The bilaterian forebrain: an evolutionary chimaera.
Tosches, M.A. & Arendt, D.
Curr Opin Neurobiol. 2013 Dec;23(6):1080-9. doi: 10.1016/j.conb.2013.09.005. Epub2013 Sep 27.
The insect, annelid and vertebrate forebrains harbour two major centres of output control, a sensory-neurosecretory centre releasing hormones and a primordial locomotor centre that controls the initiation of muscular body movements. In vertebrates, both reside in the hypothalamus. Here, we review recent comparative neurodevelopmental evidence indicating that these centres evolved from separate condensations of neurons on opposite body sides ('apical nervous system' versus 'blastoporal nervous system') and that their developmental specification involved distinct regulatory networks (apical six3 and rx versus mediolateral nk and pax gene-dependent patterning). In bilaterian ancestors, both systems approached each other and became closely intermingled, physically, functionally and developmentally. Our 'chimeric brain hypothesis' sheds new light on the vast success and rapid diversification of bilaterian animals in the Cambrian and revises our understanding of brain architecture.
Evolution of clitellate phaosomes from rhabdomeric photoreceptor cells of polychaetes - a study in the leech Helobdella robusta (Annelida, Sedentaria, Clitellata).
Doring, C., Gosda, J., Tessmar-Raible, K., Hausen, H., Arendt, D. & Purschke, G.
Front Zool. 2013 Sep 5;10(1):52. doi: 10.1186/1742-9994-10-52.
INTRODUCTION: In Annelida two types of photoreceptor cells (PRCs) are regarded as generally present, rhabdomeric and ciliary PRCs. In certain taxa, however, an additional type of PRC may occur, the so called phaosomal PRC. Whereas the former two types of PRCs are always organized as an epithelium with their sensory processes projecting into an extracellular cavity formed by the PRCs and (pigmented) supportive cells, phaosomes are seemingly intracellular vacuoles housing the sensory processes. Phaosomal PRCs are the only type of PRC found in one major annelid group, Clitellata. Several hypotheses have been put forward explaining the evolutionary origin of the clitellate phaosomes. To elucidate the evolution of clitellate PRC and eyes the leech Helobdella robusta, for which a sequenced genome is available, was chosen. RESULTS: TEM observations showed that extraocular and ocular PRCs are structurally identical. Bioinformatic analyses revealed predictions for four opsin genes, three of which could be amplified. All belong to the rhabdomeric opsin family and phylogenetic analyses showed them in a derived position within annelid opsins. Gene expression studies showed two of them expressed in the eye and in the extraocular PRCs. Polychaete eye-typic key enzymes for ommochromme and pterin shading pigments synthesis are not expressed in leech eyes. CONCLUSIONS: By comparative gene-expression studies we herein provide strong evidence that the phaosomal PRCs typical of Clitellata are derived from the rhabdomeric PRCs characteristic for polychaete adult eyes. Thus, they represent a highly derived type of PRC that evolved in the stem lineage of Clitellata rather than another, primitive type of PRC in Metazoa. Evolution of these PRCs in Clitellata is related to a loss of the primary eyes and most of their photoreceptive elements except for the rhabdomeric PRCs. Most likely this happened while changing to an endobenthic mode of life. This hypothesis of PRC evolution is in accordance with a recently published phylogeny of Annelida based on phylogenomic data. The data provide a nice example how morphologically highly divergent light sensitive structures emerged from a standard type of photoreceptor cell.
Linking micro- and macro-evolution at the cell type level: a view from the lophotrochozoan Platynereis dumerilii.
Simakov, O., Larsson, T.A. & Arendt, D.
Brief Funct Genomics. 2013 Sep;12(5):430-9. doi: 10.1093/bfgp/els049. Epub 2012Nov 20.
Ever since the origin of the first metazoans over 600 million years ago, cell type diversification has been driven by micro-evolutionary processes at population level, leading to macro-evolution changes above species level. In this review, we introduce the marine annelid Platynereis dumerilii, a member of the lophotrochozoan clade (a key yet most understudied superphylum of bilaterians), as a suitable model system for the simultaneous study, at cellular resolution, of macro-evolutionary processes across phyla and of micro-evolutionary processes across highly polymorphic populations collected worldwide. Recent advances in molecular and experimental techniques, easy maintenance and breeding, and the fast, synchronous and stereotypical development have facilitated the establishment of Platynereis as one of the leading model species in the eco-evo-devo field. Most importantly, Platynereis allows the combination of expression profiling, morphological and physiological characterization at the single cell level. Here, we discuss recent advances in the collection of -omics data for the lab strain and for natural populations collected world-wide that can be integrated with population-specific cellular analyses to result in a cellular atlas integrating genetic, phenotypic and ecological variation. This makes Platynereis a tractable system to begin understanding the interplay between macro- and micro-evolutionary processes and cell type diversity.
Methods for generating year-round access to amphioxus in the laboratory.
Benito-Gutierrez, E., Weber, H., Bryant, D.V. & Arendt, D.
PLoS One. 2013 Aug 26;8(8):e71599. doi: 10.1371/journal.pone.0071599.
Cephalochordates, commonly known as amphioxus, are key to understanding vertebrate origins. However, laboratory work suffers from limited access to adults and embryonic material. Here we report the design and experimental validation of an inland marine facility that allows establishing stable amphioxus colonies in the laboratory and obtaining embryos at any time of day and over almost the entire year, far exceeding natural conditions. This is achieved by mimicking the natural benthic environment, natural day- and moon- light, natural substrate and by providing a strictly controlled and seasonally fluctuating temperature regimen. Moreover, supplemented algae diets allow animals to refill their gonads in consecutive years. Spontaneous spawning, a major problem in previous setups, no longer occurs in our facility; instead, all breeding is induced and fertilization occurs fully in vitro. Our system makes amphioxus a standard laboratory animal model.
Somatic and visceral nervous systems - an ancient duality.
Bertucci, P. & Arendt, D.
BMC Biol. 2013 Apr 30;11(1):54. doi: 10.1186/1741-7007-11-54.
The vertebrate nervous system is deeply divided into 'somatic' and 'visceral' subsystems that respond to external and internal stimuli, respectively. Molecular characterization of neurons in different groups of mollusks by Nomaksteinsky and colleagues, published in this issue of BMC Biology, reveals that the viscero-somatic duality is evolutionarily ancient, predating Bilateria.See research article: http://www.biomedcentral.com/1741-7007/11/53.
Mesoteloblast-Like Mesodermal Stem Cells in the Polychaete Annelid Platynereis dumerilii (Nereididae).
Fischer, A.H. & Arendt, D.
J Exp Zool B Mol Dev Evol. 2013 Mar;320(2):94-104. doi: 10.1002/jez.b.22486. Epub2013 Feb 13.
Spiral cleavage is observed in animals that belong to the lophotrochozoa, a large group of marine invertebrates. As characteristic for spiral cleavage, the bulk of mesoderm forms from one cell, the "4d blastomere." This process has not yet been followed in cellular detail in annelids except in the leech, where "mesoteloblasts," a pair of mesodermal stem cells, generate two bands of mesoderm precursor cells in an iterative fashion. It is so far unknown whether such stem cell-like lineage is a general property of 4d-derived mesoderm in spiralian larvae. To address this, we have analyzed the cell lineage of the 4d blastomere in the polychaete annelid Platynereis dumerilii, an emerging model for lophotrochozoan and spiralian embryology (Fischer et al., 2010), by 4D microscopy, a semi-automated cell tracking technique based on differential interference contrast serial imaging (Schnabel et al. '97). Our data reveal that the two daughter cells of the 4d cell undergo seven consecutive rounds of unequal cell divisions. They bud off smaller cells in ventral-vegetal orientation and thus show mesoteloblast- and stem cell-like behavior. Based on these findings, we suggest that mesoteloblast-like mesodermal stem cells that form continuous mesodermal bands are part of the Errantia + Sedentaria ground pattern. In the course of annelid evolution, the number consecutive divisions of these cells would have been low initially with <10 division cycles, giving rise to larval segments only, and then increased up to 35 as observed in clitellates. J. Exp. Zool. (Mol. Dev. Evol.) 320B:94-104, 2013. (c) 2013 Wiley Periodicals, Inc.
Molecular analysis of the amphioxus frontal eye unravels the evolutionary origin of the retina and pigment cells of the vertebrate eye.
Vopalensky, P., Pergner, J., Liegertova, M., Benito-Gutierrez, E., Arendt, D. & Kozmik, Z.
Proc Natl Acad Sci U S A. 2012 Sep 18;109(38):15383-8. Epub 2012 Sep 4.
