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Molecular developmental analyses of animal larval development: searching for deep homology

Reference	BB/H006966/1
Principal Investigator / Supervisor	Professor Maximilian Telford
Co-Investigators / Co-Supervisors
Institution	University College London
Department	Genetics Evolution and Environment
Funding type	Research
Value (£)	592,597
Status	Completed
Type	Research Grant
Start date	01/03/2010
End date	31/08/2014
Duration	54 months

Abstract

Flatworms have a simple body plan and crucially lack body cavities, segmentation and a through gut; this simplicity meant they were long thought of as an early branch in metazoan evolution. Their inclusion in Lophotrochozoa alongside complex annelids and molluscs led to the inference that their simplicity must be secondarily evolved. Our first aim is to test this assumption by looking for genetic traces of a through-gut or for evidence of the primitiveness of their blind-ended gut in their embryos. We will look at expression of genes involved in mouth/anus patterning to understand the origins of these gut openings. The larvae of some platyhelminths resemble trochophore larvae common in marine annelids and molluscs. This controversial comparison is part of the argument over whether primary larvae within all Metazoa are homologous. The second aim is to establish or refute homology of platyhelminth and trochophore larvae. We will use two approaches: - Cell lineage analysis to see whether the ciliary band and apical organ of platyhelminth larvae are derived from the same blastomeres as their counterparts in trochophores. - Gene expression analysis to look for complex similarities, in terms of gene expression domains, between apical organs and ciliary bands of platyhelminth larvae and their supposed trochophoran homologs. We will use a relatively simple technique - in situ hybridisation - to determine the expression patterns of the target genes but will analyse the products of these experiments with state of the art methods for storing and aligning 3 dimensional expression patterns in a computer. This approach has been shown by one of our collaborators to allow cell specific comparisons of expression of all genes studied. Finally we will use EST sequence data (produced by 454 sequencing and also used for gene discovery) to refine our knowledge of the position of flatworms within the Lophotrochozoa

Summary

How animals evolve and adapt to their environment is a major theme of evolutionary biology. The patchy distribution of many complex characters (segmentation, coelomic cavities, eyes, central nervous system, etc.) across the animals could be interpreted in two ways: either as resulting from repeated convergent evolution of similar characters for adaptive reasons or as primitive characters that, while maintained in certain groups, have also been lost in multiple lineages. This proposal seeks to differentiate between these two scenarios for two important characters with a puzzling phylogenetic distribution amongst metazoan phyla: a through-gut and ciliated larvae. The platyhelminthes or flatworms are an important group of animals. Some are free living but others are important parasites such as tapeworms and schistosomes (the cause of Bilharzia which affects over 200 million people worldwide). They have a relatively simple body without a through gut (i.e. no separate mouth and anus) nor do they have the internal fluid filled cavities or segmented body plans seen in many other animal groups such as annelid worms (e.g. earth worms) or molluscs. For many years there was an assumption that their relative simplicity was an indication that they separated early from the main branches of the animal tree: many hundreds of millions of years ago and before the evolution of these more advanced traits. Recently it has been established that this view of their relationships to other animal groups is incorrect and that they are in fact relatively closely related to the annelids and molluscs in a large assemblage of animals called the Lophotrochozoa. This relationship implies that they originally possessed the through gut, body cavities and segments seen in their relatives but have lost them secondarily. We want to test this idea directly by looking for genetic traces of these characteristics in their larvae. The larvae of flatworms resemble, to an extent, the larvae of annelids and molluscs (a tiny ciliated swimming stage called a trochophore). We want to test, using genetic markers again, whether annelid, mollusc and flatworm larvae are in fact all inherited from a common ancestor (the progenitor of the Lophotrochozoa) that also had a larva. If so flatworm larvae would be expected to share specific genetic characteristics with the trochophore larvae of annelids and molluscs whereas if the larvae have been evolved independently in annelids and flatworms this would not be the case. This will tell us about the possibility of adding a larval stage into your lifecycle - a very controversial idea - and also inform us about the characteristics of the common ancestor of the lophotrochozoan animals which existed half a billion years ago. Finally we want to use the genetic data we generate in the parts of the project already described to refine our understanding of the evolutionary relationships between flatworms and all the other lophotrochozoan groups. An understanding of these relationships will better enable us to interpret the evolution of the characteristics that interest us.

Impact Summary

Beneficiaries within the public sector. I have a long-standing association with the Natural History Museum (I worked there for 6 years and since 2000 have been a Scientific Associate). The work we propose to undertake is into fundamental principles of metazoan evolution including phylogenetics of an important major clade of animals (Lophotrochozoa). This research into the patterns and processes of evolution are of direct relevance to the research of museum scientists and curators as well as being of obvious interest for inclusion in the museums exhibits. I am also a member of the council of the Linnean Society and of the Systematics association and the outputs of our research will similarly be of great interest to the membership of these societies. Beneficiaries within the wider public There is significant public interest in the understanding of Evolution. The planned research, while cutting edge science, is nevertheless readily explained to the public. Evolution is widely covered in newspapers and books, radio and television, and particularly so this year in the bicentenary of the birth of Charles Darwin. The UK is a leader in this field of research. I have been involved in a number of radio, television and newspaper interviews covering my research in the past (our research on the worm Xenoturbella was very widely covered and even made it into the Sunday telegraph A-Z of the year). In 2007 I took a significant part in a Radio 4 programme celebrating the 300th anniversary of the birth of Linneaus. In general I am keen to communicate my work and the broader aspects of evolutionary biology to the public by whatever means. Commercial private sector There are possibilities for exploitation of our research in the commercial sector. Maritigrella (the polyclad on which we work) is currently being studied by PharmaMar, a Spanish pharmaceutical company, interested in its ability to concentrate ecteinascidins a type of anti-tumor compound derived from its food source. We are in contact with this company and they are keen to have collaborate. We will provide early access to our EST data set which may aid them in gene discovery and longer term we would hope they will benefit from any advances we make in understanding the biology and in developing manipulation/culturing techniques for use on Maritigrella. Other practical/commercial work on Maritigrella has been undertaken by the aquaculture division of the Harbour branch oceanographic institute (we are in contact with John Scarpa and Amy Wright who were responsible for this research), again due to its potential importance as a source of anti-cancer compounds.

Committee	Research Committee A (Animal disease, health and welfare)
Research Topics	X – not assigned to a current Research Topic
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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