Evolution at two levels: on genes and form

Abstract

Emerging knowledge about organismal evolution suggests that changes in the regulation of gene expression have played a major role - a thesis proposed 30 years ago by King and Wilson.

Figure 1. Different Modes of Gene Evolution Increase the Diversity of Gene Function and Minimize Pleiotropy

The function of a progenitor gene with the simple structure of one cis-regulatory element (red circle) and a pair of exons (black rectangles) can be expanded and diversified in several ways. (A) Gene duplication followed by mutations (asterisks) in either coding or regulatory sequences of the initially identical paralogs will produce genes that may be expressed in different ways or proteins with distinct functions, while the original function can be maintained. (B) An expansion in the number of cis-regulatory elements by any of a number of means (transposition, rearrangement, duplication, point mutation) can expand the number of tissues in which the gene is active, but preserves the original function. (C) The evolution of a new exon and splicing sites creates the potential for alternative forms of a protein to be made. Mutations in alternative exons (asterisks) need not affect the original function of the protein.

Figure 2. The Modular Architecture of the cis-Regulatory Regions of Pleiotropic Genes Enables the Independent Evolution of Gene Expression in Different Body Parts

(A) Expression of the yellow pigmentation gene of Drosophila is controlled by several different cis-regulatory elements (red circles). Differences in the activity of selected elements (wing and wing spot) underlie differences in pigment patterns between species (Figure based on [35].) (B) Similarly, the expression of the Pitx1 gene of vertebrates is inferred to be controlled by multiple elements (red circles). In pelvic-reduced stickleback fish, Pitx1 expression is absent from the pelvic region. This is proposed to occur through of a selective loss of activity of the hindlimb regulatory element (cross through the red circle) (Figure based on [33].)

Figure 3. The Regulatory Evolution of FOXP2 and the Origins of Vocal Learning

(A–F) The patterns of FOXP2 expression in sections of bird brains are depicted The green area is the striatum. FOXP2 is upregulated in the vocalization center known as Area X (pink spots) in vocal-learning species such as the zebra finch (A) and black-capped chickadee (B) but not in non-learning species such as the ringdove (C). (D–F) In the canary, FOXP2 expression in Area X varies over seasons; elevated expression is associated with periods during which the song is plastic (pink spot). (Figure based on [68].)