Evolution, 4th Edition

354 CHAPTER 14

flies (Drosophila) there has been a flight of genes from the X chromosome to the

autosomes (FIGURE 14.11). Several hypotheses might explain this pattern, which

is the subject of ongoing research [42].

Evolution of Protein-Coding Genes

Although coding sequences comprise less than 2 percent of the human genome,

that slender slice of our genetic material is by far the best understood. Codons pro-

vide genetic landmarks that greatly help interpret how the genome evolves.

Evolution of coding regions by genetic drift

A strong evolutionary pattern is seen across protein-coding genes. The DNA bases

that appear in the first and second positions of codons tend to evolve slowly. DNA

bases in the third positions of codons and in introns tend to evolve much more

rapidly (see Figure 16.5). Changes to first and second positions are likely to be

nonsynonymous, that is, to change the protein, while changes to third positions

or codons are likely to be synonymous, that is, to have no effect on the protein

(see Chapters 4 and 7). In short, the DNA bases most likely to affect a gene’s prod-

uct evolve most slowly. The pattern seems puzzling. If most genetic change were

caused by natural selection, then we would expect exactly the opposite pattern.

Changes that alter a protein have a chance of improving fitness, and so nonsyn-

onymous changes should evolve the most frequently.

But the pattern makes sense if most changes to DNA sequences evolve by ran-

dom genetic drift rather than by adaptation. Between 70 percent and 97 percent of

nonsynonymous mutations are strongly deleterious, depending on the organism

[17]. Most of those mutations are eliminated by purifying selection. In contrast,

synonymous mutations do not change a gene’s product and so are expected to

have much smaller effects on fitness. Those mutations have a chance of spreading

through the species by random genetic drift, contributing to the differences we see

among species. As a result, the DNA bases in a gene that are least likely to have a

fitness effect tend to be those that evolve the most rapidly and that show the larg-

est numbers of differences among species.

This pattern lies at the heart of the famous neutral theory of molecular evolution

developed by Motoo Kimura starting in the 1960s (see Chapter 7). Kimura argued

that the vast majority of differences among species and variation within species in

DNA sequences are due to mutations that are nearly selectively neutral and have

evolved mainly by drift. Purifying selection is constantly at work eliminating del-

eterious mutations, Kimura thought, but positive selection leading to adaptive dif-

ferences among species is so rare that it makes only a negligible contribution to

Futuyma Kirkpatrick Evolution, 4e

Sinauer Associates

Troutt Visual Services

Evolution4e_14.11.ai Date 01-03-2017

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Chromosomal locations of parental genes (intron-containing)

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Chromosomal locations ofnew genes (no introns)

FIGURE 14.11 Gene trafficking in Dro-

sophila melanogaster. The height of

each bar shows how frequently genes

move by retrotransposition from one

genome location (shown on the x-axis) to

another (shown on the y-axis). The blue

lines separate the autosomes from the X

chromosome. Many genes have changed

locations. Furthermore, the movement

is not random: a large number of genes

have moved from the X chromosome to an

autosome (shown by the many bars in the

back left of the plot). (From [42].)

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