ABSTRACT
Novel phenotypes are increasingly recognized to have evolved by co-option of existing gene regulatory networks (GRNs) into new developmental contexts, yet the changes induced by cooption remain obscure. Here we provide insight into the process of co-option by characterizing the consequences of doublesex co-option in the evolution of mimetic wing color patterns in Papilio swallowtail butterflies. doublesex is the master regulator of insect sex differentiation, but has been co-opted to control the switch between discrete female wing color patterns in Papilio polytes. We show that a pulse of widespread dsx expression early in mimetic wing development activates an alternate color pattern development program that quickly becomes decoupled from dsx expression itself. RNAi and antibody stains revealed that Wnt signaling antagonizes dsx function in some regions of the wing to refine the mimetic color pattern, but that dsx function depends on engrailed, the key transcription factor effector of the Hedgehog pathway. Dsx alters spatial patterns of En expression early in pupal development, but the two genes become decoupled by mid-pupal development when En expression pre-figures melanic and red patterns in all P. polytes. Co-option of dsx into the developing wing therefore results in global changes to development GRNs that function to antagonize and synergize with dsx to specify a novel adaptive phenotype. Altogether, our findings provide strong experimental evidence for how coopted genes cause and elicit changes to GRNs during the evolution and development of novel phenotypes.
SIGNIFICANCE STATEMENT The diversity of life has been built one mutation at a time, but some mutations have larger effects than others. Recent work has shown that entire developmental programs can be copied and pasted, i.e. co-opted, into new parts of an organism and, with some more evolution, produce novel adaptive traits. This paper describes how doublesex was co-opted to produce mimetic color patterns in Papilio swallowtail butterflies and shows the role that local developmental pathways play in limiting or synergizing with the co-opted gene to produce a novel trait. Our results have important implications for understanding the evolutionary process by which developmental programs are modified to produce fuel for natural selection.
Competing Interest Statement
The authors have declared no competing interest.
