Animal segmentation

Participants

Michaël Akam, Guillaume Balavoine, Mary-Lee Dequéant, Denis Duboule, Albert Golbeter, Achim Gossler, David Ish-Horowicz, Ryoichiro Kageyama, Julian Lewis, Nipam Patel, Scott Poethig, Olivier Pourquié (Organiser), Yumiko Saga, Claudio Stern, Yoshiko Takahashi, Hiroyuki Takeda, Diethard Tautz, Peter Turpenny

Review

Animal Segmentation
by Olivier Pourquié
22-27 September 2005

The review of this meeting is written in French (see below) but you can read hereafter some titles of talks as well as some titles of articles given par their authors during the meeting:

Some titles of talks:

* Nipam Patel: Segmentation in the crustacean, Parhyale hawaiensis

* Michael Akam: Comparative studies of segmentation and segment specification in arthropods

* Diethard Tautz: Evolution of segmentation

* Scott Poethig: A role for miRNAs and trans-acting siRNAs in the temporal regulation of segment identity in plants

* Hiroyuki Takeda: Collective behavior of hairy oscillators in zebrafish

* Claudio Stem: Establishment of mesodermal pattern: from gastrulation to somites to vertebrae

* Albert Goldbeter: Modeling the segmentation dock: oscillations and bistability

* Olivier Pourquié: Segmental patterning of the vertebral axis

* Yoshiko Takahashi: Boundary formation and directed migration of cells during somitogenesis

* Yumiko Saga: Mesp2: the function and the regulation

* Peter Turnpenny: Abnormal vertebral segmentation in man

* David Ish-Horowicz: Studies in Notch signaling and segmentation

* Julian Lewis: The zebrafish somite segmentation clock: theory and experiments

* Mary-Lee Dequeant: Identification of new cyclic genes by a microarray approach

* Ryoichiro Kageyama: Molecular dissection of Hes 1/Hes7 oscillations

* Achim Gossler: Regulation of Notch activity and requirement for cyclic Notch activation in the PSM

Some articles:

A Double Segment Periodicity Underlies Segment Generation in Centipede Development

Ariel D. Chipman,1* Wallace Arthur, 2 and Michael Akam 1

1 University Museum of Zoology
Downing Street – Cambridge C52 3EJ – United Kingdom

2 Department of Zoology, National University of Ireland, Galway
University Road – Galway – Ireland

Current Biology, Vol. 14, 1250-1255, July 27, 2004, ©2004 Elsevier Ltd. All rights reserved.        DOi 10.1016/j.cub.2004.07.026

Summary

The number of leg-bearing segments in centipedes varies extensively, between 15 and 191, and yet it is always odd [1,2]. This suggests that segment genera­tion in centipedes involves a stage with double seg­ment periodicity and that evolutionary variation in seg­ment number reflects the generation of these double segmentai units. However, previous studies have re­vealed no trace of this [3-5]. Here we report the ex­pression of two genes, an odd-skipped related gene (odrl) and a caudal homolog, that serve as markers for early steps of segmentformation in the geophilomorph centipede, Strigamia maritime. Dynamic expression of odrl around the proctodaeum resolves into a series of concentric rings, revealing a pattern of double seg­ment periodicity in overtly unsegmented tissue. Ini­tially, the expression of the caudal homolog mirrors this double segment periodicity, but shortly before en­grailed expression and overt segmentation, the inter­calation of additional striges generates a repeat with single segment periodicity. Our results provide the first Glues about the causality of the unique and fascinating “all-odd” pattern of variation in centipede segment numbers and have implications for the evolution of the mechanisms of arthropod segmentation.

Early development and segment formation in the centipede, Strigamia maritima (Geophilomorpha)

Ariel D. Chipman,(a)* Wallace Arthur,(b) and Michael Akam,(a)

aLaboratory for Development and Evolution, University Museum of Zoology, Department of Zoology, Downing Street, Cambridge CB2 3EJ, UK

blntegrative Biology Group, University of Sunderland, Chester Road Campus, Sunderland SR1 3SD, UK

EVOLUTION & DEVELOPMENT 6:2, 78-89 (2004)

Summary

Geophilomorph centipedes exhibit a number of unique characteristics that make them of particular develop­mental and evolutionary interest. Segment numbers in geo­philomorphs are higher than in any other centipedes, ranging from 27 to 191. They may be constant within a species, pre­senting in extreme form the “counting” problem in develop­ment, or they may vary—a situation that provides us with the opportunity to study naturally occurring variation in segment numbers. All their segments are generated during embryo­genesis, a situation unlike that in the more basal centipede orders, which generate only a fraction of their 15 trunk segments in the embryo and develop the rest postembryon­ically. Here we provide a foundation for further develop­mental studies of the Geophilomorpha, building on the one study that has been conducted to date, on the coastal species Strigamia maritima. Development begins with the migration of nuclei to the surface of the egg, which then condense to form an embryonic rudiment of more than 20,000 cells, covering an entire hemisphere. During early development, the embryo can be divided into two distinct areas: a large terminal disc of apparently undifferentiated tissue and the germ-band, which has a clear anteroposterior axis and differentiated segments. The germ-band forms from the anterior of the terminal disc and extends anteriorly as the disc contracts. New segments are formed at the posterior margin of the germ-band. Once the process of segmentation ends, the germ-band folds and sinks into the yolk. We note that the classic description of centipede development, by Heymons more than a century ago, contains a fundamental error in the identification of the axes and hence in the interpretation of early segmentation.

