Enhancer modularity and the evolution of new traits

ABSTRACT

Animals have modular cis-regulatory regions in their genomes, and expression of a single gene is often regulated by multiple enhancers residing in such a region. In the laboratory, and also in natural populations, loss of an enhancer can result in a loss of gene expression. Although only a few examples have been well characterized to date, some studies have suggested that an evolutionary gain of a new enhancer function can establish a new gene expression domain. Our recent study showed that Drosophila guttifera has more enhancers and additional expression domains of the wingless gene during the pupal stage, compared to D. melanogaster, and that these new features appear to have evolved in the ancestral lineage leading to D. guttifera.¹ Koshikawa S, Giorgianni MW, Vaccaro K, Kassner VA, Yoder JH, Werner T, Carroll SB. Gain of cis-regulatory activities underlies novel domains of wingless gene expression in Drosophila. Proc Natl Acad Sci USA 2015; 112:7524-9; PMID:26034272; http://dx.doi.org/10.1073/pnas.1509022112[Crossref], [PubMed], [Web of Science ®] , [Google Scholar] Gain of a new expression domain of a developmental regulatory gene (toolkit gene), such as wingless, can cause co-option of the expression of its downstream genes to the new domain, resulting in duplication of a preexisting structure at this new body position. Recently, with the advancement of evo-devo studies, we have learned that the developmental regulatory systems are strikingly similar across various animal taxa, in spite of the great diversity of the animals' morphology. Even behind “new” traits, co-options of essential developmental genes from known systems are very common. We previously provided concrete evidence of gains of enhancer activities of a developmental regulatory gene underlying gains of new traits.¹ Koshikawa S, Giorgianni MW, Vaccaro K, Kassner VA, Yoder JH, Werner T, Carroll SB. Gain of cis-regulatory activities underlies novel domains of wingless gene expression in Drosophila. Proc Natl Acad Sci USA 2015; 112:7524-9; PMID:26034272; http://dx.doi.org/10.1073/pnas.1509022112[Crossref], [PubMed], [Web of Science ®] , [Google Scholar] Broad occurrence of this scenario is testable and should be validated in the future.