The evolution of developmental programs : a case study in the gastropod mollusc Patella vulgata

Abstract

At the interface between evolutionary biology and developmental biology is the so-called field of evolutionary developmental biology (‘evo-devo’ in short). This field asks how different adult animals (species) came into being by heritable changes during their embryonic development. One way to study this question is a comparative analysis of genes that are important for the development of different species. Many genes appear to be conserved during evolution, i.e. the same gene can have a comparable role during the development of very different species. This developmental genetic unity underlying very different animals has puzzled evolutionists as well as developmental biologists. It has led to two main questions: -what aspects of gene function can be considered as conserved, thus evolutionary very ancient, perhaps even ancestral to metazoans (or bilaterians)? -how can such different animals be generated from such similar sets of genes? This study is involved with the phylum Mollusca (snails, slugs, octopuses and the like). Very little is known on the genetics of early development of molluscs. Data on the role of genes during the development of molluscan animals, therefore, is likely to provide new insights and will contribute to answering the abovementioned questions. The study organism of this thesis is the gastropod mollusk Patella vulgata. Orthologs (gene homologs) of seven genes are described: snail, twist, orthodenticle, orthopedia, engrailed, dpp en hedgehog. The question asked is in this thesis is: what insights do we obtain when we broaden our comparative analysis of the role developmental genes play to molluscs? The research on these seven genes has given a number of new insights. One is a better understanding on what role of these genes has been conserved during evolution. It is very likely that the common evolutionary ancestor to all animals already had these genes with these particular functions. Despite the fact that many animals have genes in common, often with the same function, not all animals are alike. The research described in this thesis contributed to our understanding of this apparent paradox. A gene can have a certain function, which allows it to contribute to the development of very different structures or organs. For example, the engrailed gene is involved in generating boundaries between groups of cells. During development, cells expressing the engrailed gene form a compartment excluding other, neighbouring cells that form another compartment (and do not express engrailed). Both compartments become different parts of the adult organism. In the fruitfly, for example, engrailed plays a role in boundary formation between segments, the ‘building blocks’ of the body of the fly. But also in molluscs, such as Patella, engrailed is involved in boundary formation, namely between cells that form the shell and the surrounding cells that do not contribute to shell formation. The fact that such very different structures such as segments in flies and shells in snails use the same gene for their formation can thus be explained by the fact that engrailed is a ‘boundary formation’ gene. This is the way evolution creates different animals from the same set of genes: by recombining similar building blocks in new ways, new structures can be formed, a phenomenon called ‘tinkering’ (or ‘bricolage’).