The origin of vertebrate eyes is still enigmatic. The "frontal eye" of amphioxus, our most primitive chordate relative, has long been recognized as a candidate precursor to the vertebrate eyes. However, the amphioxus frontal eye is composed of simple ciliated cells, unlike vertebrate rods and cones, which display more elaborate, surface-extended cilia. So far, the only evidence that the frontal eye indeed might be sensitive to light has been the presence of a ciliated putative sensory cell in the close vicinity of dark pigment cells. We set out to characterize the cell types of the amphioxus frontal eye molecularly, to test their possible relatedness to the cell types of vertebrate eyes. We show that the cells of the frontal eye specifically coexpress a combination of transcription factors and opsins typical of the vertebrate eye photoreceptors and an inhibitory Gi-type alpha subunit of the G protein, indicating an off-responding phototransductory cascade. Furthermore, the pigmented cells match the retinal pigmented epithelium in melanin content and regulatory signature. Finally, we reveal axonal projections of the frontal eye that resemble the basic photosensory-motor circuit of the vertebrate forebrain. These results support homology of the amphioxus frontal eye and the vertebrate eyes and yield insights into their evolutionary origin.
Extensive chordate and annelid macrosynteny reveals ancestral homeobox gene organization.
Hui, J.H., McDougall, C., Monteiro, A.S., Holland, P.W., Arendt, D., Balavoine, G. & Ferrier, D.E.
Mol Biol Evol. 2012 Jan;29(1):157-65. doi: 10.1093/molbev/msr175. Epub 2011 Jul4.
Genes with the homeobox motif are crucial in developmental biology and widely implicated in the evolution of development. The Antennapedia (ANTP)-class is one of the two major classes of animal homeobox genes, and includes the Hox genes, renowned for their role in patterning the anterior-posterior axis of animals. The origin and evolution of the ANTP-class genes are a matter of some debate. A principal guiding hypothesis has been the existence of an ancient gene Mega-cluster deep in animal ancestry. This hypothesis was largely established from linkage data from chordates, and the Mega-cluster hypothesis remains to be seriously tested in protostomes. We have thus mapped ANTP-class homeobox genes to the chromosome level in a lophotrochozoan protostome. Our comparison of gene organization in Platynereis dumerilii and chordates indicates that the Mega-cluster, if it did exist, had already been broken up onto four chromosomes by the time of the protostome-deuterostome ancestor (PDA). These results not only elucidate an aspect of the genome organization of the PDA but also reveal high levels of macrosynteny between P. dumerilii and chordates. This implies a very low rate of interchromosomal genome rearrangement in the lineages leading to P. dumerilii and the chordate ancestor since the time of the PDA.
A holistic approach to marine eco-systems biology.
Karsenti, E., Acinas, S.G., Bork, P., Bowler, C., De Vargas, C., Raes, J., Sullivan, M., Arendt, D., Benzoni, F., Claverie, J.M., Follows, M., Gorsky, G., Hingamp, P., Iudicone, D., Jaillon, O., Kandels-Lewis, S., Krzic, U., Not, F., Ogata, H., Pesant, S., Reynaud, E.G., Sardet, C., Sieracki, M.E., Speich, S., Velayoudon, D., Weissenbach, J. & Wincker, P.
PLoS Biol. 2011 Oct;9(10):e1001177. doi: 10.1371/journal.pbio.1001177. Epub 2011Oct 18.
The structure, robustness, and dynamics of ocean plankton ecosystems remain poorly understood due to sampling, analysis, and computational limitations. The Tara Oceans consortium organizes expeditions to help fill this gap at the global level.
The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii.
Steinmetz, P.R., Kostyuchenko, R.P., Fischer, A. & Arendt, D.
Evol Dev. 2011 Jan-Feb;13(1):72-9. doi: 10.1111/j.1525-142X.2010.00457.x.
SUMMARY Annelids and arthropods, despite their distinct classification as Lophotrochozoa and Ecdysozoa, present a morphologically similar, segmented body plan. To elucidate the evolution of segmentation and, ultimately, to align segments across remote phyla, we undertook a refined expression analysis to precisely register the expression of conserved regionalization genes with morphological boundaries and segmental units in the marine annelid Platynereis dumerilii. We find that Pdu-otx defines a brain region anterior to the first discernable segmental entity that is delineated by a stripe of engrailed-expressing cells. The first segment is a "cryptic" segment that lacks chaetae and parapodia. This and the subsequent three chaetigerous larval segments harbor the anterior expression boundary of gbx, hox1, hox4, and lox5 genes, respectively. This molecular segmental topography matches the segmental pattern of otx, gbx, and Hox gene expression in arthropods. Our data thus support the view that an ancestral ground pattern of segmental identities existed in the trunk of the last common protostome ancestor that was lost or modified in protostomes lacking overt segmentation.
Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium.
Tomer, R., Denes, A.S., Tessmar-Raible, K. & Arendt, D.
Cell. 2010 Sep 3;142(5):800-9.
The evolution of the highest-order human brain center, the "pallium" or "cortex," remains enigmatic. To elucidate its origins, we set out to identify related brain parts in phylogenetically distant animals, to then unravel common aspects in cellular composition and molecular architecture. Here, we compare vertebrate pallium development to that of the mushroom bodies, sensory-associative brain centers, in an annelid. Using a newly developed protocol for cellular profiling by image registration (PrImR), we obtain a high-resolution gene expression map for the developing annelid brain. Comparison to the vertebrate pallium reveals that the annelid mushroom bodies develop from similar molecular coordinates within a conserved overall molecular brain topology and that their development involves conserved patterning mechanisms and produces conserved neuron types that existed already in the protostome-deuterostome ancestors. These data indicate deep homology of pallium and mushroom bodies and date back the origin of higher brain centers to prebilaterian times.
Hedgehog signaling regulates segment formation in the annelid Platynereis.
Dray, N., Tessmar-Raible, K., Le Gouar, M., Vibert, L., Christodoulou, F., Schipany, K., Guillou, A., Zantke, J., Snyman, H., Behague, J., Vervoort, M., Arendt, D. & Balavoine, G.
Science. 2010 Jul 16;329(5989):339-42.
Annelids and arthropods share a similar segmented organization of the body whose evolutionary origin remains unclear. The Hedgehog signaling pathway, prominent in arthropod embryonic segment patterning, has not been shown to have a similar function outside arthropods. We show that the ligand Hedgehog, the receptor Patched, and the transcription factor Gli are all expressed in striped patterns before the morphological appearance of segments in the annelid Platynereis dumerilii. Treatments with small molecules antagonistic to Hedgehog signaling disrupt segment formation. Platynereis Hedgehog is not necessary to establish early segment patterns but is required to maintain them. The molecular similarity of segment patterning functions of the Hedgehog pathway in an annelid and in arthropods supports a common origin of segmentation in protostomes.
Three consecutive generations of nephridia occur during development of Platynereis dumerilii (Annelida, Polychaeta).
Hasse, C., Rebscher, N., Reiher, W., Sobjinski, K., Moerschel, E., Beck, L., Tessmar-Raible, K., Arendt, D. & Hassel, M.
Dev Dyn. 2010Jul;239(7):1967-76.
Molecular data for nephridial development in polychaetes are not available yet. The scope of our work was to establish a reference system for future investigations using two markers for nephridial development: beta-tubulin as marker for cilia and alkaline phosphatase (AP) activity for secretory epithelia. The markers identified, unexpectedly, three consecutively forming generations of nephridia: (1) a transitory unciliated, but AP-positive head kidney, (2) a transitory larval nephridium, which undergoes a morphological transition from a protonephridium to a funnelled nephridium concomitant with the development of the coelomic cavity and finally, (3) the serially arranged metanephridia. The spatial arrangement of larval and definitive nephridia, revealed an up to now unknown developmental boundary between the synchronously forming larval and the serially proliferating definitive segments. Development of three consecutive sets of nephridia with different morphology and biochemical properties was unexpected and reveals an interesting multistep process in the development of excretory structures in Platynereis.
Ancient animal microRNAs and the evolution of tissue identity.
Christodoulou, F., Raible, F., Tomer, R., Simakov, O., Trachana, K., Klaus, S., Snyman, H., Hannon, G.J., Bork, P. & Arendt, D.
Nature. 2010 Feb 25;463(7284):1084-8. Epub 2010 Jan 31.
