Bicoid protein is expressed at the anterior of the embryo (left), where it reinforces the expression of crocodile, a target of the Torso terminal pathway (right). Credit: Valérie Schaeffer and Ernst Wimmer.

When we think of Drosophila, it's often in terms of the genes and processes that it has in common with higher animals. The well scrutinized pathway of how a fly embryo tells its head from its tail (and everything inbetween) has laid the paradigm for the patterning function of morphogens in development. But it is puzzling that many other insects — never mind ourselves — don't undergo patterning in quite the same way. The fly uses two different pathways to specify the anterior tip of its head. Now Schaeffer et al. show that these two pathways, whose function in anterior development has been acquired recently in evolution, converge on similar targets and that removal of one of them can be compensated by boosting the other.

The Drosophila body plan is set up by the action of three sets of maternally contributed genes: the anterior, posterior and terminal systems. The terminal system requires local signalling through the torso (tor) receptor tyrosine kinase, which specifies the extreme tips of the head and tail. The anterior and posterior systems consist of localized mRNAs that, once translated, form gradients that regulate target genes in a concentration-dependent manner. The homeoprotein Bicoid is the most notable among the anterior-group genes, and embryos born to bcd− mothers lack a head, thorax and part of the abdomen.

Schaeffer et al. show that, in the anterior of the fly embryo, bcd and tor are part of two independent pathways that share common target genes. What's more, a deletion mutant of bcd that is expressed 3–4 times higher than the wild-type protein can rescue the phenotype of the tor pathway, to give embryos with normal anterior structures. Indeed, increased doses of wild-type Bicoid protein suffice to rescue the anterior defects of terminal-pathway mutants. This argues that one function of Tor is to potentiate the anterior system, as the rescue occurs by upregulating downstream targets, such as huckebein .

The additive effect of the terminal system on bcd had already been suspected: hypomorphic mutants of bcd, or mutations in the genes that localize bcd mRNA, look virtually identical to embryos with terminal phenotypes, with double mutants being much more severe. In addition, correct huckebein expression can be induced by either Tor or Bcd activity alone.

Bicoid seems to be a recently acquired gene in fruitflies, and the use of bcd and tor at the anterior is an eccentricity of Drosophila.

If, as is proposed, Tor antagonises repressors of Bcd targets then, in insects that lack bcd, the anterior terminal system could assist other genes (e.g. orthodenticle, thought to be one of the ancestral head determinants). The fact that tor is dispensable for head development might explain why most insects (e.g. with short germband development) can form a head even if it develops further down the egg.