Abstract
Morphogenesis involves the dynamic reorganization of cell and tissue shapes to create the three-dimensional body. Intriguingly, different species have evolved different morphogenetic processes to achieve the same general outcomes during embryonic development. How are meaningful comparisons between species made, and where do the differences lie? In this Perspective, we argue that examining the evolution of embryonic morphogenesis requires the simultaneous consideration of different levels of biological organization: (1) genes, (2) cells, (3) tissues, and (4) the entire egg, or other gestational context. To illustrate the importance of integrating these levels, we use the extraembryonic epithelia of insects—a lineage-specific innovation and evolutionary hotspot—as an exemplary case study. We discuss how recent functional data, primarily from RNAi experiments targeting the Hox3/Zen and U-shaped group transcription factors, provide insights into developmental processes at all four levels. Comparisons of these data from several species both challenge and inform our understanding of homology, in assessing how the process of epithelial morphogenesis has itself evolved.
Highlights
In the rapidly developing fruit fly Drosophila melanogaster, the predominant insect model for developmental genetics, embryonic morphogenesis occurs largely after cell fates are determined
We show that the insect EE epithelia provide a case study with a rich evolutionary history, making them well suited to assessing the evolution of morphogenesis
While differences in tissue organization are expected between dorsal closure involving an amnioserosa and dorsal closure involving a serosa and amnion, we find differences between species with both EE membranes (Figure 1: “most insects” schematic)
Summary
In the rapidly developing fruit fly Drosophila melanogaster, the predominant insect model for developmental genetics, embryonic morphogenesis occurs largely after cell fates are determined. Perhaps as a result of our profound knowledge in Drosophila, many evolutionary developmental (evo-devo) studies in arthropods take a gene-centered approach and focus on early patterning, as early fate specification is often a powerful signal for comparisons of species that are separated by long periods of evolutionary time (e.g., Peel et al, 2005; Sachs et al, 2015). In this Perspective article, we highlight the importance of studying the morphogenetic movements that occur during animal development and of integrating multiple levels of biological organization when making interspecific comparisons. We show that the insect EE epithelia provide a case study with a rich evolutionary history, making them well suited to assessing the evolution of morphogenesis
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