molecular strategies that permitted rapid phenotypic differentiation, adaptation and speciation of mammalian dentition.

COMPARATIVE PATTERNS OF CRANIOFACIAL DEVELOPMENT IN EUTHERIAN AND METATHERIAN MAMMALS.

The sequence of differentiation of major elements of the skeletal, muscular and nervous systems of the head is examined in developmental series of five eutherian (placental) and four metatherian (marsupial) mammals. The analysis identifies the elements that are conserved across the Theria, those that are unique to the Metatheria and to the Eutheria, and those that are variable. It is shown that although there are slight shifts in the sequence of development within the somatic tissues of the head, the primary difference between marsupial and placental mammals involves the timing and rate of differentiation of structures of the central nervous system (CNS) relative to a specific subset of structures of the cranial skeleton and musculature. In eutherians, CNS morphogenesis is well underway before the somatic tissues of the head begin differentiation. In metatherians, CNS development is delayed considerably and certain elements of the skeletal and muscular systems are advanced. It is concluded that the developmental differences between marsupial and placental mammals are best explained by the interaction of several processes including neurogenesis as a potential rate-limiting step, the developmental requirements of somatic elements, and the extremely short period of organogenesis of marsupial mammals. Several other issues, including the way that these data may be applied to determine the primitive therian developmental condition, and the use of comparative developmental data to address basic questions on morphogenetic processes, are discussed.

Further Problems in the Interpretation and Homology of the Insect Ovipositor

AbstractAn attempt is made to re-evaluate the data on the origin of the ovipositor in insects and to explain its mode of development in living forms. Comparative developmental data from other groups of animals is cited to substantiate the claim that part of the insect ectodermal genitalia is appendicular rather than sternal in origin. It is suggested that the primary abdominal segmental appendages have provided a source of competent tissue which through subtle changes in selection, has evolved along many pathways, to form the gonocoxae, the pleuropodia, the pseudoplacenta and perhaps the prolegs in many different taxa.It is shown, by aid of sections through the insect embryo and larval stages, that the primary embryonic segmental appendages on the abdomen, do not differentiate; there is no loss of tissue and it cannot be proven that such appendages have been lost in insect phylogeny. The fact that they are represented still in the modern embryo, indicates that they have been retained. To explain the observable developmental details, it is suggested that abdominal limb histogenesis is arrested or suppressed in normal development, but this limb tissue retains its competence to differentiate. Thus development may be initiated again at a later time in postembryonic life. In this manner, the original limb tissue is available for organ formation in the maturing insect.The study has suggested that the appendages on the eighth and ninth segments of the abdomen initiate but do not complete their development in the polypod embryo. Possibly the potential limb tissue is arrested in development because it has not undergone some vital change as regards its capacity to respond (competence) to an inductor, perhaps the inductor is not available or perhaps it is not available in the correct form.There is evidence to suggest that the developmental capacity of the limb anlagen are reduced with time, so that full limb formation is not possible in postembryonic life: this can explain the development of abdominal coxae in the Thysanura and hence gonocoxae in higher insects. It is noted that should Gustafson's suggestion that the eversible sacs and gonapophyses are homologous with primary segmental genitalic ampullae prove acceptable, then the female ectodermal genitalia in insects would appear to have a dual origin.It is emphasized that the speculation expressed are being subjected to experimental study in an attempt to verify the suggested ontogeny and phylogeny.

Metabolic studies on perinatal human brain.

Oxygen consumption and carbon dioxide production were determined on minced samples of cerebral cortex, caudate nucleus, thalamus and medulla oblongata of the brains of 22 human infants ranging in age from 160 to 283 days of gestation. A significant correlation of age and oxygen consumption was obtained for cerebral cortex, caudate nucleus and thalamus. The oxygen consumption of these parts was greater than that of the medulla oblongata after 200 days of gestation age. The results emphasize the impossibility of comparing the brain of the neonatal human being with the young of other species until more comparative developmental data are available. Submitted on April 30, 1959