Maternal co-ordinate gene regulation and axis polarity in the scuttle fly Megaselia abdita

Axis specification and segment determination in dipteran insects are an excellent model system for comparative analyses of gene network evolution. Antero-posterior polarity of the embryo is established through systems of maternal morphogen gradients. In Drosophila melanogaster, the anterior system acts through opposing gradients of Bicoid (Bcd) and Caudal (Cad), while the posterior system involves Nanos (Nos) and Hunchback (Hb) protein. These systems act redundantly. Both Bcd and Hb need to be eliminated to cause a complete loss of polarity resulting in mirror-duplicated abdomens, so-called bicaudal phenotypes. In contrast, knock-down of bcd alone is sufficient to induce double abdomens in non-drosophilid cyclorrhaphan dipterans such as the hoverfly Episyrphus balteatus or the scuttle fly Megaselia abdita. We investigate conserved and divergent aspects of axis specification in the cyclorrhaphan lineage through a detailed study of the establishment and regulatory effect of maternal gradients in M. abdita. Our results show that the function of the anterior maternal system is highly conserved in this species, despite the loss of maternal cad expression. In contrast, hb does not activate gap genes in this species. The absence of this activatory role provides a precise genetic explanation for the loss of polarity upon bcd knock-down in M. abdita, and suggests a general scenario in which the posterior maternal system is increasingly replaced by the anterior one during the evolution of the cyclorrhaphan dipteran lineage.This study was funded by the MEC-EMBL agreement for the EMBL/CRG Research Unit in Systems Biology, AGAUR SGR Grant 406 (http:// www10.gencat.cat/agaur_web), as well as grants BFU2009-10184 and BFU2012-33775 from MINECO (formerly MICINN; http://www.idi.mineco.gob.es). The Centre for Genomic Regulation (CRG) acknowledges support from MINECO, ‘Centro de Excelencia Severo Ochoa 2013-2017’, SEV-2012-0208. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript