<i>oskar</i> acts with the transcription factor Creb to regulate long-term memory in crickets.

Abstract

Novel genes have the potential to drive the evolution of new biological mechanisms, or to integrate into preexisting regulatory circuits and contribute to the regulation of older, conserved biological functions. One such gene, the novel insect-specific gene <i>oskar,</i> was first identified based on its role in establishing the <i>Drosophila melanogaster</i> germ line. We previously showed that this gene likely arose through an unusual domain transfer event involving bacterial endosymbionts and played a somatic role before evolving its well-known germ line function. Here, we provide empirical support for this hypothesis in the form of evidence for a neural role for <i>oskar</i>. We show that <i>oskar</i> is expressed in the adult neural stem cells of a hemimetabolous insect, the cricket <i>Gryllus bimaculatus</i>. In these stem cells, called neuroblasts, <i>oskar</i> is required together with the ancient animal transcription factor <i>Creb</i> to regulate long-term (but not short-term) olfactory memory. We provide evidence that <i>oskar</i> positively regulates <i>Creb</i>, which plays a conserved role in long-term memory across animals, and that <i>oskar</i> in turn may be a direct target of Creb. Together with previous reports of a role for <i>oskar</i> in nervous system development and function in crickets and flies, our results are consistent with the hypothesis that <i>oskar</i>'s original somatic role may have been in the insect nervous system. Moreover, its colocalization and functional cooperation with the conserved pluripotency gene <i>piwi</i> in the nervous system may have facilitated <i>oskar</i>'s later co-option to the germ line in holometabolous insects.