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While the mRNA expression patterns of homeotic genes have been examined in numerous arthropod species, data on their protein accumulation is extremely limited. To address this gap, we analyzed the protein expression pattern of the hox gene Sex combs reduced (Scr) in six hemimetabolous insects from four divergent orders (Thysanura, Orthoptera, Dictyoptera and Hemiptera). Our comparative analysis reveals that the original domain of SCR expression was likely confined to the head and then subsequently moved into the prothorax (T1) in winged insect lineages. The data also show a trend toward the posteriorization of the anterior boundary of SCR expression in the head, which starts in the mandibles (Thysanura) and then gradually shifts to the maxillary (Orthoptera) and labial segments (Dictyoptera and Hemiptera), respectively. In Thermobia (firebrat) and Oncopeltus (milkweed bug) we also identify instances where SCR protein is not detected in regions where mRNA is expressed. This finding suggests the presence of a post-transcriptional regulatory mechanism of Scr in these species. Finally, we show that SCR expression in insect T1 legs is highly variable and exhibits divergent patterning even among related species. In addition, signal in the prothoracic legs of more basal insect lineages cannot be associated with any T1 specific features, indicating that the acquisition of SCR in this region preceded any apparent gain of function. Overall, our results show that Scr expression has diverged considerably among hemimetabolous lineages and establish a framework for subsequent analyses to determine its role in the evolution of the insect head and prothorax.

Evolving expression patterns of the homeotic gene Scr in insects