The spectacular escalation in complexity in early bilaterian evolution correlates with a strong increase in the number of microRNAs. To explore the link between the birth of ancient microRNAs and body plan evolution, we set out to determine the ancient sites of activity of conserved bilaterian microRNA families in a comparative approach. We reason that any specific localization shared between protostomes and deuterostomes (the two major superphyla of bilaterian animals) should probably reflect an ancient specificity of that microRNA in their last common ancestor. Here, we investigate the expression of conserved bilaterian microRNAs in Platynereis dumerilii, a protostome retaining ancestral bilaterian features, in Capitella, another marine annelid, in the sea urchin Strongylocentrotus, a deuterostome, and in sea anemone Nematostella, representing an outgroup to the bilaterians. Our comparative data indicate that the oldest known animal microRNA, miR-100, and the related miR-125 and let-7 were initially active in neurosecretory cells located around the mouth. Other sets of ancient microRNAs were first present in locomotor ciliated cells, specific brain centres, or, more broadly, one of four major organ systems: central nervous system, sensory tissue, musculature and gut. These findings reveal that microRNA evolution and the establishment of tissue identities were closely coupled in bilaterian evolution. Also, they outline a minimum set of cell types and tissues that existed in the protostome-deuterostome ancestor.
Six3 demarcates the anterior-most developing brain region in bilaterian animals.
Steinmetz, P.R., Urbach, R., Posnien, N., Eriksson, J., Kostyuchenko, R.P., Brena, C., Guy, K., Akam, M., Bucher, G. & Arendt, D.
Evodevo. 2010 Dec 29;1(1):14.
BACKGROUND: The heads of annelids (earthworms, polychaetes, and others) and arthropods (insects, myriapods, spiders, and others) and the arthropod-related onychophorans (velvet worms) show similar brain architecture and for this reason have long been considered homologous. However, this view is challenged by the 'new phylogeny' placing arthropods and annelids into distinct superphyla, Ecdysozoa and Lophotrochozoa, together with many other phyla lacking elaborate heads or brains. To compare the organisation of annelid and arthropod heads and brains at the molecular level, we investigated head regionalisation genes in various groups. Regionalisation genes subdivide developing animals into molecular regions and can be used to align head regions between remote animal phyla. RESULTS: We find that in the marine annelid Platynereis dumerilii, expression of the homeobox gene six3 defines the apical region of the larval body, peripherally overlapping the equatorial otx+ expression. The six3+ and otx+ regions thus define the developing head in anterior-to-posterior sequence. In another annelid, the earthworm Pristina, as well as in the onychophoran Euperipatoides, the centipede Strigamia and the insects Tribolium and Drosophila, a six3/optix+ region likewise demarcates the tip of the developing animal, followed by a more posterior otx/otd+ region. Identification of six3+ head neuroectoderm in Drosophila reveals that this region gives rise to median neurosecretory brain parts, as is also the case in annelids. In insects, onychophorans and Platynereis, the otx+ region instead harbours the eye anlagen, which thus occupy a more posterior position. CONCLUSIONS: These observations indicate that the annelid, onychophoran and arthropod head develops from a conserved anterior-posterior sequence of six3+ and otx+ regions. The six3+ anterior pole of the arthropod head and brain accordingly lies in an anterior-median embryonic region and, in consequence, the optic lobes do not represent the tip of the neuraxis. These results support the hypothesis that the last common ancestor of annelids and arthropods already possessed neurosecretory centres in the most anterior region of the brain. In light of its b
The normal development of Platynereis dumerilii (Nereididae, Annelida).
Fischer, A.H., Henrich, T. & Arendt, D.
Front Zool. 2010 Dec 30;7:31.
ABSTRACT: BACKGROUND: The polychaete annelid Platynereis dumerilii is an emerging model organism for the study of molecular developmental processes, evolution, neurobiology and marine biology. Annelids belong to the Lophotrochozoa, the so far understudied third major branch of bilaterian animals besides deuterostomes and ecdysozoans. P. dumerilii has proven highly relevant to explore ancient bilaterian conditions via comparison to the deuterostomes, because it has accumulated less evolutionary change than conventional ecdysozoan models. Previous staging was mainly referring to hours post fertilization but did not allow matching stages between studies performed at (even slightly) different temperatures. To overcome this, and to provide a first comprehensive description of P. dumerilii normal development, a temperature-independent staging system is needed. RESULTS: Platynereis dumerilii normal development is subdivided into 16 stages, starting with the zygote and ending with the death of the mature worms after delivering their gametes. The stages described can be easily identified by conventional light microscopy or even by dissecting scope. Developmental landmarks such as the beginning of phototaxis, the visibility of the stomodeal opening and of the chaetae, the first occurrence of the ciliary bands, the formation of the parapodia, the extension of antennae and cirri, the onset of feeding and other characteristics are used to define different developmental stages. The morphology of all larval stages as well as of juveniles and adults is documented by light microscopy. We also provide an overview of important steps in the development of the nervous system and of the musculature, using fluorescent labeling techniques and confocal laser-scanning microscopy. Timing of each developmental stage refers to hours post fertilization at 18 +/- 0.1 degrees C. For comparison, we determined the pace of development of larvae raised at 14 degrees C, 16 degrees C, 20 degrees C, 25 degrees C, 28 degrees C and 30 degrees C. A staging ontology representing the comprehensive list of developmental stages of P. dumerilii is available online. CONCLUSIONS: Our atlas of Platynereis dumerilii normal development represents an important resource for the growing Platynereis community and can also be applied to other nereidid annelids.
The evolution of phototransduction and eyes.
Lamb, T.D., Arendt, D. & Collin, S.P.
Philos Trans R Soc Lond B Biol Sci. 2009 Oct 12;364(1531):2791-3. Europe PMC
The 'division of labour' model of eye evolution.
Arendt, D., Hausen, H. & Purschke, G.
Philos Trans R Soc Lond B Biol Sci. 2009 Oct 12;364(1531):2809-17.
The 'division of labour' model of eye evolution is elaborated here. We propose that the evolution of complex, multicellular animal eyes started from a single, multi-functional cell type that existed in metazoan ancestors. This ancient cell type had at least three functions: light detection via a photoreceptive organelle, light shading by means of pigment granules and steering through locomotor cilia. Located around the circumference of swimming ciliated zooplankton larvae, these ancient cells were able to mediate phototaxis in the absence of a nervous system. This precursor then diversified, by cell-type functional segregation, into sister cell types that specialized in different subfunctions, evolving into separate photoreceptor cells, shading pigment cells (SPCs) or ciliated locomotor cells. Photoreceptor sensory cells and ciliated locomotor cells remained interconnected by newly evolving axons, giving rise to an early axonal circuit. In some evolutionary lines, residual functions prevailed in the specialized cell types that mirror the ancient multi-functionality, for instance, SPCs expressing an opsin as well as possessing rhabdomer-like microvilli, vestigial cilia and an axon. Functional segregation of cell types in eye evolution also explains the emergence of more elaborate photosensory-motor axonal circuits, with interneurons relaying the visual information.
CNS evolution: new insight from the mud.
Benito-Gutierrez, E. & Arendt, D.
Curr Biol. 2009 Aug 11;19(15):R640-2.
Whether the highly centralised nervous systems of chordates and protostomes arose from a common ancestral precursor or independently has been a long-standing debate. Now, analysis of neural gene expression in an evolutionarily important chordate outgroup--the sand-dwelling, hemichordate acorn worms--reveals the presence of a central and peripheral nervous system, suggesting a common origin of central nervous systems.
Features of the ancestral bilaterian inferred from Platynereis dumerilii ParaHox genes.
Hui, J.H., Raible, F., Korchagina, N., Dray, N., Samain, S., Magdelenat, G., Jubin, C., Segurens, B., Balavoine, G., Arendt, D. & Ferrier, D.E.
BMC Biol. 2009 Jul 23;7:43.
BACKGROUND: The ParaHox gene cluster is the evolutionary sister to the Hox cluster. Whilst the role of the Hox cluster in patterning the anterior-posterior axis of bilaterian animals is well established, and the organisation of vertebrate Hox clusters is intimately linked to gene regulation, much less is known about the more recently discovered ParaHox cluster. ParaHox gene clustering, and its relationship to expression, has only been described in deuterostomes. Conventional protostome models (Drosophila melanogaster and Caenorhabditis elegans) are secondarily derived with respect to ParaHox genes, suffering gene loss and cluster break-up. RESULTS: We provide the first evidence for ParaHox gene clustering from a less-derived protostome animal, the annelid Platynereis dumerilii. Clustering of these genes is thus not a sole preserve of the deuterostome lineage within Bilateria. This protostome ParaHox cluster is not entirely intact however, with Pdu-Cdx being on the opposite end of the same chromosome arm from Pdu-Gsx and Pdu-Xlox. From the genomic sequence around the P. dumerilii ParaHox genes the neighbouring genes are identified, compared with other taxa, and the ancestral arrangement deduced. CONCLUSION: We relate the organisation of the ParaHox genes to their expression, and from comparisons with other taxa hypothesise that a relatively complex pattern of ParaHox gene expression existed in the protostome-deuterostome ancestor, which was secondarily simplified along several invertebrate lineages. Detailed comparisons of the gene content around the ParaHox genes enables the reconstruction of the genome surrounding the ParaHox cluster of the protostome-deuterostome ancestor, which existed over 550 million years ago.
