Selection for rapid embryonic development sculpted the new gene Shrew into an accelerator of Drosophila dorsal-ventral axis specification

Assignment of cell fate along the dorsal/ventral (D/V) axis of the Drosophila embryo occurs during the 40 minutes immediately prior to gastrulation. The mechanism is the rapid redistribution of Decapentaplegic-Screw morphogens from lateral to dorsal regions. Redistribution requires the activity of Short gastrulation (Sog), Twisted gastrulation (Tsg), Tolloid (Tld) and Shrew. The function of Sog, Tsg and Tld and their vertebrate homologs are well known. Shrew remains an enigma, though previous studies showed that Shrew is a truncated relative of Tsg. Our phylogenetic survey revealed that Shrew is Drosophila specific and likely derived from a different Tsg family member Crossveinless. A second survey identified a correlation between insects with Shrew and those with the fastest time to gastrulation. The correlation suggests the hypothesis that Shrew functions as an accelerator of D/V axis formation as an adaption to selective pressure for rapid egg development that reduces exposure to predators. We tested the hypothesis by slowing down egg development with reduced temperature generating the prediction that an accelerator would then be unnecessary. Consistent with the prediction, at reduced temperature shrew was nonessential, with two normally lethal shrew mutants surviving to adult. Together the evolutionary and experimental data suggest that Shrew is an exemplar of a new gene that modifies a developmental process as an adaptation to an identified selective pressure. From a broader perspective the analysis of Shrew reveals that developmental processes are adaptable phenotypes, and that new gene creation is an effective response to selection.