Ecological Developmental Biology: Developmental Biology Meets the Real World1

The production of phenotype is regulated by differential gene expression. However, the regulators of gene expression need not all reside within the embryo. Environmental factors, such as temperature, photoperiod, diet, population density, or the presence of predators, can produce specific phenotypes, presumably by altering gene-expression patterns. The field of ecological developmental biology seeks to look at development in the real world of predators, competitors, and changing seasons. Ecological concerns had played a major role in the formation of experimental embryology, and they are returning as the need for knowledge about the effects of environmental change on embryos and larvae becomes crucial. This essay reviews some of the areas of ecological developmental biology, concentrating on new studies of Amphibia and Homo.     

Embryogenomics: developmental biology meets genomics

Fundamental questions in developmental biology are: what genes are expressed, where and when they are expressed, what is the level of expression and how are these programs changed by the functional and structural alteration of genes? These questions have been addressed by studying one gene at a time, but a new research field that handles many genes in parallel is emerging. The methodology is at the interface of large-scale genomics approaches and developmental biology. Genomics needs developmental biology because one of the goals of genomics – collection and analysis of all genes in an organism – cannot be completed without working on embryonic tissues in which many genes are uniquely expressed. However, developmental biology needs genomics – the high-throughput approaches of genomics generate information about genes and pathways that can give an integrated view of complex processes. This article discusses these new approaches and their applications to mammalian developmental biology.     

The morphogenesis of evolutionary developmental biology

The early studies of evolutionary developmental biology (Evo-Devo) come from several sources. Tributaries flowing into Evo-Devo came from such disciplines as embryology, developmental genetics, evolutionary biology, ecology, paleontology, systematics, medical embryology and mathematical modeling. This essay will trace one of the major pathways, that from evolutionary embryology to Evo-Devo and it will show the interactions of this pathway with two other sources of Evo-Devo: ecological developmental biology and medical developmental biology. Together, these three fields are forming a more inclusive evolutionary developmental biology that is revitalizing and providing answers to old and important questions involving the formation of biodiversity on Earth. The phenotype of Evo-Devo is limited by internal constraints on what could be known given the methods and equipment of the time and it has been framed by external factors that include both academic and global politics.     

Chemical genetics: adding to the developmental biology toolbox

Recent advances in cell and molecular biology have generated important tools to probe developmental questions. In addition, new genetic model systems such as Danio rerio now make large-scale vertebrate early developmental mutant screens feasible. Nonetheless, some developmental questions remain difficult to study because of the need for finer temporal, spatial, or tuneable control of gene function within a developmental system. New uses for old teratogens as well as novel chemical modulators of development have begun to fill this void.     

Functional evolutionary developmental biology (evo-devo) of morphological novelties in plants

The origin of morphological and ecological novelties is a long-standing problem in evolutionary biology.Understanding these processes requires investigation from both the development and evolution standpoints,which promotes a new research field called evolutionary developmental biology (evo-devo).The fundamental mechanism for the origin of a novel structure may involve heterotopy,heterochrony,ectopic expression,or loss of an existing regulatory factor.Accordingly,the morphological and ecological traits cont...     

Four decades of teaching developmental biology in Germany

I have taught developmental biology in Essen for 30 years. Since my department is named Zoophysiologie (Zoophysiology), besides Developmental Biology, I also have to teach General Animal Physiology. This explains why the time for teaching developmental biology is restricted to a lecture course, a laboratory course and several seminar courses. However, I also try to demonstrate in the lecture courses on General Physiology the close relationship between developmental biology, physiology, morphology, anatomy, teratology, carcinogenesis, evolution and ecology (importance of environmental factors on embryogenesis). Students are informed that developmental biology is a core discipline of biology. In the last decade, knowledge about molecular mechanisms in different organisms has exponentially increased. The students are trained to understand the close relationship between conserved gene structure, gene function and signaling pathways, in addition to or as an extension of, classical concepts. Public reports about the human genome project and stem cell research (especially therapeutic and reproductive cloning) have shown that developmental biology, both in traditional view and at the molecular level, is essential for the understanding of these complex topics and for serious and non-emotional debate.     

