Is genetic evolution predictable?

Abstract

Ever since the integration of Mendelian genetics into evolutionary biology in the early 20th century, evolutionary geneticists have for the most part treated genes and mutations as generic entities. However, recent observations indicate that all genes are not equal in the eyes of evolution. Evolutionarily relevant mutations tend to accumulate in hotspot genes and at specific positions within genes. Genetic evolution is constrained by gene function, the structure of genetic networks, and population biology. The genetic basis of evolution may be predictable to some extent, and further understanding of this predictability requires incorporation of the specific functions and characteristics of genes into evolutionary theory.

Fig. 1

Morphological divergence between species has been caused by repeated evolution at an input-output gene. (A) D. melanogaster and D. sechellia differ in the pattern of fine trichomes decorating the dorsal and lateral surfaces of the larvae. This difference is caused entirely by evolution of the cis-regulatory region of the shavenbaby gene (). (B) The cis-regulatory region of the shavenbaby gene integrates extensive information from developmental patterning genes to generate a pattern of Shavenbaby protein expression that prefigures the pattern of trichomes on the first-instar larva. Cells accumulating Shavenbaby will differentiate a trichome because Shavenbaby protein regulates a large battery of genes that act together to transform an epithelial cell into a trichome ().

Fig. 2

Bristle patterns on the dorsal thorax of Drosophila species have evolved within species and between species because of different kinds of mutations. (A) A mutation generating a null allele of the poils au dos gene within a population of D. melanogaster increases the number of large bristles on the dorsal thorax (white triangles indicate normal bristles and green triangles indicate extra bristles) (). In contrast, the increased number of bristles in D. quadrilineata results at least in part from changes in the cis-regulatory region of the scute gene (). The extra bristles caused by the poils au dos mutation are not as precisely positioned as the extra bristles caused by the scute mutation (indicated by purple triangles). (B) The two evolving genes, poils au dos and scute, occupy different locations in the genetic network that generates the pattern of bristles. The scute gene is an input-output gene, whereas the poils au dos gene is a developmental patterning gene. The null mutation in poils au dos increases sensory organ numbers not only in the thorax but also in the wing.

Fig. 3

Different kinds of mutations occur with different frequency during short-term and long-term evolution. Among all mutations causing morphological variation identified to date, the proportion of cis-regulatory mutations (black bars) is higher for long-term evolution than for short-term evolution. For all mutations that have been reported to cause phenotypic variation in either morphology or physiology, the proportion caused by null coding mutations (red bars) is higher for short-term evolution than for long-term evolution. The numbers above the bars refer to the total number of examples in each category. The number of cases of morphological evolution (black bars) is a subset of the number of cases of phenotypic evolution (red bars). Data are from ().