  Cell fate decisions in multicellular organisms are precisely coordinated,
leading to highly reproducible macroscopic outcomes of developmental processes.
The origins of this reproducibility can be found at the molecular level during
the earliest stages of development when spatial patterns of morphogen
(form-generating) molecules emerge reproducibly. However, the initial
conditions for these early stages are determined by the female during
oogenesis, and it is unknown whether reproducibility is passed on to the zygote
or whether it is reacquired by the zygote. Here we examine the earliest
reproducible pattern in the Drosophila embryo, the Bicoid protein gradient.
Using a unique combination of absolute molecule counting techniques, we show
that it is generated from a highly controlled source of mRNA molecules that is
reproducible from embryo to embryo to within ~8%. This occurs in a perfectly
linear feed-forward process: changes in the female's gene dosage lead to
proportional changes in the mRNA and protein counts in the embryo. In this
setup, noise is kept low in the transition from one molecular species to
another, allowing the female to precisely deposit the same absolute number of
mRNA molecules in each embryo and therefore confer reproducibility to the
Bicoid pattern. Our results indicate that the reproducibility of the
morphological structures that emerge in the embryo originates during oogenesis
when all initial patterning signals are controlled with precision similar to
what we observe for the Bicoid pattern.