Evolutionary developmental biology its roots and characteristics

The rise of evolutionary developmental biology was not the progressive isolation and characterization of developmental genes and gene networks. Many obstacles had to be overcome: the idea that all genes were more or less involved in development; the evidence that developmental processes in insects had nothing in common with those of vertebrates.Different lines of research converged toward the creation of evolutionary developmental biology, giving this field of research its present heterogeneity. This does not prevent all those working in the field from sharing the conviction that a precise characterization of evolutionary variations is required to fully understand the evolutionary process.Some evolutionary developmental biologists directly challenge the Modern Synthesis. I propose some ways to reconcile these apparently opposed visions of evolution. The turbulence seen in evolutionary developmental biology reflects the present entry of history into biology.     

Educating for social responsibility: changing the syllabus of developmental biology

Developmental biology is deeply embedded in the social issues of our times. Such topics as cloning, stems cells, reproductive technologies, sex selection, environmental hormone mimics and gene therapy all converge on developmental biology. It is therefore critical that developmental biologists learn about the possible social consequences of their work and of the possible molding of their discipline by social forces. We present two models for integrating social issues into the developmental biology curriculum. One model seeks to place discussions of social issues into the laboratory portion of the curriculum; the other model seeks to restructure the course, such that developmental biology and its social contexts are synthesized directly.     

Student-oriented learning: an inquiry-based developmental biology lecture course

In this junior-level undergraduate course, developmental life cycles exhibited by various organisms are reviewed, with special attention--where relevant--to the human embryo. Morphological features and processes are described and recent insights into the molecular biology of gene expression are discussed. Ways are studied in which model systems, including marine invertebrates, amphibia, fruit flies and other laboratory species are employed to elucidate general principles which apply to fertilization, cleavage, gastrulation and organogenesis. Special attention is given to insights into those topics which will soon be researched with data from the Human Genome Project. The learning experience is divided into three parts: Part I is a in which the Socratic (inquiry) method is employed by the instructor (GMM) to organize a review of classical developmental phenomena; Part II represents an in which students study the details related to the surveys included in Part I as they have been reported in research journals; Part III focuses on a class project--the preparation of a spiral bound on a topic of relevance to human developmental biology (e.g.,Textbook of Embryonal Stem Cells). Student response to the use of the Socratic method increases as the course progresses and represents the most successful aspect of the course.     

Comparative methods in developmental biology

The need for a phylogenetic framework is becoming appreciated in many areas of biology. Such a framework has found limited use in developmental studies. Our current research program is therefore directed to applying comparative and phylogenetic methods to developmental data. In this paper, we examine the concepts underlying this work, discuss potential difficulties, and identify some solutions. While developmental biologists frequently make cross-species comparisons, they usually adopt a phenetic approach, whereby degrees of overall similarity in development are sought. Little emphasis is placed on reconstructing the evolutionary divergence in developmental characters. Indeed, developmental biologists have historically concentrated on apparently ‘conserved’ or ‘universal’ developmental mechanisms. Thus, there has been little need for phylogenetic methodologies which analyse specialised features shared only within a subset of species (i.e., synapomorphies). We discuss the potential value of such methodologies, and argue that difficulties in adapting them to developmental studies fall into three interlinked areas: One concerns the nature and definition of developmental characters. Another is the difficulty of identifying equivalent developmental stages in different species. Finally the phylogenetic non-independence of developmental characters presents real problems under some protocols. These problems are not resolved. However, it is clear that the application of phylogenetic methodology to developmental data is both necessary and fundamental to research into the relationship between evolution and development.     

How developmental is evolutionary developmental biology?

Evolutionary developmental biology (evo-devo) offers both an account of developmental processes and also new integrative frameworks for analyzing interactions between development and evolution. Biologists and philosophers are keen on evo-devo in part because it appears to offer a comfort zone between, on the one hand, what some take to be the relative inability of mainstream evolutionary biology to integrate a developmental perspective; and, on the other hand, what some take to be more intractable syntheses of development and evolution. In this article, I outline core concerns of evo-devo, distinguish theoretical and practical variants, and counter Sterelny's recent argument that evo-devo's attention to development, while important, offers no significant challenge to evolutionary theory as we know it. This revised version was published online in July 2006 with corrections to the Cover Date.     

