Gastrulation constitutes a fundamental yet diverse morphogenetic process of metazoan development. Modes of gastrulation range from stochastic translocation of individual cells to coordinated infolding of an epithelial sheet. How such morphogenetic differences are genetically encoded and whether they have provided specific developmental advantages is unclear. Here we identify two genes, folded gastrulation and t48, which in the evolution of fly gastrulation acted as a likely switch from an ingression of individual cells to the invagination of the blastoderm epithelium. Both genes are expressed and required for mesoderm invagination in the fruit fly Drosophila melanogaster but do not appear during mesoderm ingression of the midge Chironomus riparius. We demonstrate that early expression of either or both of these genes in C.riparius is sufficient to invoke mesoderm invagination similar to D.melanogaster. The possible genetic simplicity and a measurable increase in developmental robustness might explain repeated evolution of similar transitions in animal gastrulation.DOI: http://dx.doi.org/10.7554/eLife.18318.001

To understand how and when developmental traits of the fruit fly Drosophila melanogaster originated during the course of insect evolution, similar traits are functionally studied in variably related satellite species. The experimental toolkit available for relevant fly models typically comprises gene expression and loss as well as gain-of-function analyses. Here, we extend the set of available molecular tools to piggyBac-based germ line transformation in two satellite fly models, Megaselia abdita and Chironomus riparius. As proof-of-concept application, we used a Gateway variant of the piggyBac transposon vector pBac{3xP3-eGFPafm} to generate a transgenic line that expresses His2Av-mCherry as fluorescent nuclear reporter ubiquitously in the gastrulating embryo of M. abdita. Our results open two phylogenetically important nodes of the insect order Diptera for advanced developmental evolutionary genetics.Electronic supplementary materialThe online version of this article (doi:10.1007/s00427-015-0504-5) contains supplementary material, which is available to authorized users.

Evolutionary novelty can be generally traced back to continuous changes rather than disruptive transformations, yet the sudden appearance of novel developmental traits is not well understood. Here we use the extraembryonic amnioserosa in Drosophila melanogaster as example for a suddenly and newly evolved epithelium, and we ask how this tissue originated by gradual transitions from its two ancestors, amnion and serosa. To address this question, we used in toto time-lapse recordings to analyze an intermediate mode of extraembryonic development in the scuttle fly Megaselia abdita. Our results suggest that the amnioserosa evolved by loss of serosa spreading without disrupting the developmental programs of serosa and amnion. Our findings imply that the Drosophila amnioserosa has retained properties of the ancient serosa and, more generally, indicate that non-autonomous interactions between tissues can be a compelling variable for the evolution of epithelial properties. Impact StatementThe Drosophila amnioserosa originated as a composite extraembryonic epithelium by loss of epithelial spreading and rather than changes in amnion or serosa tissue differentiation.

Extraembryonic tissues contribute to animal development, which often entails spreading over embryo or yolk. Apart from changes in cell shape, the requirements for this tissue spreading are not well understood. Here, we analyze spreading of the extraembryonic serosa in the scuttle fly Megaselia abdita. The serosa forms from a columnar blastoderm anlage, becomes a squamous epithelium, and eventually spreads over the embryo proper. We describe the dynamics of this process in long-term, whole-embryo time-lapse recordings, demonstrating that free serosa spreading is preceded by a prolonged pause in tissue expansion. Closer examination of this pause reveals mechanical coupling to the underlying yolk sac, which is later released. We find mechanical coupling prolonged and serosa spreading impaired after knockdown of M. abdita Matrix metalloprotease 1. We conclude that tissue–tissue interactions provide a critical functional element to constrain spreading epithelia.

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