Abstract
Segments are formed simultaneously in the blastoderm of the fly Drosophila melanogaster through a hierarchical cascade of interacting transcription factors. Conversely, in many insects and in all non-insect arthropods most segments are formed sequentially from the posterior. We have looked at segmentation in the milkweed bug Oncopeltus fasciatus. Posterior segments are formed sequentially, through what is probably the ancestral arthropod mechanism. Formation of anterior segments bears many similarities to the Drosophila segmentation mode. These segments appear nearly simultaneously in the blastoderm, via a segmentation cascade that involves orthologues of Drosophila gap genes working through a functionally similar mechanism. We suggest that simultaneous blastoderm segmentation evolved at or close to the origin of holometabolous insects, and formed the basis for the evolution of the segmentation mode seen in Drosophila. We discuss the changes in segmentation mechanisms throughout insect evolution, and suggest that the appearance of simultaneous segmentation as a novel feature of holometabolous insects may have contributed to the phenomenal success of this group.
Highlights
Insects are the most diverse taxon on the Earth and are characterized by a highly conserved body plan [1]
In order to understand how long germ development has evolved from short germ, we need to look for a species that is close enough to Holometabola and displays both sequential and simultaneous segmentation
In analysing the involvement of these genes in Oncopletus blastoderm segmentation, we show that it bears significant similarities to the blastoderm segmentation process in Drosophila, suggesting that simultaneous segmentation in the blastoderm evolved before the holometabolous radiation
Summary
Insects are the most diverse taxon on the Earth and are characterized by a highly conserved body plan [1]. Despite myriad variations in lifestyle, ecology and feeding, all insects have a segmented body divided into three distinct body regions (tagmata): a head composed of three pre-oral and three gnathal segments, a thorax composed of three leg-bearing segments, two of which usually bear wings, and an abdomen with 9–11 segments This conservation of general body plan masks a diversity of mechanisms employed to establish it during embryogenesis [2]. In order to understand how long germ development has evolved from short germ, we need to look for a species that is close enough to Holometabola and displays both sequential and simultaneous segmentation. The pair-rule gene even-skipped (eve) is expressed in an early broad domain in Drosophila and resolves to a pair-rule periodicity through clearing of intersegmental stripes In other arthropods, it has a key early role in generating a repeated pattern. In analysing the involvement of these genes in Oncopletus blastoderm segmentation, we show that it bears significant similarities to the blastoderm segmentation process in Drosophila, suggesting that simultaneous segmentation in the blastoderm evolved before the holometabolous radiation
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