Beyond Arabidopsis. Translational biology meets evolutionary developmental biology

Developmental processes shape plant morphologies, which constitute important adaptive traits selected for during evolution. Identifying the genes that act in developmental pathways and determining how they are modified during evolution is the focus of the field of evolutionary developmental biology, or evo-devo. Knowledge of genetic pathways in the plant model Arabidopsis serves as the starting point for investigating how the toolkit of developmental pathways has been used and reused to form different plant body plans. One productive approach is to identify genes in other species that are orthologous to genes known to control developmental pathways in Arabidopsis and then determine what changes have occurred in the protein coding sequence or in the gene's expression to produce an altered morphology. A second approach relies on natural variation among wild populations or crop plants. Natural variation can be exploited to identify quantitative trait loci that underlie important developmental traits and, thus, define those genes that are responsible for adaptive changes. The possibility of applying comparative genomics approaches to Arabidopsis and related species promises profound new insights into the interplay of evolution and development.     

Mouse models and the evolutionary developmental biology of the skull

Understanding development is relevant to understanding evolutionbecause developmental processes structure the expression ofphenotypic variation upon which natural selection acts. Advancesin developmental biology are fueling a new synthesis of developmentaland evolutionary biology, but it remains unclear how to usedevelopmental information that largely derives from a few modelorganisms to test hypotheses about the evolutionary developmentalbiology of taxa such as humans and other primates that havenot been or are not amenable to direct study through experimentaldevelopmental biology. In this article, we discuss how and whenmodel organisms like mice are useful for studying the evolutionarydevelopmental biology of even rather distantly related and morphologicallydifferent groups like primates. A productive approach is tofocus on processes that are likely to play key roles in producingevolutionarily significant phenotypic variation across a largephylogenetic range. We illustrate this approach by applyingthe analysis of craniofacial variation in mouse mutant modelsto primate and human evolution.     

Study of developmental homeostasis: From population developmental biology and the health of environment concept to the sustainable development concept

The study of the indices of developmental homeostasis in natural populations leads to the definition of the fundamentals of population developmental biology, which is associated with the assessment of the nature of phenotypic diversity and the mechanisms of population dynamics and microevolutionary changes. Characterization of environmental quality based on the assessment of population status by developmental homeostasis determines the fundamentals of the health of environment concept. The use of the ideas of developmental homeostasis and the health of environment in the studies of homeostatic mechanisms of biological systems of different levels (from the organism and population to the community and ecosystem) is promising. This gives new opportunities for understanding the mechanisms that provide sustainability and their ratio at different levels as well as for the characterization of ontogenetic stability significance. The notion of developmental homeostasis, or homeorhesis, is promising for the elaboration of the ecological and biological basics of sustainable development.     

Ecological developmental biology: environmental signals for normal animal development

The environment plays instructive roles in development and selective roles in evolution. This essay reviews several of the instructive roles whereby the organism has evolved to receive cues from the environment in order to modulate its developmental trajectory. The environmental cues can be abiotic (such as temperature or photoperiod) or biotic (such as those emanating from predators, conspecifics, or food), and the “alteration” produces a normal, not a pathological, phenotype, that is appropriate for the environment. In addition, symbiotic organisms can produce important signals during normal development. Environmental cues can be obligatory, such that the organism cannot develop without the environmental cue. These cues often permit and instruct the organism to proceed from one developmental stage to another, as when larvae receive cues to settle and undergo metamorphosis from substrates. Such obligatory cues can also be given by symbionts, as when Wolbachia bacteria prevent apoptosis in developing ovaries of some wasps. Other environmental cues can be used facultatively, allowing organisms to follow different developmental trajectories depending on whether the cue is present or not. This can be seen in the temperature‐dependent determination of sex in many reptiles and in the determination of thermotolerance in aphids by their symbiotic bacteria. Signaling from the environment is essential in development, and co‐development appears to be normative between symbionts and their hosts. Here, one sees the reciprocal induction of gene expression, just as within the embryonic organism. The ability of organisms to respond to environmental cues by producing different phenotypes may be critically important in evolution, and it may be an essential feature that can facilitate or limit evolution.     

