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Priapulid Endomesoderm Development and Ecdysozoan Body Plan Evolution

Final Report Summary - PEMDEEV (Priapulid Endomesoderm Development and Ecdysozoan Body Plan Evolution)

All animals originate from a single cell that multiplies and gives rise to all their differentiated anatomical structures. This process is termed embryogenesis, and at one point involves the division of an undifferentiated mass of cells into three major tissue layers: the ectoderm (the external ‘skin’ of the embryo), the endoderm (the internal tissue), and the mesoderm (the cells that lie in between the ectoderm and the endoderm). Each of these germ layers will form a particular set of differentiated tissues, organs and structures. The ectoderm will form the skin and nervous system of the animal; the digestive system and associated glands will originate from the endoderm; and the mesoderm will give rise to connective tissues, muscles and skeleton, among others. In many aspects, the evolution of the astonishing diversity of animal body plans can be related to changes in the way the segregation and patterning of these primary germ layers occurs during embryogenesis.

One such case of changes in the development of the germ layers is observed in the group of animals called Ecdysozoa, which comprises organisms as different as insects, spiders, velvet worms and round worms, and the two most relevant invertebrate biomedical and developmental model systems, namely the fruit fly Drosophila melanogaster and the nematode worm Caenorhabditis elegans. All these organisms exhibit a great diversity in the way the germ layers form during embryogenesis, and in particular, in the way the endoderm gets specified. For instance, D. melanogaster forms the endoderm in two opposing regions of the embryo, which then get internalized and migrate internally until they meet in the center of the embryo. On the other hand, C. elegans develops the whole digestive system from one single endodermal cell, which originates already when the embryo consists of only 8 cells. Despite being some of the most studied animals, how these disparate modes of endoderm formation evolved, and how changes in these early developmental events relate to the appearance of the tremendously different digestive systems of D. melanogaster and C. elegans is still unclear.

Priapulid worms, commonly referred to as ‘penis worms’, are an enigmatic group of vermiform animals, with only 19 species described. Members of the Ecdysozoa, they were among the most abundant animals in the Cambrian, when they were already morphologically similar to the known extant species. Thus regarded as living fossils, priapulid worms have recently emerged as a key animal group to understand the early evolution of ecdysozoan animals. However, they have been largely neglected in developmental and evolutionary studies. In 2012, the first comprehensive morphological description of the embryonic development of the priapulid worm Priapulus caudatus came out. This study demonstrated that priapulid worms form the primary germ layers and establish the basic organization of the digestive system as it likely happened in the ancestor to all bilaterally symmetrical animals.

The goal of this Marie Curie Intra-European Fellowship (IEF) was to advance in our understanding of the earliest events of the embryonic development of P. caudatus, and in particular of the specification and subsequent differentiation of the endoderm. The implementation of the proposed research project resulted in a detailed morphological description of the process of endoderm formation and differentiation, in particular in relation to mesoderm development. In order to better understand the genetic underpinnings of this event, I characterized the expression domains of an extensive set of endo- and mesodermal-related genes. This allowed me to demonstrate that the digestive system forms from a small population of cells located at the posterior pole of the embryo before gastrulation. Most importantly, I could show that the subsequent development of the endoderm into a functional digestive tract involved the establishment of a molecular patterning highly similar to the one observed in other ecdysozoan taxa, in particular D. melanogaster and C. elegans. Taking advantage of the vast diversity of animals that my host laboratory has in culture, I extended my investigations into other related invertebrate groups, namely brachiopods, nemerteans, annelids, and bryozoans. All these investigations delivered a comprehensive view of the evolution of the endoderm, of its specification, and its patterning into a functional gut. Additionally, I established international collaborations that helped uncovering the peculiar morphology of the early nervous system of priapulid worms and the evolutionary history of the Nodal signaling pathway in animals.

The execution of the research plan of this IEF grant has significantly contributed to the establishment of priapulid worms as a tractable organism for developmental and evolutionary studies. Moreover, it has shown how comparative analysis can shed light into the evolution of the Ecdysozoa, which is in turn critical for comparisons between the two most prominent invertebrate model systems (D. melanogaster and C. elegans) and their vertebrate counterparts. In a broader context, the implementation of the research plan has had a profound impact in establishing me as a more rounded researcher, improving my independence and leadership skills. This IEF fellowship has enhanced my visibility and strengthened my contacts with other European researchers and groups worldwide. I have also taken special care in outreaching my research through regular contributions with online podcasts, which has allowed me to learn how effectively communicate science to a broad non-expert audience. All things considered, I have successfully achieved the goals proposed in this IEF grant, thus contributing to the scientific output and strategic objectives of the European Research Area.