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The Toll signaling pathway is the main source of embryonic DV polarity in the fly Drosophila melanogaster. This pathway appears to have been co-opted from an ancestral innate immunity system within the insects and has been deployed in different ways among insect taxa. Here we report the expression and function of homologs of the important components of the D. melanogaster Toll pathway in the wasp Nasonia vitripennis. We found homologs for all the components; many components had one or more additional paralogs in the wasp relative the fly. We also found significant deviations in expression patterns of N. vitripennis homologs. Finally, we provide some preliminary functional analyses of the N. vitripennis homologs, where we find a mixture of conservation and divergence of function.

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Dorsoventral pattering relies on Toll and BMP signalling in all insects studied so far, with variations in the relative contributions of both pathways. Drosophila and the beetle Tribolium share extensive dependence on Toll, while representatives of more distantly related lineages like the wasp Nasonia and bug Oncopeltus rely more strongly on BMP signalling. Here, we show that in the cricket Gryllus bimaculatus, an evolutionarily distant outgroup, Toll has, like in Drosophila, a direct patterning role for the ventral half of the embryo. In addition, Toll polarises BMP signalling, although this does not involve the conserved BMP inhibitor Sog/Chordin. Finally, Toll activation relies on ovarian patterning mechanisms with striking similarity to Drosophila. Our data suggest two surprising hypotheses: (1) that Toll's patterning function in Gryllus and Drosophila is the result of convergent evolution or (2) a Drosophila-like system arose early in insect evolution and was extensively altered in multiple independent lineages.

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BACKGROUND: Gene regulatory networks (GRNs) underlie developmental patterning and morphogenetic processes, and changes in the interactions within the underlying GRNs are a major driver of evolutionary processes. In order to make meaningful comparisons that can provide significant insights into the evolution of regulatory networks, homologous networks from multiple taxa must be deeply characterized. One of the most thoroughly characterized GRNs is the dorsoventral (DV) patterning system of the Drosophila melanogaster embryo. We have developed the wasp Nasonia as a comparative DV patterning model because it has shown the convergent evolution of a mode of early embryonic patterning very similar to that of the fly, and it is of interest to know whether the similarity at the gross level also extends to the molecular level. RESULTS: We used RNAi to dorsalize and ventralize Nasonia embryos, RNAseq to quantify transcriptome-wide expression levels, and differential expression analysis to identify genes whose expression levels change in either RNAi case. This led to the identification of >100 genes differentially expressed and regulated along the DV axis. Only a handful of these genes are shared DV components in both fly and wasp. Many of those unique to Nasonia are cytoskeletal and adhesion molecules, which may be related to the divergent cell and tissue behavior observed at gastrulation. In addition, many transcription factors and signaling components are only DV regulated in Nasonia, likely reflecting the divergent upstream patterning mechanisms involved in producing the conserved pattern of cell fates observed at gastrulation. Finally, several genes that lack Drosophila orthologs show robust and distinct expression patterns. These include genes with vertebrate homologs that have been lost in the fly lineage, genes that are found only among Hymenoptera, and several genes that entered the Nasonia genome through lateral transfer from endosymbiotic bacteria. CONCLUSIONS: Altogether, our results provide insights into how GRNs respond to new functional demands and how they can incorporate novel components.

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In Drosophila, Toll signaling leads to a gradient of nuclear uptake of Dorsal with a peak at the ventral egg pole and is the source for dorsoventral (DV) patterning and polarity of the embryo. In contrast, Toll signaling plays no role in embryonic patterning in most animals, while BMP signaling plays the major role. In order to understand the origin of the novelty of the Drosophila system, we have examined DV patterning in Nasonia vitripennis (Nv), a representative of the Hymenoptera and thus the most ancient branch points within the Holometabola. We have previously shown that while the expression of several conserved DV patterning genes is almost identical in Nasonia and Drosophila embryos at the onset of gastrulation, the ways these patterns evolve in early embryogenesis are very different from what is seen in Drosophila or the beetle Tribolium. In contrast to Drosophila or Tribolium, we find that wasp Toll has a very limited ventral role, whereas BMP is required for almost all DV polarity of the embryo, and these two signaling systems act independently of each other to generate DV polarity. This result gives insights into how the Toll pathway could have usurped a BMP-based DV patterning system in insects. In addition, our work strongly suggests that a novel system for BMP activity gradient formation must be employed in the wasp, since orthologs of crucial components of the fly system are either missing entirely or lack function in the embryo.

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The transforming growth factor beta (TGF)-ß signaling pathway and its modulators are involved in many aspects of cellular growth and differentiation in all metazoa. Although most of the core components of the pathway are highly conserved, many lineage-specific adaptations have been observed including changes regarding paralog number, presence and absence of modulators, and functional relevance for particular processes. In the parasitic jewel wasp Nasonia vitripennis, the bone morphogenetic proteins (BMPs), one of the major subgroups of the TGF-ß superfamily, play a more fundamental role in dorsoventral (DV) patterning than in all other insects studied so far. However, Nasonia lacks the BMP antagonist Short gastrulation (Sog)/chordin, which is essential for polarizing the BMP gradient along the DV axis in most bilaterian animals. Here, we present a broad survey of TGF-ß signaling in Nasonia with the aim to detect other lineage-specific peculiarities and to identify potential mechanisms, which explain how BMP-dependent DV pattering occurs in the early Nasonia embryo in the absence of Sog.

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Regulatory networks composed of interacting genes are responsible for pattern formation and cell type specification in a wide variety of developmental contexts. Evolution must act on these regulatory networks in order to change the proportions, distribution, and characteristics of specified cells. Thus, understanding how these networks operate in homologous systems across multiple levels of phylogenetic divergence is critical for understanding the evolution of developmental systems. Among the most thoroughly characterized regulatory networks is the dorsal-ventral patterning system of the fly Drosophila melanogaster. Due to the thorough understanding of this system, it is an ideal starting point for comparative analyses. Here we report an analysis of the DV patterning system of the wasp, Nasonia vitripennis. This wasp undergoes a mode of long germ embryogenesis that is superficially nearly identical to that of Drosophila, but one that was likely independently derived. We have found that while the expression of genes just prior to the onset of gastrulation is almost identical in Nasonia and Drosophila, both the upstream network responsible for generating this pattern, and the downstream morphogenetic movements that it sets in motion, are significantly diverged. From this we conclude that many network structures are available to evolution to achieve particular developmental ends.

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The establishment of the germline is a critical, yet surprisingly evolutionarily labile, event in the development of sexually reproducing animals. In the fly Drosophila, germ cells acquire their fate early during development through the inheritance of the germ plasm, a specialized maternal cytoplasm localized at the posterior pole of the oocyte. The gene oskar (osk) is both necessary and sufficient for assembling this substance. Both maternal germ plasm and oskar are evolutionary novelties within the insects, as the germline is specified by zygotic induction in basally branching insects, and osk has until now only been detected in dipterans. In order to understand the origin of these evolutionary novelties, we used comparative genomics, parental RNAi, and gene expression analyses in multiple insect species. We have found that the origin of osk and its role in specifying the germline coincided with the innovation of maternal germ plasm and pole cells at the base of the holometabolous insects and that losses of osk are correlated with changes in germline determination strategies within the Holometabola. Our results indicate that the invention of the novel gene osk was a key innovation that allowed the transition from the ancestral late zygotic mode of germline induction to a maternally controlled establishment of the germline found in many holometabolous insect species. We propose that the ancestral role of osk was to connect an upstream network ancestrally involved in mRNA localization and translational control to a downstream regulatory network ancestrally involved in executing the germ cell program.

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