Redeployment of a conserved gene regulatory network during Aedes aegypti development

Kushal Suryamohan, Casey Hanson, Emily Andrews, Saurabh Sinha, Molly Duman Scheel, Marc S. Halfon

Research output: Contribution to journalArticle

8 Scopus citations

Abstract

Changes in gene regulatory networks (GRNs) underlie the evolution of morphological novelty and developmental system drift. The fruitfly Drosophila melanogaster and the dengue and Zika vector mosquito Aedes aegypti have substantially similar nervous system morphology. Nevertheless, they show significant divergence in a set of genes co-expressed in the midline of the Drosophila central nervous system, including the master regulator single minded and downstream genes including short gastrulation, Star, and NetrinA. In contrast to Drosophila, we find that midline expression of these genes is either absent or severely diminished in A. aegypti. Instead, they are co-expressed in the lateral nervous system. This suggests that in A. aegypti this “midline GRN” has been redeployed to a new location while lost from its previous site of activity. In order to characterize the relevant GRNs, we employed the SCRMshaw method we previously developed to identify transcriptional cis-regulatory modules in both species. Analysis of these regulatory sequences in transgenic Drosophila suggests that the altered gene expression observed in A. aegypti is the result of trans-dependent redeployment of the GRN, potentially stemming from cis-mediated changes in the expression of sim and other as-yet unidentified regulators. Our results illustrate a novel “repeal, replace, and redeploy” mode of evolution in which a conserved GRN acquires a different function at a new site while its original function is co-opted by a different GRN. This represents a striking example of developmental system drift in which the dramatic shift in gene expression does not result in gross morphological changes, but in more subtle differences in development and function of the late embryonic nervous system.

Original languageEnglish (US)
Pages (from-to)402-413
Number of pages12
JournalDevelopmental Biology
Volume416
Issue number2
DOIs
StatePublished - Aug 15 2016

Keywords

  • Aedes aegypti
  • Central Nervous System (CNS) development
  • Developmental system drift
  • Drosophila melanogaster
  • Enhancer discovery
  • Evolution of regulatory networks
  • GRN
  • Gene regulatory networks
  • Neofunctionalization
  • Ventral midline
  • Zika vector mosquito

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology
  • Cell Biology

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