Abstract

In Drosophila, all body segments are patterned in the embryonic blastoderm prior to gastrulation, via the action of a cascade of maternal, gap, pair-rule and segment-polarity genes. This textbook paradigm for insect segmentation is evolutionary derived. Ancestrally in insects, only anterior body segments were patterned in the blastoderm, with posterior (i.e. abdominal) segments forming after gastrulation, in the context of a cellularized and extending germband. I have previously argued that the evolution of the Drosophila segmentation paradigm required distinct evolutionary transitions to occur at either pole of the egg (Peel, 2008; Peel & Akam, 2003): at the anterior pole, the establishment of a secondary patterning centre as a prerequisite for an anterior shift in the embryonic fate map within the egg, and at the posterior pole, the recruitment of gap genes to drive stripes of pair-rule gene expression that ancestrally formed later, sequentially, and under the temporal control of an insect segmentation clock, similar to that operating in vertebrate somitogenesis. I will present recent data from the emerging model beetle Tribolium castaneum that support these evolutionary hypotheses: In Tribolium, maternal mRNAs are localized to the anterior pole in a microtubule dependent manner, similar to Drosophila, despite the patterning of anterior (i.e. head and trunk) segments in the posterior half of the blastoderm. Secondly, during the sequential formation of abdominal segments, pair-rule gene homologues oscillate in their expression, with a two-segment periodicity, supporting their involvement in a Tribolium segmentation clock. I will argue that Tribolium might represent an intermediate stage in the evolution of the Drosophila segmentation paradigm, and that recent data from this, as well as other holometabolous insects, highlights the important role genetic cooption has played in the evolution of developmental gene networks.