Evolution of Segmentation: Rolling Back the Clock

Andrew Peel and Michael Akam

Current Biology, Vol. 13, R708—R710, September 16, 2003, ©2003 Elsevier Science Ltd. Ail rights reserved. DOI 10.1016/S0960-9822(03)00647-X

Recent work has revealed striking similarities in the genetic mechanisms underpinning somitogenesis in zebrafish and segmentation in the spider. Could this mean that the bilaterian common ancestor was segmented after all?

Mechanisms of germ cell specification across the metazoans: epigenesis and preformation

Cassandre G. Extavour* and Michael Akam

Laboratory for Development and Evolution, University Museum of Zoology, Department of Zoology, Downing Street, Cambridge CB2 3EJ, UK

Development 130, 5869-5884 D 2003 The Company of Biologists Ltd doi:10.1242/dev.00804

Summary

Germ cells play a unique role in gamete production, heredity and evolution. Therefore, to understand the mechanisms that specify germ cells is a central challenge in developmental and evolutionary biology. Data from model organisms show that germ cells can be specified either by maternally inherited determinants (preformation) or by inductive signals (epigenesis). Here we review existing data on 28 metazoan phyla, which indicate that although preformation is seen in most model organisms, it is actually the less prevalent mode of germ cell specification, and that epigenetic germ cell specification may be ancestral to the Metazoa.

 

Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic

Charles E. Cook 1(1) (1), Qiaoyun Yue (2) and Michael Akam (1)

(1) Department and Museum of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3E,7, UK

(2) Pedobiologia, Shanghai Institute of Entornology, Chinese Academy of Sciences, 225 Chongqing(S), Shanghai 200025, People’s Republic of China

Proc. R. Soc. B (2005) 272, 1295-1304 doi:10.1098/rspb.2004.3042  Published online 1 June 2005

For over a century the relationships between the four major groups of the phylum Arthropoda (Chelicerata, Crustacea, Hexapoda and Myriapoda) have been debated. Recent molecular evidence has confirmed a close relationship between the Crustacea and the Hexapoda, and has included the suggestion of a paraphyletic Hexapoda. To test this hypothesis we have sequenced the complete or near-complete mitochondrial genomes of three crustaceans (Parhyale hawaiensis, Squilla mantis and Triops longicaudatus), two collembolans (Onychiurus orientalis and Podura aquatica) and the insect Thermobia domestica. We observed rearrangement of transfer RNA genes only in O. orientalis, P. aquatica and P. hawaiensis. Of these, only the rearrangement in O. orientalis, an apparent autapomorphy for the collembolan family Onychiuridae, was phylogenetically informative.

We aligned the nuclear and amino acid sequences from the mitochondrial protein-encoding genes of these taxa with their homologues from other arthropod taxa for phylogenetic analysis. Our dataset contains many more Crustacea than previous molecular phylogenetic analyses of the arthropods. Neighbour­joining, maximum-likelihood and Bayesian posterior probabilities all suggest that crustaceans and hexapods are mutually paraphyletic. A crustacean clade of Malacostraca and Branchiopoda emerges as sister to the Insecta sensu stricto and the Collembola group with the maxillopod crustaceans. Some, but not all, analyses strongly support this mutual paraphyly but statistical tests do not reject the null hypotheses of a monophyletic Hexapoda or a monophyletic Crustacea. The dual monophyly of the Hexapoda and Crustacea has rarely been questioned in recent years but the idea of both groups’ paraphyly dates back to the nineteenth century. We suggest that the mutual paraphyly of bath groups should seriously be considered.

Keywords: Arthropoda; Hexapoda; mitochondria; genome; phylogeny; Pancrustacea

 

Review in French

La segmentation des animaux se traduit par l’arrangement périodique de structures anatomiques le long de l’axe antéro-postérieur du corps. Chez l’homme, l’aspect segmenté est particulièrement évident au niveau des vertèbres. L’aspect périodique de la colonne vertébrale est établi au cours du développement embryonnaire par la segmentation des somites.

Le colloque organisé à la Fondation des Treilles a réuni la plupart des meilleurs embryologistes venant d’Europe, d’Amérique ou du Japon et s’intéressant au problème de la segmentation. Le problème a été traité depuis les plantes jusqu’à l’homme. La question de la conservation de ce processus au cours de l’évolution a fait l’objet de plusieurs présentations mettant en évidence des similitudes jusqu’ici insoupçonnées entre la segmentation des arthropodes, des annélides et celles observées chez les vertébrés.

Le débat sur la conservation de la segmentation au cours de l’évolution remonte au début du 19e siècle et les résultats présentés au cours du colloque suggèrent qu’il pourrait être en passe d’être résolu.

La dissection des mécanismes impliqués dans les différentes étapes de la segmentation de plusieurs espèces de vertébrés a été largement débattue. L’apport des techniques modernes de la génomique à l’étude de ce problème a été présenté et plusieurs orateurs ont également abordé les aspects théoriques et la modélisation mathématique de ce processus.

Enfin, nous avons évoqué le problème de la régionalisation des structures segmentées au cours du développement aboutissant à la mise en place des grandes régions anatomiques du corps.

Le niveau des présentations était exceptionnel et les exposés ont donné lieu à d’excellentes discussions dans une atmosphère très détendue.

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