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Background  The heads of annelids (earthworms, polychaetes, and others) and arthropods (insects, myriapods, spiders, and others) and the arthropod-related onychophorans (velvet worms) show similar brain architecture and for this reason have long been considered homologous. However, this view is challenged by the 'new phylogeny' placing arthropods and annelids into distinct superphyla, Ecdysozoa and Lophotrochozoa, together with many other phyla lacking elaborate heads or brains. To compare the organisation of annelid and arthropod heads and brains at the molecular level, we investigated head regionalisation genes in various groups. Regionalisation genes subdivide developing animals into molecular regions and can be used to align head regions between remote animal phyla.    Results  We find that in the marine annelid  Platynereis dumerilii , expression of the homeobox gene  six3  defines the apical region of the larval body, peripherally overlapping the equatorial  otx+  expression. The  six3+  and  otx+  regions thus define the developing head in anterior-to-posterior sequence. In another annelid, the earthworm  Pristina , as well as in the onychophoran  Euperipatoides , the centipede  Strigamia  and the insects  Tribolium  and  Drosophila , a  six3/optix+  region likewise demarcates the tip of the developing animal, followed by a more posterior  otx/otd+  region. Identification of  six3 + head neuroectoderm in  Drosophila  reveals that this region gives rise to median neurosecretory brain parts, as is also the case in annelids. In insects, onychophorans and  Platynereis , the  otx+  region instead harbours the eye anlagen, which thus occupy a more posterior position.    Conclusions  These observations indicate that the annelid, onychophoran and arthropod head develops from a conserved anterior-posterior sequence of  six3+  and  otx+  regions. The  six3+  anterior pole of the arthropod head and brain accordingly lies in an anterior-median embryonic region and, in consequence, the optic lobes do not represent the tip of the neuraxis. These results support the hypothesis that the last common ancestor of annelids and arthropods already possessed neurosecretory centres in the most anterior region of the brain. In light of its broad evolutionary conservation in protostomes and, as previously shown, in deuterostomes, the  six3 - otx  head patterning system may be universal to bilaterian animals.

Six3 demarcates the anterior-most developing brain region in bilaterian animals