To be or not to be a flatworm: the acoel controversy.
Egger, B., Steinke, D., Tarui, H., De Mulder, K., Arendt, D., Borgonie, G., Funayama, N., Gschwentner, R., Hartenstein, V., Hobmayer, B., Hooge, M., Hrouda, M., Ishida, S., Kobayashi, C., Kuales, G., Nishimura, O., Pfister, D., Rieger, R., Salvenmoser, W., Smith, J., Technau, U., Tyler, S., Agata, K., Salzburger, W. & Ladurner, P.
PLoS One. 2009;4(5):e5502. Epub 2009 May 11.
Since first described, acoels were considered members of the flatworms (Platyhelminthes). However, no clear synapomorphies among the three large flatworm taxa -- the Catenulida, the Acoelomorpha and the Rhabditophora -- have been characterized to date. Molecular phylogenies, on the other hand, commonly positioned acoels separate from other flatworms. Accordingly, our own multi-locus phylogenetic analysis using 43 genes and 23 animal species places the acoel flatworm Isodiametra pulchra at the base of all Bilateria, distant from other flatworms. By contrast, novel data on the distribution and proliferation of stem cells and the specific mode of epidermal replacement constitute a strong synapomorphy for the Acoela plus the major group of flatworms, the Rhabditophora. The expression of a piwi-like gene not only in gonadal, but also in adult somatic stem cells is another unique feature among bilaterians. These two independent stem-cell-related characters put the Acoela into the Platyhelminthes-Lophotrochozoa clade and account for the most parsimonious evolutionary explanation of epidermal cell renewal in the Bilateria. Most available multigene analyses produce conflicting results regarding the position of the acoels in the tree of life. Given these phylogenomic conflicts and the contradiction of developmental and morphological data with phylogenomic results, the monophyly of the phylum Platyhelminthes and the position of the Acoela remain unresolved. By these data, both the inclusion of Acoela within Platyhelminthes, and their separation from flatworms as basal bilaterians are well-supported alternatives.
Eye evolution: the blurry beginning.
Nilsson, D.E. & Arendt, D.
Curr Biol. 2008 Dec 9;18(23):R1096-8.
Recent work on the expression of retinal transcription factors and other molecular cues delivers interesting but partly contradictory information on the early phases of eye evolution.
Mechanism of phototaxis in marine zooplankton.
Jekely, G., Colombelli, J., Hausen, H., Guy, K., Stelzer, E.H.K., Nedelec, F. & Arendt, D.
Nature. 2008 Nov 20;456(7220):395-9.
The simplest animal eyes are eyespots composed of two cells only: a photoreceptor and a shading pigment cell. They resemble Darwin's 'proto-eyes', considered to be the first eyes to appear in animal evolution. Eyespots cannot form images but enable the animal to sense the direction of light. They are characteristic for the zooplankton larvae of marine invertebrates and are thought to mediate larval swimming towards the light. Phototaxis of invertebrate larvae contributes to the vertical migration of marine plankton, which is thought to represent the biggest biomass transport on Earth. Yet, despite its ecological and evolutionary importance, the mechanism by which eyespots regulate phototaxis is poorly understood. Here we show how simple eyespots in marine zooplankton mediate phototactic swimming, using the marine annelid Platynereis dumerilii as a model. We find that the selective illumination of one eyespot changes the beating of adjacent cilia by direct cholinergic innervation resulting in locally reduced water flow. Computer simulations of larval swimming show that these local effects are sufficient to direct the helical swimming trajectories towards the light. The computer model also shows that axial rotation of the larval body is essential for phototaxis and that helical swimming increases the precision of navigation. These results provide, to our knowledge, the first mechanistic understanding of phototaxis in a marine zooplankton larva and show how simple eyespots regulate it. We propose that the underlying direct coupling of light sensing and ciliary locomotor control was a principal feature of the proto-eye and an important landmark in the evolution of animal eyes.
The evolution of cell types in animals: emerging principles from molecular studies.
Nat Rev Genet. 2008 Nov;9(11):868-82.
Cell types are fundamental units of multicellular life but their evolution is obscure. How did the first cell types emerge and become distinct in animal evolution? What were the sets of cell types that existed at important evolutionary nodes that represent eumetazoan or bilaterian ancestors? How did these ancient cell types diversify further during the evolution of organ systems in the descending evolutionary lines? The recent advent of cell type molecular fingerprinting has yielded initial insights into the evolutionary interrelationships of cell types between remote animal phyla and has allowed us to define some first principles of cell type diversification in animal evolution.
The evolution of nervous system centralization.
Arendt, D., Denes, A.S., Jekely, G. & Tessmar-Raible, K.
Philos Trans R Soc Lond B Biol Sci. 2008 Apr 27;363(1496):1523-8.
It is yet unknown when and in what form the central nervous system in Bilateria first came into place and how it further evolved in the different bilaterian phyla. To find out, a series of recent molecular studies have compared neurodevelopment in slow-evolving deuterostome and protostome invertebrates, such as the enteropneust hemichordate Saccoglossus and the polychaete annelid Platynereis. These studies focus on the spatially different activation and, when accessible, function of genes that set up the molecular anatomy of the neuroectoderm and specify neuron types that emerge from distinct molecular coordinates. Complex similarities are detected, which reveal aspects of neurodevelopment that most likely occurred already in a similar manner in the last common ancestor of the bilaterians, Urbilateria. This way, different aspects of the molecular architecture of the urbilaterian nervous system are reconstructed and yield insight into the degree of centralization that was in place in the bilaterian ancestors.
4DXpress: a database for cross-species expression pattern comparisons.
Haudry, Y., Berube, H., Letunic, I., Weeber, P.D., Gagneur, J., Girardot, C., Kapushesky, M., Arendt, D., Bork, P., Brazma, A., Furlong, E.E., Wittbrodt, J. & Henrich, T.
Nucleic Acids Res. 2008 Jan;36(Database issue):D847-53. Epub 2007 Oct 4.
In the major animal model species like mouse, fish or fly, detailed spatial information on gene expression over time can be acquired through whole mount in situ hybridization experiments. In these species, expression patterns of many genes have been studied and data has been integrated into dedicated model organism databases like ZFIN for zebrafish, MEPD for medaka, BDGP for Drosophila or GXD for mouse. However, a central repository that allows users to query and compare gene expression patterns across different species has not yet been established. Therefore, we have integrated expression patterns for zebrafish, Drosophila, medaka and mouse into a central public repository called 4DXpress (expression database in four dimensions). Users can query anatomy ontology-based expression annotations across species and quickly jump from one gene to the orthologues in other species. Genes are linked to public microarray data in ArrayExpress. We have mapped developmental stages between the species to be able to compare developmental time phases. We store the largest collection of gene expression patterns available to date in an individual resource, reflecting 16 505 annotated genes. 4DXpress will be an invaluable tool for developmental as well as for computational biologists interested in gene regulation and evolution. 4DXpress is available at http://ani.embl.de/4DXpress.
atonal- and achaete-scute-related genes in the annelid Platynereis dumerilii: insights into the evolution of neural basic-Helix-Loop-Helix genes.
Simionato, E., Kerner, P., Dray, N., Le Gouar, M., Ledent, V., Arendt, D. & Vervoort, M.
BMC Evol Biol. 2008 Jun 9;8:170.
BACKGROUND: Functional studies in model organisms, such as vertebrates and Drosophila, have shown that basic Helix-loop-Helix (bHLH) proteins have important roles in different steps of neurogenesis, from the acquisition of neural fate to the differentiation into specific neural cell types. However, these studies highlighted many differences in the expression and function of orthologous bHLH proteins during neural development between vertebrates and Drosophila. To understand how the functions of neural bHLH genes have evolved among bilaterians, we have performed a detailed study of bHLH genes during nervous system development in the polychaete annelid, Platynereis dumerilii, an organism which is evolutionary distant from both Drosophila and vertebrates. RESULTS: We have studied Platynereis orthologs of the most important vertebrate neural bHLH genes, i.e. achaete-scute, neurogenin, atonal, olig, and NeuroD genes, the latter two being genes absent of the Drosophila genome. We observed that all these genes have specific expression patterns during nervous system formation in Platynereis. Our data suggest that in Platynereis, like in vertebrates but unlike Drosophila, (i) neurogenin is the main proneural gene for the formation of the trunk central nervous system, (ii) achaete-scute and olig genes are involved in neural subtype specification in the central nervous system, in particular in the specification of the serotonergic phenotype. In addition, we found that the Platynereis NeuroD gene has a broad and early neuroectodermal expression, which is completely different from the neuronal expression of vertebrate NeuroD genes. CONCLUSION: Our analysis suggests that the Platynereis bHLH genes have both proneural and neuronal specification functions, in a way more akin to the vertebrate situation than to that of Drosophila. We conclude that these features are ancestral to bilaterians and have been conserved in the vertebrates and annelids lineages, but have diverged in the evolutionary lineage leading to Drosophila.
Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution.
Tessmar-Raible, K., Raible, F., Christodoulou, F., Guy, K., Rembold, M., Hausen, H. & Arendt, D.
Cell. 2007 Jun 29;129(7):1389-400.
Neurosecretory control centers form part of the forebrain in many animal phyla, including vertebrates, insects, and annelids. The evolutionary origin of these centers is largely unknown. To identify conserved, and thus phylogenetically ancient, components of neurosecretory brain centers, we characterize and compare neurons that express the prohormone vasotocin (vasopressin/oxytocin)-neurophysin in the developing forebrain of the annelid Platynereis dumerilii and of the zebrafish. These neurons express the same tissue-restricted microRNA, miR-7, and conserved, cell-type-specific combinations of transcription factors (nk2.1, rx, and otp) that specify their identity, as evidenced by the specific requirement of zebrafish rx3 for vasotocin-neurophysin expression. MiR-7 also labels another shared population of neurons containing RFamides. Since the vasotocinergic and RFamidergic neurons appear to be directly sensory in annelid and fish, we propose that cell types with dual sensory-neurosecretory properties were the starting point for the evolution of neurosecretory brain centers in Bilateria.
Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii.
Rebscher, N., Zelada-Gonzalez, F., Banisch, T.U., Raible, F. & Arendt, D.
Dev Biol. 2007 Jun 15;306(2):599-611. Epub 2007 Apr 1.
To elucidate the evolution of germ cell specification in Metazoa, recent comparative studies focus on ancestral animal groups. Here, we followed the germline throughout the life cycle of the polychaete annelid Platynereis dumerilii, by examining mRNA and protein expression of vasa and other germline-specific factors in combination with lineage tracing experiments. In the fertilised egg, maternal Vasa protein localises to the yolk-free cytoplasm at the animal pole. It then asymmetrically segregates first into the micromeres, then into the founder cells of the mesodermal posterior growth zone (MPGZ). Vasa transcripts initially show ubiquitous distribution, but then become progressively restricted to the MPGZ. The cells of the MPGZ are highly proliferative, as evidenced by BrdU pulse labelling experiments. Besides vasa, they express nanos along with the stem cell-specific genes piwi, and PL10. At 4 days of development, four primordial germ cells are singled out from within the MPGZ, and migrate into the anterior segments to colonise a newly discovered "primary gonad". Our data suggest a common origin of germ cells and of somatic stem cells, similar to the situation found in planarians and cnidarians, which may constitute the ancestral mode of germ cell specification in Metazoa.
Cellular resolution expression profiling using confocal detection of NBT/BCIP precipitate by reflection microscopy.
Jekely, G. & Arendt, D.
Biotechniques. 2007 Jun;42(6):751-5.
The determination of gene expression patterns in three dimensions with cellular resolution is an important goal in developmental biology. However the most sensitive, efficient, and widely used staining technique for whole-mount in situ hybridization (WMISH), nitroblue tetrazolium (NBT)/5-bromo-4-chloro-3-indolyl phosphate (BCIP) precipitation by alkaline phosphatase, could not yet be combined with the most precise, high-resolution detection technique, confocal laser-scanning microscopy (CLSM). Here we report the efficient visualization of the NBT/BCIP precipitate using confocal reflection microscopy for WMISH samples of Drosophila, zebrafish, and the marine annelid worm, Platynereis dumerilii. In our simple WMISH protocol for reflection CLSM, NBT/BCIP staining can be combined with fluorescent WMISH, immunostainings, or transgenic green fluorescent protein (GFP) marker lines, allowing double labeling of cell types or of embryological structures of interest. Whole-mount reflection CLSM will thus greatly facilitate large-scale cellular resolution expression profiling in vertebrate and invertebrate model organisms.
Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria.
Denes, A.S., Jekely, G., Steinmetz, P.R., Raible, F., Snyman, H., Prud'homme, B., Ferrier, D.E., Balavoine, G. & Arendt, D.
Cell. 2007 Apr 20;129(2):277-88.
To elucidate the evolutionary origin of nervous system centralization, we investigated the molecular architecture of the trunk nervous system in the annelid Platynereis dumerilii. Annelids belong to Bilateria, an evolutionary lineage of bilateral animals that also includes vertebrates and insects. Comparing nervous system development in annelids to that of other bilaterians could provide valuable information about the common ancestor of all Bilateria. We find that the Platynereis neuroectoderm is subdivided into longitudinal progenitor domains by partially overlapping expression regions of nk and pax genes. These domains match corresponding domains in the vertebrate neural tube and give rise to conserved neural cell types. As in vertebrates, neural patterning genes are sensitive to Bmp signaling. Our data indicate that this mediolateral architecture was present in the last common bilaterian ancestor and thus support a common origin of nervous system centralization in Bilateria.
Duplication of the ribosomal gene cluster in the marine polychaete Platynereis dumerilii correlates with ITS polymorphism.
Hui, JHL; Kortchagina, N; Arendt, D.; Balavoine, G; Ferrier, DEK
Journal of the Marine Biological Association of the United Kingdom 2007/04 87(2) 443-449
Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation.
Steinmetz, P.R., Zelada-Gonzales, F., Burgtorf, C., Wittbrodt, J. & Arendt, D.
Proc Natl Acad Sci U S A. 2007 Feb 14;.
During frog and fish development, convergent extension movements transform the spherical gastrula into an elongated neurula. Such transformation of a ball- into a worm-shaped embryo is an ancestral and fundamental feature of bilaterian development, yet this is modified or absent in the protostome model organisms Caenorhabditis or Drosophila. In the polychaete annelid Platynereis dumerilii, early embryonic and larval stages resemble a sphere that subsequently elongates into worm shape. Cellular and molecular mechanisms of polychaete body elongation are yet unknown. Our in vivo time-lapse analysis of Platynereis axis elongation reveals that the polychaete neuroectoderm converges and extends by mediolateral cell intercalation. This occurs on both sides of the neural midline, the line of fusion of the slit-like blastopore. Convergent extension moves apart mouth and anus that are both derived from the blastopore. Tissue elongation is actin-dependent but microtubule-independent. Dependence on JNK activity and spatially restricted expression of strabismus indicates involvement of the noncanonical Wnt pathway. We detect a morphogenetic boundary between the converging and extending trunk neuroectoderm and the anterior otx-expressing head neuroectoderm that does not elongate. Our comparative analysis uncovers striking similarities but also differences between convergent extension in the polychaete and in the frog (the classical vertebrate model for convergent extension). Based on these findings, we propose that convergent extension movements of the trunk neuroectoderm represent an ancestral feature of bilaterian development that triggered the separation of mouth and anus along the elongating trunk.
Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa).
Kulakova, M., Bakalenko, N., Novikova, E., Cook, C.E., Eliseeva, E., Steinmetz, P.R., Kostyuchenko, R.P., Dondua, A., Arendt, D., Akam, M. & Andreeva, T.
Dev Genes Evol. 2007 Jan;217(1):39-54. Epub 2006 Dec 19.
The bilaterian animals are divided into three great branches: the Deuterostomia, Ecdysozoa, and Lophotrochozoa. The evolution of developmental mechanisms is less studied in the Lophotrochozoa than in the other two clades. We have studied the expression of Hox genes during larval development of two lophotrochozoans, the polychaete annelids Nereis virens and Platynereis dumerilii. As reported previously, the Hox cluster of N. virens consists of at least 11 genes (de Rosa R, Grenier JK, Andreeva T, Cook CE, Adoutte A, Akam M, Carroll SB, Balavoine G, Nature, 399:772-776, 1999; Andreeva TF, Cook C, Korchagina NM, Akam M, Dondua AK, Ontogenez 32:225-233, 2001); we have also cloned nine Hox genes of P. dumerilii. Hox genes are mainly expressed in the descendants of the 2d blastomere, which form the integument of segments, ventral neural ganglia, pre-pygidial growth zone, and the pygidial lobe. Patterns of expression are similar for orthologous genes of both nereids. In Nereis, Hox2, and Hox3 are activated before the blastopore closure, while Hox1 and Hox4 are activated just after this. Hox5 and Post2 are first active during the metatrochophore stage, and Hox7, Lox4, and Lox2 at the late nectochaete stage only. During larval stages, Hox genes are expressed in staggered domains in the developing segments and pygidial lobe. The pattern of expression of Hox cluster genes suggests their involvement in the vectorial regionalization of the larval body along the antero-posterior axis. Hox gene expression in nereids conforms to the canonical patterns postulated for the two other evolutionary branches of the Bilateria, the Ecdysozoa and the Deuterostomia, thus supporting the evolutionary conservatism of the function of Hox genes in development.
Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome.
Raible, F., Tessmar-Raible, K., Arboleda, E., Kaller, T., Bork, P., Arendt, D. & Arnone, M.I.
Dev Biol. 2006 Dec 1;300(1):461-75. Epub 2006 Sep 5.
Rhodopsin-type G-protein-coupled receptors (GPCRs) contribute the majority of sensory receptors in vertebrates. With 979 members, they form the largest GPCR family in the sequenced sea urchin genome, constituting more than 3% of all predicted genes. The sea urchin genome encodes at least six Opsin proteins. Of these, one rhabdomeric, one ciliary and two G(o)-type Opsins can be assigned to ancient bilaterian Opsin subfamilies. Moreover, we identified four greatly expanded subfamilies of rhodopsin-type GPCRs that we call sea urchin specific rapidly expanded lineages of GPCRs (surreal-GPCRs). Our analysis of two of these groups revealed genomic clustering and single-exon gene structures similar to the most expanded group of vertebrate rhodopsin-type GPCRs, the olfactory receptors. We hypothesize that these genes arose by rapid duplication in the echinoid lineage and act as chemosensory receptors of the animal. In support of this, group B surreal-GPCRs are most prominently expressed in distinct classes of pedicellariae and tube feet of the adult sea urchin, structures that have previously been shown to react to chemical stimuli and to harbor sensory neurons in echinoderms. Notably, these structures also express different opsins, indicating that sea urchins possess an intricate molecular set-up to sense their environment.
The expression of a hunchback ortholog in the polychaete annelid Platynereis dumerilii suggests an ancestral role in mesoderm development and neurogenesis.
Kerner, P., Zelada Gonzalez, F., Le Gouar, M., Ledent, V., Arendt, D. & Vervoort, M.
Dev Genes Evol. 2006 Dec;216(12):821-8. Epub 2006 Sep 16.
Orthologs of the Drosophila gap gene hunchback have been isolated so far only in protostomes. Phylogenetic analysis of recently available genomic data allowed us to confirm that hunchback genes are widely found in protostomes (both lophotrochozoans and ecdysozoans). In contrast, no unequivocal hunchback gene can be found in the genomes of deuterostomes and non-bilaterians. We cloned hunchback in the marine polychaete annelid Platynereis dumerilii and analysed its expression during development. In this species, hunchback displays an expression pattern indicative of a role in mesoderm formation and neurogenesis, and similar to the expression found for hunchback genes in arthropods. These data suggest altogether that these functions are ancestral to protostomes.
The regulatory genome - Gene regulatory networks in development and evolution.
Science 2006 314(5802)
Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium.
Jekely, G. & Arendt, D.
Bioessays. 2006 Feb;28(2):191-8.
The cilium/flagellum is a sensory-motile organelle ancestrally present in eukaryotic cells. For assembly cilia universally rely on intraflagellar transport (IFT), a specialised bidirectional transport process mediated by the ancestral and conserved IFT complex. Based on the homology of IFT complex proteins to components of coat protein I (COPI) and clathrin-coated vesicles, we propose that the non- vesicular, membrane-bound IFT evolved as a specialised form of coated vesicle transport from a protocoatomer complex. IFT thus shares common ancestry with all protocoatomer derivatives, including all vesicle coats and the nuclear pore complex (NPC). This has major implications for the evolutionary origin of the cilium. First, it reinforces the tenet that duplication and divergence of pre-existing structures, rather than symbiosis, were the major themes during cilium evolution. Second, it suggests that the initial step in the autogenous origin of the cilium was the establishment of a membrane patch with transmembrane proteins transported by the ancestral vesicle-coating IFT complex. We propose a scenario for how the initial membrane patch gradually protruded to enhance exposure to the environment, then started to move, and finally compartmentalised to render receptor signalling and ciliary beating more efficient.
Photoreceptor cells and eyes in Annelida.
Purschke, G., Arendt, D., Hausen, H. & Müller, M.C.M.
Arthropod Structure & Development 2006 35 211-230
Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii.
Raible, F., Tessmar-Raible, K., Osoegawa, K., Wincker, P., Jubin, C., Balavoine, G., Ferrier, D., Benes, V., de Jong, P., Weissenbach, J., Bork, P. & Arendt, D.
Science 2005 Nov 25;310(5752):1325-6.
Previous genome comparisons have suggested that one important trend in vertebrate evolution has been a sharp rise in intron abundance. By using genomic data and expressed sequence tags from the marine annelid Platynereis dumerilii, we provide direct evidence that about two-thirds of human introns predate the bilaterian radiation but were lost from insect and nematode genomes to a large extent. A comparison of coding exon sequences confirms the ancestral nature of Platynereis and human genes. Thus, the urbilaterian ancestor had complex, intron-rich genes that have been retained in Platynereis and human.
Fluorescent two-color whole mount in situ hybridization in Platynereis dumerilii (Polychaeta, Annelida), an emerging marine molecular model for evolution and development.
Tessmar-Raible, K., Steinmetz, P.R., Snyman, H., Hassel, M. & Arendt, D.
Biotechniques 2005 Oct;39(4):460, 462, 464. Europe PMC
Ancestry of photic and mechanic sensation?
Fritzsch, B., Piatigorsky, J., Tessmar-Raible, K., Jekely, G., Guy, K., Raible, F., Wittbrodt, J. & Arendt, D.
Science 2005 May 20;308(5725):1113-1114. Europe PMC
New animal models for evolution and development.
Tessmar-Raible, K. & Arendt, D.
Genome Biol 2005;6(1):303. Epub 2004 Dec 21.
A report on the annual UK Evolutionary Developmental Biology meeting, Oxford, UK, 13 September 2004.
Genes and homology in nervous system evolution: Comparing gene functions, expression patterns, and cell type molecular fingerprints.
Theory in Biosciences 2005 Nov;124(2):185-197.
The evolution of the nervous system is one of the most fascinating, but also most nebulous fields of homology research. We do not know for example whether the last common ancestors of human, squid, and fly already possessed an elaborate brain and eyes, or rather had a simple, diffuse nervous system. Nevertheless, in the past decade molecular data has greatly advanced our understanding of bilaterian nervous system evolution. In this methodological review, I explain the four levels on which molecular genetic studies advance the quest for homologies between animal nervous systems. (1) Bioinformatic homology research elucidates the evolutionary history of gene families relevant for nervous system evolution such as the opsin superfamily. It tells us when and in what order genes and their functions have emerged. Based on this, we can (11) infer the organismal complexity of some remote ancestor from the functional diversity of its reconstructed proteome. (111) Most common in molecular homology research has been the comparison of expression patterns of developmental control genes. This approach matches and aligns embryonic regions along the body axes, between remote bilaterians. It does not tell us much, however, about the complexity of structures that developed from these regions in Urbilateria. (IV) This is overcome by a novel variant of molecular homology research, the comparison of cell types. Here, a similar "molecular fingerprint" of cells is taken as indication of cross-bilaterian homology. This approach makes it possible to reconstruct the cell-type repertoire of the urbilaterian nervous system. (c) 2005 Elsevier GmbH. All rights reserved.
Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain.
Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A.W. & Wittbrodt, J.
Science 2004 Oct 29;306(5697):869-71.
For vision, insect and vertebrate eyes use rhabdomeric and ciliary photoreceptor cells, respectively. These cells show distinct architecture and transduce the light signal by different phototransductory cascades. In the marine rag-worm Platynereis, we find both cell types: rhabdomeric photoreceptor cells in the eyes and ciliary photoreceptor cells in the brain. The latter use a photopigment closely related to vertebrate rod and cone opsins. Comparative analysis indicates that both types of photoreceptors, with distinct opsins, coexisted in Urbilateria, the last common ancestor of insects and vertebrates, and sheds new light on vertebrate eye evolution.
Metazoan evolution: some animals are more equal than others.
Raible, F. & Arendt, D.
Curr Biol 2004 Feb 3;14(3):R106-8.
Comparison of newly available sequence data facilitates reconstruction of the gene inventory of the Urbilateria, the last common ancestor of flies, nematodes and humans. The most surprising outcome is that human genes seem to be closer to the bilaterian roots than previously assumed.
Comparative aspects of gastrulation.
In "Gastrulation", Stern, C. (ed.), Cold Spring Harbor Press, New York
Arthropod-like expression patterns of engrailed and wingless in the annelid Platynereis dumerilii suggest a role in segment formation.
Prud'homme, B., de Rosa, R., Arendt, D., Julien, J.F., Pajaziti, R., Dorresteijn, A.W., Adoutte, A., Wittbrodt, J. & Balavoine, G.
Curr Biol 2003 Oct 28;13(21):1876-81.
