Echinoderms

Current Biology Vol 15 No 23 R944 restricted diet of either of these two fish. In the wild, kittiwakes have to learn to look for particular colours and patterns in the ocean to find the best place to fish. The researchers tried to recreate this for the captive birds by making them search for their food among a chequerboard of different coloured bowls. Chicks on the unrestricted fatty diet quickly learned which bowls contained food, but chicks on lean rations were very slow learners and never really worked out the colours and patterns associated with the food. “The ability of kittiwakes to associate the colour of a dish with the presence of food decreased proportionally with the magnitude of nutritional stress they had experienced during development,” the team write in the paper in the Proceedings of the Royal Society (published online). A climate shift in the north Pacific and Bering Sea in the mid-1970s resulted in fewer lipid-rich fish around the islands. By the early 1980s redlegged kittiwake populations on the islands had fallen by 50 per cent. “The results of our study suggest that declines in availability of lipid-rich fish — caused by climate change or human-induced — are likely to result in an inferior quality of seabirds in later life and an increased chance of mortality,” the team write. Previous studies have shown that passerine birds such as blackbird and sparrow appear to struggle to learn their mating songs if they do not have a good diet as a chick. A healthy diet looks vital — what is not clear is how much climate change and human interference is likely to impact on the preferred food of seabird populations. Many coastlines could be heading for a collapse in seabird numbers in the face of breeding failure or the fledging of disadvantaged chicks. Quick guide Echinoderms Chris T. Amemiya1,2, Tsutomu Miyake1 and Jonathan P. Rast3 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. Magazine R945 Figure 1. Interrelationships of echinoderms and related taxa. The deuterostomes comprise three phyla: Chordata (vertebrates, cephalochordates and urochordates), Hemichordata and Echinodermata, which are more closely related to each other than to any of the protostome phyla. 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 Current Biology Vol 15 No 23 R946 resources for the sea urchin can be found at http://www.ncbi.nlm.nih.gov/geno me/guide/sea_urchin/ and at http://hgsc.bcm.tmc.edu/projects/ seaurchin/. Where can I find out more? Cameron, C.B., Garey, J.R., and Swalla, B.J. (2000). Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla. Proc. Natl. Acad. Sci. USA 97, 4469–4474. Davidson, E.H., Rast, J.P., Oliveri, P., Ransick, A., Calestani, C., Yuh, C.H., Minokawa, T., Amore, G., Hinman, V., Arenas-Mena, C., et al. (2002). A genomic regulatory network for development. Science 295, 1669–1678. Davidson, E.H., and Cameron, R.A. (2002). Arguments for sequencing the genome of the sea urchin, Strongylocentrotus purpuratus. A white paper submitted to the National Human Genome Research Institute. http://www.genome.gov/Pages/Researc h/Sequencing/SeqProposals/SeaUrchin_Genome.pdf Duboc, V., Rottinger, E., Lapraz, F., Besnardeau, L., and Lepage, T. (2005). Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev. Cell 9, 147–158. Ettensohn, C.A., Wessel, G.M., and Wray, G.A. eds. (2004). Development of sea urchins, ascidians and other invertebrate deuterostomes: Experimental Approaches, Volume 74 (London: Elsevier Academic Press). Hinman, V.F., Nguyen, A.T., Cameron, R.A., and Davidson, E.H. (2003). Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proc. Natl. Acad. Sci. USA 100, 13356–13361. Peterson, K.J., Arenas-Mena, C., and Davidson, E.H. (2000). The A/P axis in echinoderm ontogeny and evolution: evidence from fossils and molecules. Evol. Dev. 2, 93–101. Raff, E.C., Popodi, E.M., Kauffman, J.S., Sly, B.J., Turner, F.R., Morris, V.B., and Raff, R.A. (2003). Regulatory punctuated equilibrium and convergence in the evolution of developmental pathways in direct-developing sea urchins. Evol. Dev. 5, 478–493. Shu, D.-G., Conway Morris, S., Han, J., Zhang, Z.-F., and Liu, J.-N. (2004). Ancestral echinoderms from the Chengjiang deposits of China. Nature 430, 422–428. 1Molecular Genetics Program, Benaroya Research Institute at Virginia Mason, 1201 Ninth Avenue, Seattle, WA 98101, USA. 2Department of Biology, University of Washington, 24 Kincaid Hall, Seattle, Washington 98195, USA. 3Department of Molecular & Cellular Biology, Sunnybrook & Women’s Research Institute and Medical Biophysics, University of Toronto, 2075 Bayview Avenue, Toronto, Ontario M4N 3MS, Canada. Primer Evolution of the avian brain and intelligence Nathan J. Emery and Nicola S. Clayton In Western society, the term ‘bird brain’ is often used as a derogatory term for a person of diminished intellect, partly because many people tend to think of birds as pecking machines, responding reflexively to stimuli in their environment, and partly because birds seem so different from us, with their beady eyes and small heads. But over 40 years ago William Thorpe, who was the leading authority on bird learning at that time, pointed out: “The poor development in birds of any brain structures clearly corresponding to the cerebral cortex of mammals led to the assumption among neurologists not only that birds are primarily creatures of instinct, but also that they are very little endowed with the ability to learn...this misconceived view of brain mechanisms, hindered the development of experimental studies on bird learning”. In the 1960s little was known about the cognitive capacities of birds, but recent studies lend support for Thorpe’s view: we now know that some bird species make and use tools, can count, remember specific past events and reason about the mental states of individuals, behaviours that some have considered to be unique to humans. Despite the apparent cognitive similarity between humans and some birds, neuroscientists have tended to view bird brains as interesting curiosities with little relevance to the workings of the human brain. Recently, however, the Avian Brain Nomenclature Consortium published a series of papers attempting to re-address the issue of the importance of the bird brain to neuroscience by investigating how the avian brain evolved, how the structure of the avian brain relates to that of the mammalian brain, and how names have had a negative influence on how birds are perceived. Negativity surrounding the avian brain began in the late nineteenth century, when Ludwig Edinger provided names for the various parts of the vertebrate brain. His form of nomenclature was based on the naïve view that evolution occurs in a linear progression, so that each new species is an elaboration of an older species. This scala naturae is often represented as a ladder. With respect to intelligence, Arthur Jenson, one of the key figures in studies of human intelligence argued that “single-cell protozoans, such as amoeba, rank at the bottom of the scale, followed in order by the invertebrates, the lower vertebrates, the lower mammals... and finally the primates, in order: New World monkeys, Old World monkeys, the apes, and at the pinnacle, humans”. With respect to brain evolution, Edinger applied this scala naturae suggesting that the brains of living vertebrates retained ancestral structures, but that new brain areas were added onto older ones, or older areas increased in size and complexity to form new areas (Figure 1A). According to this view, evolutionarily older brains are simple, and so produce simple instinctive behaviour, and evolutionarily newer brains are complex, and therefore can control learned and intelligent behaviour. The oldest brain regions — those present in all vertebrates — were prefixed with the term ‘paleo-‘, the next oldest brain regions were given the prefix ‘archi-’, whereas the new brain regions — those present in the species closest to the top of the ‘ladder’ — were assigned the prefix ‘neo-’. We now know that, as with other parts of the body, the brains of distantly related species tend to be derived from the same basic elements found in the common ancestor — they exhibit homology (Figure 1B). So although the common ancestor of birds and mammals lived approximately 300