The interface between cell and developmental biology

Cell differentiation, morphology, migration, polarity, intercellular communication and adhesion are all cellular processes that control embryo morphogenesis and lie at the interface of cell and developmental biology. The interface between these two fields is best illustrated, however, in studies of axiation and cytoskeletal remodeling during development. Recent advances reveal novel mechanisms for axiation, including the role of RNA and protein degradation in regulating the timely expression of morphogenetic signals. Significant progress has also been made in identifying components of the cytoskeleton and the extracellular matrix that mediate embryonic cell migration and polarity. Cellular processes at the interface of cell and developmental biology are overseen by the Wnt signaling cascade that coordinates both axiation and cytoskeletal remodeling during development.     

Evolutionary developmental biology and the problem of variation

Abstract. One of the oldest problems in evolutionary biology remains largely unsolved. Which mutations generate evolutionarily relevant phenotypic variation? What kinds of molecular changes do they entail? What are the phenotypic magnitudes, frequencies of origin, and pleiotropic effects of such mutations? How is the genome constructed to allow the observed abundance of phenotypic diversity? Historically, the neo‐Darwinian synthesizers stressed the predominance of micromutations in evolution, whereas others noted the similarities between some dramatic mutations and evolutionary transitions to argue for macromutationism. Arguments on both sides have been biased by misconceptions of the developmental effects of mutations. For example, the traditional view that mutations of important developmental genes always have large pleiotropic effects can now be seen to be a conclusion drawn from observations of a small class of mutations with dramatic effects. It is possible that some mutations, for example, those in cis‐regulatory DNA, have few or no pleiotropic effects and may be the predominant source of morphological evolution. In contrast, mutations causing dramatic phenotypic effects, although superficially similar to hypothesized evolutionary transitions, are unlikely to fairly represent the true path of evolution. Recent developmental studies of gene function provide a new way of conceptualizing and studying variation that contrasts with the traditional genetic view that was incorporated into neo‐Darwinian theory and population genetics. This new approach in developmental biology is as important for micro‐evolutionary studies as the actual results from recent evolutionary developmental studies. In particular, this approach will assist in the task of identifying the specific mutations generating phenotypic variation and elucidating how they alter gene function. These data will provide the current missing link between molecular and phenotypic variation in natural populations.     

Principles of developmental biology

The field of developmental biology has a history that spans the last 500 years. Within the last 10 years, our understanding of developmental mechanisms has grown exponentially by employing modern techniques of genetics and molecular biology, frequently combined with experimental embryology and the use of molecular markers, rather than solely morphology, to identify critical populations of cells and their state of differentiation. Three main principles have emerged. First, mechanisms of development are highly conserved, both among developing rudiments of a variety of organ systems and among diverse organisms. This conservation occurs both at the level of tissue and cellular mechanisms, and at the molecular level. Second, the development of organ rudiments is influenced by surrounding tissues through interactions called inductive interactions. Such interactions are mediated by highly conserved growth factors and signaling systems. Third, development is a life-long process and can be reawakened in events such as wound healing and regeneration, and in certain diseases. Advances in understanding normal development provide hope that diseases in which development runs amuck, such as cancer, may soon be preventable and fully treatable. Supported by NS 18112 and DC 04185 from the NIH.     

The role of textbooks in communicating developmental biology

Writing a textbook that synthesized the field from the perspectives of embryology, genetics, cell biology and molecular biology was a challenge. Because this field evolves so rapidly, a textbook can only lay the basic foundation for understanding new information and provide the framework that helps scholars place new information into context throughout their career. In this essay, I propose that an international college of specialists be established to provide authoritative online updates on developmental biology topics as a service to students and the professional developmental biology community.