The origin of animal segmentation, the periodic repetition of anatomical structures along the anteroposterior axis, is a long-standing issue that has been recently revived by comparative developmental genetics. In particular, a similar extensive morphological segmentation (or metamerism) is commonly recognized in annelids and arthropods. Mostly based on this supposedly homologous segmentation, these phyla have been united for a long time into the clade Articulata. However, recent phylogenetic analysis dismissed the Articulata and thus challenged the segmentation homology hypothesis. Here, we report the expression patterns of genes orthologous to the arthropod segmentation genes engrailed and wingless in the annelid Platynereis dumerilii. In Platynereis, engrailed and wingless are expressed in continuous ectodermal stripes on either side of the segmental boundary before, during, and after its formation; this expression pattern suggests that these genes are involved in segment formation. The striking similarities of engrailed and wingless expressions in Platynereis and arthropods may be due to evolutionary convergence or common heritage. In agreement with similarities in segment ontogeny and morphological organization in arthropods and annelids, we interpret our results as molecular evidence of a segmented ancestor of protostomes.
Emerging systems: between vertebrates and arthropods, the Lophotrochozoa.
Tessmar-Raible, K. & Arendt, D.
Curr Opin Genet Dev 2003 Aug;13(4):331-40.
Novel molecular model organisms for the study of development and regeneration are emerging among the Lophotrochozoa, the third major branch of bilaterian animals. The polychaete Platynereis, the leech Helobdella, the snail Ilyanassa, and several planarians are efficiently accessed for molecular techniques including large-scale whole-mount in situ hybridization screening, RNA interference or morpholino knock-down. Joint efforts include the generation of genomic resources in the form of expressed sequence tag collections and bacterial artificial chromosome libraries. Current research focuses on early pattern formation during cleavage, the emergence and diversification of body segments, and the formation of photoreceptor cells and eyes. Several lophotrochozoan groups (in particular nereid polychaetes) exhibit modes of development, organ design, or body plans that are considered ancestral in many respects. This is also reflected in the level of genes, making these groups ideally suited for developmental comparative studies.
Evolution of eyes and photoreceptor cell types.
Int J Dev Biol 2003;47(7-8):563-71.
The evolution of the eye is a matter of debate ever since Darwin's Origin of Species. While morphological comparisons of eye anatomy and photoreceptor cell types led to the view that animal eyes evolved multiple times independently, the molecular conservation of the pax6 eye-specifying cascade has indicated the contrary - that animal eyes evolved from a common, simple precursor, the proto-eye. Morphological and molecular comparative approaches are combined here in a novel Evo-Devo approach, the molecular comparison of cell types ("comparative molecular cell biology"). In the eye, the various types of photoreceptor cells, as well as pigment and lens cells, each require distinct combinations of specifying transcription factors that control their particular differentiation programmes, such as opsin expression in photoreceptors, specific neurotransmitter metabolism, or axonal outgrowth. Comparing the molecular combinatorial codes of cell types of animal extant eyes, their evolutionary histories can be reconstructed. This is exemplified here on the evolution of ciliary and rhabdomeric photoreceptor cells in bilaterian eyes and on the evolution of cell type diversity in the vertebrate retina. I propose that the retinal ganglion, amacrine and horizontal cells are evolutionary sister cell types that evolved from a common rhabdomeric photoreceptor cell precursor.
Spiralians in the limelight.
Genome Biol 2003;5(1):303.
A report on the meeting 'Developmental Basis of Evolutionary Change', University of Chicago, USA, 16-18 October 2003.
Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria.
Arendt, D., Tessmar, K., de Campos-Baptista, M.I., Dorresteijn, A. & Wittbrodt, J.
Development 2002 Mar;129(5):1143-54.
The role of Pax6 in eye development in insects and vertebrates supports the view that their eyes evolved from simple pigment-cup ocelli present in their last common ancestors (Urbilateria). The cerebral eyes in errant polychaetes represent prototype invertebrate pigment-cup ocelli and thus resemble the presumed ancestral eyes. We have analysed expression of conserved eye specification genes in the early development of larval and adult pigment-cup eyes in Platynereis dumerilii (Polychaeta, Annelida, Lophotrochozoa). Both larval and adult eyes form in close vicinity of the optic anlagen on both sides of the developing brain ganglia. While pax6 is expressed in the larval, but not in the developing, adult eyes, expression of six1/2 from trochophora stages onwards specifically outlines the optic anlagen and thus covers both the developing larval and adult eyes. Using Platynereis rhabdomeric opsin as differentiation marker, we show that the first pair of adult eye photoreceptor cells is detected within bilateral clusters that transitorily express ath, the Platynereis atonal orthologue, thus resembling proneural sensory clusters. Our data indicate that--similar to insects, but different from the vertebrates--polychaete six1/2 expression outlines the entire visual system from early developmental stages onwards and ath-positive clusters generate the first photoreceptor cells to appear. We propose that pax6-, six1/2- and ath-positive larval eyes, as found in today's trochophora, were present already in Urbilateria.
Reconstructing the eyes of Urbilateria.
Arendt, D. & Wittbrodt, J.
Philos Trans R Soc Lond B Biol Sci 2001 Oct 29;356(1414):1545-63.
The shared roles of Pax6 and Six homologues in the eye development of various bilaterians suggest that Urbilateria, the common ancestors of all Bilateria, already possessed some simple form of eyes. Here, we re-address the homology of bilaterian cerebral eyes at the level of eye anatomy, of eye-constituting cell types and of phototransductory molecules. The most widespread eye type found in Bilateria are the larval pigment-cup eyes located to the left and right of the apical organ in primary, ciliary larvae of Protostomia and Deuterostomia. They can be as simple as comprising a single pigment cell and a single photoreceptor cell in inverse orientation. Another more elaborate type of cerebral pigment-cup eyes with an everse arrangement of photoreceptor cells is found in adult Protostomia. Both inverse larval and everse adult eyes employ rhabdomeric photoreceptor cells and thus differ from the chordate cerebral eyes with ciliary photoreceptors. This is highly significant because on the molecular level we find that for phototransduction rhabdomeric versus ciliary photoreceptor cells employ divergent rhodopsins and non-orthologous G-proteins, rhodopsin kinases and arrestins. Our comparison supports homology of cerebral eyes in Protostomia; it challenges, however, homology of chordate and non-chordate cerebral eyes that employ photoreceptor cells with non-orthologous phototransductory cascades.
Medaka eyeless is the key factor linking retinal determination and eye growth.
Loosli, F., Winkler, S., Burgtorf, C., Wurmbach, E., Ansorge, W., Henrich, T., Grabher, C., Arendt, D., Carl, M., Krone, A., Grzebisz, E. & Wittbrodt, J.
Development 2001 Oct;128(20):4035-44.
The complete absence of eyes in the medaka fish mutation eyeless is the result of defective optic vesicle evagination. We show that the eyeless mutation is caused by an intronic insertion in the Rx3 homeobox gene resulting in a transcriptional repression of the locus that is rescued by injection of plasmid DNA containing the wild-type locus. Functional analysis reveals that Six3- and Pax6- dependent retina determination does not require Rx3. However, gain- and loss-of-function phenotypes show that Rx3 is indispensable to initiate optic vesicle evagination and to control vesicle proliferation, by that regulating organ size. Thus, Rx3 acts at a key position coupling the determination with subsequent morphogenesis and differentiation of the developing eye.
Evolution of the bilaterian larval foregut.
Arendt, D., Technau, U. & Wittbrodt, J.
Nature 2001 Jan 4;409(6816):81-5.
Bilateria are subdivided into Protostomia and Deuterostomia. Indirect development through primary, ciliary larvae occurs in both of these branches; however, the closing blastopore develops into mouth and anus in Protostomia and into anus only in Deuterostomia. Because of this important difference in larval gut ontogeny, the tube-shaped guts in protostome and deuterostome primary larvae are thought to have evolved independently. To test this hypothesis, we have analysed the expression of brachyury, otx and goosecoid homologues in the polychaete Platynereis dumerilii, which develops by means of a trochophora larva-the primary, ciliary larva prototypic for Protostomia. Here we show that brachyury expression in the ventral portion of the developing foregut in Platynereis and also otx expression along ciliated bands in the mouth region of the trochophora larva parallels expression in primary larvae in Deuterostomia. In addition, goosecoid expression in the foregut of Platynereis mirrors the function in higher Deuterostomia. We present molecular evidence for the evolutionary conservation of larval foreguts and mouth regions of Protostomia and Deuterostomia. Our data indicate that Urbilateria, the common bilaterian ancestors, developed through a primary, ciliary larva that already possessed a tripartite tube-shaped gut.
Comparison of early nerve cord development in insects and vertebrates.
Arendt, D. & Nubler-Jung, K.
Development 1999 Jun;126(11):2309-25.
