Echinoderms

Abstract

What are echinoderms? Echinoderms — from the Greek for spiny skin — are invertebrates that exclusively inhabit marine environments. Most species have a five-fold radial body plan. Echinoderms are monophyletic and comprise a sister-group to the hemichordates (acorn worms). There are approximately 7,000 extant echinoderm species which fall into five well-defined taxonomic classes (Figure 1): Crinoidea (sea lilies and feather stars); Asteroidea (starfishes); Ophiuroidea (basket stars and brittle stars); Holothuroidea (sea cucumbers); and Echinoidea (sea urchins, sand dollars, and sea biscuits). This group has left an exceptional fossil record dating back to at least the Cambrian; this well defined fossil record allows comparative molecular studies to be made over a wide range of relatively well documented divergence times. Echinoderms have several shared features that distinguish them from other animals, including a water vascular system and a characteristic form of calcium carbonate endoskeleton called stereom. Most echinoderms begin life as larvae and undergo complex metamorphosis to form an adult. As a group they display a diverse array of life history traits. Most have a sexual mode of reproduction, although some can reproduce asexually. Their larvae are primitively free-living and planktonic, and show a considerable diversity in morphology and function, some of the traits being clearly shared with the larvae of certain hemichordates. Nearly all echinoderm adults adopt a benthic adult form following metamorphosis, though a few deep-water holothuroids are pelagic or epibenthic swimmers. Adult echinoderms are radially symmetrical, usually pentameric, with intricate internal skeletons of calcium carbonate ossicles, supported by a characteristic array of collagenous ligaments. When present in larvae, skeletons take the form of elaborate rods which are independently derived in Ophiuroidea and Echinoidea (and absent in larvae of the other three echinoderm classes). What is their history as experimental models? Echinoderm embryos and larvae have been used as experimental model systems for more than a century. Research on echinoderms has led to significant advances in the areas of developmental biology, cell biology and immunology, several specific lines of research being recognized with Nobel Prizes. Echinoderm larvae were central to classic studies that resulted in fundamental biological concepts including Hans Driesch’s demonstration of nuclear equivalence in development, Theodor Boveri’s characterization of the chromosomal basis of inheritance, and Elie Metchnikoff’s exploration of cellular immunity. How do echinoderms develop? Echinoderm species exhibit a variety of developmental strategies, from maximally indirect development, where adults emerge from metamorphosis of a larva with virtually no similarity to the adult, to direct developmental transition from a fertilized egg into an adult. The bilaterally symmetrical larvae of indirect developing species are feeding, long-lived and very simple in structure and cell number (in the most-used sea urchin models the pluteus larva has only about 2000 cells). A variety of intermediate developmental modes exist with, for example, non-feeding larvae or facultative larval feeding. For echinoderms indirect development is primitive, and a dipleurula-type larva is found in all five living classes, as well as in the sister-phylum Hemichordata. Are echinoderms really considered bilaterians? Yes. While adult echinoderms are radially symmetric (usually pentameric, but sometimes with higher-order symmetry), phylogenetic analysis unequivocally shows this state is derived from a bilaterian ancestor. Analyses of hox gene expression and fossil evidence indicate that the anterior–posterior axis of echinoderms runs along the axis of the gut. Echinoderm larvae exhibit bilateral symmetry, with the first ontogenetic signs of a pentameric form appearing in the adult anlage (rudiment) in the advanced larva. Extinct Paleozoic forms with bilateral adult body architecture are known from fossils. Which echinoderms are used as models? Nearly all of the molecular biology research and most of the classical embryology studies have been done using the embryos and larvae of a few species of indirectly developing sea urchins. Some work has been done also with starfish embryos. Congenic pairs of sea urchin species, one exhibiting direct and the other indirect development, have been used to investigate the developmental basis for changes in life history strategies. Why are echinoderm embryos used for developmental studies? From embryological and molecular perspectives, they offer advantages over other deuterostome models. Sea urchins produce enormous quantities of eggs, which are fertilized in sea water and develop as simple, optically clear, free-living embryos. They can be grown as staged cultures (by the millions and, if necessary, billions) and provide large quantities of materials for biochemical or molecular biology analyses. They are easy to maintain and their development can be conveniently manipulated at the cellular and molecular levels. Importantly the embryos form feeding larvae that provide an exceptionally simple deuterostome model with the basic attributes of any animal. Why are they used for gene regulatory network analysis? The studies of gene regulatory networks aim to map and understand the transcriptional circuitry of developmental programs. This requires accurate measurement of mRNA prevalence, efficient cis-regulatory analysis, and specific perturbation of regulatory interactions in order to create a predictive network model, which can then be tested by further perturbations and measurements. Most of these analyses must be made in a genuine developmental context, and sea urchin embryos are convenient for each of these steps. They are relatively simple in morphology and developmental mechanism. Thousands of transgenic embryos can be routinely generated in a single injection session. Perturbation agents, such as morpholino antisense oligonucleotides, mRNAs and interfering mutated expression constructs, can be easily injected and outcomes analyzed. These molecular perturbations can be combined with experimental manipulation and transplantation techniques developed over more than a century of embryological research using echinoderms. Further information on gene networks in the sea urchin can be found at http://sugp.caltech.edu/endomes/ How does their development relate to that of more complex vertebrates? Despite their simplicity, sea urchin embryos and larvae use homologs of many of the same transcription factors employed by more complex bilaterians, some specific to the deuterostomes. Co-expression of many of these factors in the specification of mesoderm, endoderm and ectoderm, and later in cell type differentiation and function, suggests conservation at the wider gene network level. This has been tested in one case where conservation of interactions that specify endomesoderm in sea urchin has been demonstrated in a starfish, which shares a common ancestor with the sea urchins that existed at least 500 million years ago. The simplicity of these echinoderm systems can be exploited to characterize similar network interactions that are conserved within vertebrates. Is there an echinoderm genome project? Yes, the genome of the purple sea urchin, Strongylocentrotus purpuratus, is being sequenced at the Baylor College of Medicine Human Genome Sequencing Center under the auspices of the National Human Genome Research Institute. A compilation of genome resources for the sea urchin can be found at http://www.ncbi.nlm.nih.gov/genome/guide/sea_urchin/ and at http://hgsc.bcm.tmc.edu/projects/seaurchin/.