Abstract
BackgroundOne of the best studied developmental processes is the Drosophila segmentation cascade. However, this cascade is generally considered to be highly derived and unusual, with segments being patterned simultaneously, rather than the ancestral sequential segmentation mode. We present a detailed analysis of the segmentation cascade of the milkweed bug Oncopletus fasciatus, an insect with a more primitive segmentation mode, as a comparison to Drosophila, with the aim of reconstructing the evolution of insect segmentation modes.ResultsWe document the expression of 12 genes, representing different phases in the segmentation process. Using double staining we reconstruct the spatio-temporal relationships among these genes. We then show knock-down phenotypes of representative genes in order to uncover their roles and position in the cascade.ConclusionsWe conclude that sequential segmentation in the Oncopeltus germband includes three slightly overlapping phases: Primary pair-rule genes generate the first segmental gene expression in the anterior growth zone. This pattern is carried anteriorly by a series of secondary pair-rule genes, expressed in the transition between the growth zone and the segmented germband. Segment polarity genes are expressed in the segmented germband with conserved relationships. Unlike most holometabolous insects, this process generates a single-segment periodicity, and does not have a double-segment pattern at any stage. We suggest that the evolutionary transition to double-segment patterning lies in mutually exclusive expression patterns of secondary pair-rule genes. The fact that many aspects of the putative Oncopeltus segmentation network are similar to those of Drosophila, is consistent with a simple transition between sequential and simultaneous segmentation.
Highlights
One of the best studied developmental processes is the Drosophila segmentation cascade
To facilitate inter-species comparison, we only report on genes that are orthologs of genes involved in the segmentation cascade of Drosophila, realizing that this does not give the full picture, as there may be other genes involved in segmentation in Oncopeltus that do not have such a role in Drosophila [18, 19]
Following striped expression of eve, several other genes are expressed in a similar domain, including at least odd, sob and hh. Based on their spatial relationships we suggest that these genes are activated by eve, but we cannot test this functionally since knocking down eve leads to a complete truncation of the growth zone and sequential segmentation does not take place
Summary
One of the best studied developmental processes is the Drosophila segmentation cascade. This cascade is generally considered to be highly derived and unusual, with segments being patterned simultaneously, rather than the ancestral sequential segmentation mode. A defining feature of the arthropod body plan is its segmental organization. The formation of segments occurs very differently in different groups of arthropods. While there is no doubt that segments are homologous among all arthropods, when looking across their full phylogenetic spread, there is relatively little in common in the segmentation process. The segmentation process has been best studied in the fruit fly Drosophila melanogaster [2].
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