It is widely held that the insect and vertebrate CNS evolved independently. This view is now challenged by the concept of dorsoventral axis inversion, which holds that ventral in insects corresponds to dorsal in vertebrates. Here, insect and vertebrate CNS development is compared involving embryological and molecular data. In insects and vertebrates, neurons differentiate towards the body cavity. At early stages of neurogenesis, neural progenitor cells are arranged in three longitudinal columns on either side of the midline, and NK-2/NK-2.2, ind/Gsh and msh/Msx homologs specify the medial, intermediate and lateral columns, respectively. Other pairs of regional specification genes are, however, expressed in transverse stripes in insects, and in longitudinal stripes in the vertebrates. There are differences in the regional distribution of cell types in the developing neuroectoderm. However, within a given neurogenic column in insects and vertebrates some of the emerging cell types are remarkably similar and may thus be phylogenetically old: NK-2/NK-2.2-expressing medial column neuroblasts give rise to interneurons that pioneer the medial longitudinal fascicles, and to motoneurons that exit via lateral nerve roots to then project peripherally. Lateral column neuroblasts produce, among other cell types, nerve root glia and peripheral glia. Midline precursors give rise to glial cells that enwrap outgrowing commissural axons. The midline glia also express netrin homologs to attract commissural axons from a distance.
Rearranging gastrulation in the name of yolk: evolution of gastrulation in yolk-rich amniote eggs.
Arendt, D. & Nubler-Jung, K.
Mech Dev. 1999 Mar;81(1-2):3-22.
Gastrulating birds and mammals form a primitive streak in lieu of a circular blastopore, and a conspicuous underlying tissue layer, the hypoblast. In an attempt to understand the evolution of these amniote characteristics, pregastrula and gastrulation stages in selected amniotes are compared with the more ancestral situation in amphibians. At blastula/blastoderm stages, the overall fate maps and the arrangement of tissues around the organizer are rather similar, as is exemplified by a comparison of gene expression and fate maps in the frog and chick. Compared with amphibians, however, the eggs of reptiles, birds and monotreme mammals have a disproportionately large yolk that alters gastrulation morphology. During amphibian gastrulation, the organizer moves from anterior to posterior, to lay down the dorsal axis around the vegetal hemisphere (Arendt, D., Nubler-Jung, K., 1997. Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates. Mech. Dev. 61, 1-15). In contrast, in amniote eggs, the large yolk impedes the organizer from moving around the entire vegetal hemisphere so that axis formation begins and ends at the same side of the egg. This has apparently provoked an evolutionary transformation of an amphibian-like blastopore, first into the 'blastoporal canal' of reptiles, and then into the birds' and mammals' primitive streak. The blastopore divides into two functionally divergent parts, one as the site of mesoderm internalization ('intraembryonic blastopore') and the other as the site of ectodermal epiboly ('extraembryonic blastopore'). The hypoblast is proposed to derive from the 'endodermal wedge' that is seen already in the amphibian gastrula. Hypoblast formation would then represent a special kind of gastrulation movement that also exists in the amphibians, and for which the term 'hypoboly' is introduced.
Dorsoventral axis inversion: Enteropneust anatomy links invertebrates to chordates turned upside down.
Nübler-Jung, K. and Arendt, D. (1999
J. Zool. Syst. Evol. Res. 1999 37(2) 93-100
The relationships between chordates with their dorsal nerve cord and other animal groups remain unclear. The hemichordata, specifically the enteropneusta (acorn worms), have been considered a sister group to the chordata. Enteropneusts combine Various chordate features (e.g. lateral gill openings, dorsal nerve cord) with features that are usually associated with gastroneuralian invertebrates (e.g. dorsal heart, circumenteric nerve ring, ventral nerve cord). Here we analyse various morphological and functional characteristics that enteropneusts share with either invertebrates or chordates in the light of our recent proposal that the chordata may derive - by bodily dorsoventral inversion - from a gastroneuralian ancestor. We show that many seemingly non-chordate Features of enteropneusts will align with similar features in the chordates - provided that we compare the ventral side of an enteropneust to the dorsal side of a chordate. This inversion proposes several interesting and new putative homologies between enteropneusts and acranian chordates, such as between their epibranchial ridge/endostyle (later thyroid gland), their postanal tails, atrial walls, and also between the chordates' dorsal notochord and the enteropneusts' posteroventral pygochord. Significantly, positional homology between notochord and pygochord is also supported by the expression domains of Brachyury orthologs in vertebrates and invertebrates: a Brachyury ortholog is active in the posteroventral mesoderm in Drosophila and in the dorsral mesoderm in chordates. In conclusion, we propose that the anatomy of enteropneusts may serve as a conceptual 'missing link' between gastroneuralian invertebrates and notoneuralian chordates. We discuss whether the enteropneust's dorsoanterior nervous centre plus their ventral trunk cord then corresponds to brain and dosal nerve cord in the chordata.
Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates.
Arendt, D. & Nubler-Jung, K.
Mech Dev. 1997 Jan;61(1-2):7-21.
The idea that chordates, during their evolution, have inverted their dorsoventral body axis has recently gained substantial support. It has been shown that various dorsoventral patterning genes that are evolutionarily conserved between insects and vertebrates are expressed dorsally in insects, and ventrally in vertebrates, or vice versa. The ventral body side of insects thus seems to correspond to the dorsal body side of vertebrates, and these are nerve cord-bearing, neural body sides in both groups. In order to exclude that the inverted polarity of gene patterning activity is purely accidental, we compare here vertebrate and invertebrate blastula fate maps and their gastrulation patterns in the framework of early gene expression. From this comparison it appears that the neural body sides, 'ventral' in annelids or arthropods, and 'dorsal' in chordates, develop at similar positions with respect to the initial egg asymmetry. In addition, the formation of the neural body sides involves similar movements during gastrulation. We further suggest that the deuterostome gastrulation seen in today's chordates can be derived from a more ancestral gastrulation pattern seen in today's annelids and arthropods, and that the ventral midline cells of insects correspond to the dorsal midline cells of vertebrates.
Enteropneusts and chordate evolution.
Nübler-Jung, K. & Arendt, D.
Curr Biol. 1996 Apr 1;6(4):352-3. Europe PMC
Common ground plans in early brain development in mice and flies.
Arendt, D. & Nubler-Jung, K.
Bioessays. 1996 Mar;18(3):255-9.
Comparing expression patterns of orthologous genes between insects and vertebrates, we have recently proposed that the ventral nerve cord in insects may correspond to the dorsal nerve cord in vertebrates. Here we show that the early development of the insect and vertebrate brain anlagen is indeed very similar. Insect and vertebrate brains express similar sets of genes in comparable areas with similar functions in the adult. In addition, early axogenesis establishes surprisingly similar patterns of axonal connectivity in both groups. We therefore propose that insect and vertebrate brains are built according to a common ground plan, and that specific areas of the insect and vertebrate brains be considered as homologous, meaning that these areas already existed, with their specific functions, in their common ancestor.
Inversion of dorsoventral axis?
Arendt, D. & Nubler-Jung, K.
Nature 1994 Sep 1;371(6492):26. Europe PMC
Blocked endocytotic uptake by the oocyte causes accumulation of vitellogenins in the haemolymph of the female-sterile mutants quitPX61 and stand stillPS34 of Drosophila.
Gutzeit, H.O. & Arendt, D.
Cell Tissue Res. 1994 Feb;275(2):291-8.
The developmental lesions in two female-sterile mutants, quitPX61 (qui) and stand stillPS34 (stil), of Drosophila have been analysed. Previtellogenic development is normal in mutant qui ovarioles but, during vitellogenic stages, only small quantities of yolk accumulate in the oocyte. The nurse-cell cytoplasm does not stream into the oocyte. However, the follicle cells continue their developmental program and synthesize an excessive quantity of eggshell material. In the mutant stil, the oocyte remains small and contains only a fraction of the yolk proteins present in wild-type follicles. Histological and ultrastructural observations and the failure to incorporate trypan blue indicate that the yolk proteins present in the mutant follicles are neither derived from the fat body nor from the follicle cells. Since, in both mutants, the uptake mechanism of vitellogenin is affected, the 3 polypeptides accumulate in the haemolymph (in stil, the protein concentration is up to 4 times higher than in wild-type females) and the haemolymph volume increases. Reciprocal transplantations of ovarioles show that the developmental lesions in both mutants are ovary-autonomous. Furthermore, genetic chimeras of stil show that the activity of the stil gene is required in the germline cells and not in the somatic tissues.
Is ventral in insects dorsal in vertebrates? A history of embryological arguments favouring axis inversion in chordate ancestors. Roux's Arch
Nübler-Jung, K. and Arendt, D. (1994).
Roux's Arch. Dev. Biol. 203, 357-366
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