T HE EvoluTion of GEnEs And GEnomEs 357
type to find humans is its ability to detect human odors [47].
An odorant receptor protein called Or4 that is expressed on
the mosquito’s antennae has recently evolved in two ways.
Domestic mosquitoes carry alleles for the receptor with cod-
ing differences that enable it to detect sulcatone, a chemical
that is characteristic of human body odor. A second change
is that domestic mosquitoes express roughly twice as much of
the receptor on their antennae. The combined effect of these
changes is to make the domestic form of Aedes aegypti very
efficient at feeding on humans—and transmitting disease.
In the previous section you saw how a gene adapts by
changes to its coding sequence that alter the biochemistry
of the protein made by the gene. The evolution of the Or4
gene illustrates a second pathway to adaptation: changes in
expression. Selection can alter how often, when, and where
a gene is transcribed, how the transcript is spliced and pro-
cessed, if and how the transcript is translated into a protein,
and how the protein is deployed (see Chapter 15). Several
mechanisms are involved. Many evolutionary changes to
gene expression come from changes in sites that bind tran-
scription factors. Gene expression can also evolve through
changes to alternative splicing patterns, and by epigenetic
changes to the DNA and the histones that are bound to it.
When a population adapts to a new environment, regions
of the genome that are under positive selection will diverge
most rapidly from other populations and closely related spe-
cies. This fact has been used to study how marine popula-
tions of three-spined stickleback fish (Gasterosteus aculeatus)
have adapted in parallel in several independent coloniza-
tions of rivers and streams (see also Figure 8.8) [32]. Of the
many places in the genome that show evidence of adapta-
tion, between 40 percent and 80 percent are regulatory,
while only 17 percent are in coding regions (FIGURE 14.13).
In recent human evolution, it appears that adaptive evolu-
tion of the nervous system has resulted largely from changes
to gene regulation. For example, after modern humans
diverged from Neanderthals some 600,000 years ago, a mutation was fixed in an
intron of the FOXP2 gene that changes its expression. That discovery is intriguing
because FOXP2 may have been involved in the evolution of speech [52].
Comparisons among the genomes of distantly related species reveal small
regions of noncoding DNA that are much more similar than the rest of the genome.
These ultraconserved elements are thought to be under strong purifying selection
that constrains them from drifting apart [59]. Ultraconserved elements have been
used to identify thousands of noncoding regions in mammalian genomes that may
be regulatory elements [41].
Operons are clusters of genes that are transcribed together into a single mRNA.
This message can be translated as a single unit or can be spliced into several mes-
sages that are translated separately. This setup provides an economical way to
regulate expression because all of the genes in an operon are turned on and off
together. The favorite food of the gut bacterium Escherichia coli is glucose. But if
there is no glucose nearby, a set of genes called the lac operon turns on, producing
the enzymes needed to feed on lactose. Expression patterns can evolve by add-
ing and removing individual genes from operons [58]. Operons are particularlyFutuyma Kirkpatrick Evolution, 4e
Sinauer Associates
Troutt Visual Services
Evolution4e_14.13.ai Date 02-02-2017EyeHeartPectoral muscleLiverGillHypothalamusTelencephalon******41% (26)
Regulatory17% (11)
Coding42% (27)
Probably
regulatory0 40 80
Gene count120FIGURE 14.13 Many changes in the brain, skeleton, and physiol-
ogy evolve in three-spined sticklebacks (Gasterosteus aculeatus)
when they invade fresh water from marine populations. Certain
regions of the genome consistently show excess divergence be-
tween freshwater and marine populations, indicating they are in-
volved in adaptation to fresh water. The pie chart shows that about
one-sixth (17 percent) of these regions involve nonsynonymous
changes to coding sequences, while the remainder are in genome
regions that are probably or definitely regulatory. The genome
regions that show excess sequence divergence are enriched in
genes that are expressed differently in freshwater and marine
populations. Each pair of bars in the bar graph shows the results
from a different tissue. The blue bars show the numbers of genes
whose expression levels are expected to be different by chance,
and the red bars show the numbers of genes observed. Six of the
seven tissues show statistically significant expression differences
(indicated by asterisks), showing that gene expression evolves as
the fish adapt. The freshwater and marine environments have many
differences in addition to salinity, for example in the prey that the
fish eat and the parasites that attack them. (After [32].)14_EVOL4E_CH14.indd 357 3/22/17 2:44 PM