19) The Molecular Genetic Basis of Gene Regulatory Evolution (by Rey J. Rosa Morales)

        Comparative studies of gene expression are showing that gene duplication and nucleotide substitution both contribute to the diversification of gene regulation. For example, the genes snail and slug in vertebrates are both descendants, via gene duplication, of an ancestral gene in the common invertebrate ancestor of all vertebrates, which is thought to be developmentally similar to the cephalochordate amphioxus (the living sister group of vertebrates). In both invertebrates and vertebrates, proteins encoded by the snail gene family (which includes both snail and slug) have evolutionarily conserved functions in mesoderm formation and neural development during embryogenesis. In the lineage containing amphioxus and the vertebrates, snail and slug acquired expression and new developmental roles in the eye lens, the tailbud, and the premigratory neural crest cells (PNCs; these are epidermal cells that originate in the neural crest and migrate to different parts of the body, where they differentiate into a wide variety of cell types, including pigment cells and jaw and facial tissues). Recently, Locascio et al. (2002) have demonstrated that, although expression of slug in the developing lens is conserved across vertebrates, the particular roles of snail and slug in PNCs and tailbud cells have greatly diversified (Figure 1 see below). For example, birds have lost snail expression in the tailbud, but have gained slug expression there, whereas mammalians have retained snail expression in the PNCs and tailbud, and do not express slug either of these tissues. This pattern of regulatory evolution does not conform to a simple duplication-diversification model, especially in the case of the chicken, which has apparently "re-activated" slug expression in the tailbud, a condition that disappeared much earlier in vertebrate history. Locascio and colleagues propose that a rare event such as chromosomal translocation may account for the reappearance of regulatory elements that direct slug expression in the tailbud of birds.

Figure 1. Evolution of the roles of the genes snail and slug in vertebrate development.   (After Locascio et al. 2002.). Colored symbols indicate the expression of the genes in the developing eye lens, premigratory neural crest cells (PNC), and tailbud.   

References:

1. Futuyma, D.J. (2005). Evolution. Sinauer Associates, Inc. Publishers Sunderland, Massachusetts U.S. 
2. Locascio, A., M. Manzanares, M. J. Blanco, and M.A. Nieto. (2002). Modularity and reshuffling of snail and slug expression during vertebrate evolution. Proc. Natl. Acad. Sci. USA 99: 16841-168-16.
3. Ludwig, M. Z. and M. Kreitman. 1995. Evolutionary dynamics of the enhancer region of even-skipped in Drosophila. Mol. BioI. Evol. 12:1002-1011.