EvoluTion And dEvEloPmEnT 383
transcription factors. Drosophila biarmipes has evolved a large melanized spot on
the wing, resulting from a change in one of the enhancers of the yellow gene so
that it now binds both a repressor protein and a transcription factor produced
by the gene Distal-less (FIGURE 15.17) [4, 20]. This also represents a new expres-
sion pattern for Distal-less, which plays various other regulatory roles. So the
wing spot in D. biarmipes is an example of a novel characteristic that is based
on evolutionary changes in both cis- and trans-regulation of a gene, that is, the
yellow gene.
Where do new cis-regulatory elements come from? Some arise de
novo. (See Chapter 14, p. 347, on novel genes.) Others originate by
duplication and sequence divergence of ancestral sequences. But one
source is intriguing: in mammals, some of the binding sites for various
transcription factors are embedded within transposable elements [75].
A dramatic example is in the endometrial stromal cells of the placenta
in humans and other placental mammals. A gene that encodes the hor-
mone prolactin is expressed in these cells, in response to cAMP [40].
The cAMP-responsive enhancer of this gene is derived from a DNA
transposon, MER20. MER20-related sequences are close to the coding
sequences of hundreds of genes that are expressed in these cells, and
these sequences have been experimentally shown to bind several tran-
scription factors that are important in pregnancy.Evolution by trans-regulatory mutations
Alterations of genes that encode transcription factors, by changing
their binding to enhancers, have also proven to play major roles in phe-
notypic evolution [11, 39, 84]. For example, insects, which evolved from
a crustacean lineage, have legs only on the three thoracic segments.
In Drosophila embryos, Ubx is expressed in the abdomen and inhib-
its leg development. When biologists caused the gene to be ectopically
expressed in the thorax as well, it inhibited the development of embry-
onic limbs. However, Ubx is expressed throughout the segments in the
brine shrimp (Artemia), which, like other crustaceans, has appendages
on most of the body segments. When brine shrimp Ubx was transferred
into Drosophila embryos, it did not suppress embryonic limb devel-
opment [63]. Researchers found the same effect when they used UbxFutuyma Kirkpatrick Evolution, 4e
Sinauer Associates
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Evolution4e_15.15.ai Date 12-19-2016(A) Marine(B) FreshwaterPelvic spineDorsal spinesPitx1 expression
(ventral view)FIGURE 15.15 oss of expression of L Pitx1 in the pelvis is associat-
ed with reduction of the pelvic girdle and fins in freshwater pop-
ulations of the three-spined stickleback (Gasterosteus aculeatus).
Adult specimens from (A) marine and (B) freshwater populations.
The pelvis and spines associated with fins characterize the marine
population but not the freshwater population. In the magnified
ventral views of embryos at left, in situ hybridization reveals much
greater Pitx1 expression (purple) in the pelvic area in the marine
population than in the freshwater population. (After [71]; photos
courtesy of D. M. Kingsley.)FIGURE 15.16 The spotted wing pattern of Dro-
sophila guttifera is based on novel expression of the wg
gene. The wings of adult D. melanogaster and D. gut-
tifera are shown below the pupal wings, when pigmen-
tation develops as a result of wg expression, visualized
by blue color. The gene is expressed in D. guttifera not
only in the same sites as in D. melanogaster (arrows), but
also in small sensory structures (arrowheads) and at the
tips of the wing veins (asterisks). These sites match the
spot pattern in the adult. (From [33]; D. guttifera photo
courtesy of Nicolas Gompel and Sean Carroll.)Futuyma Kirkpatrick Evolution, 4e
Sinauer Associates
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Evolution4e_15.16.ai Date 12-19-2016D. melanogaster D. guttifera* wg***wgPupal wingsAdult wings15_EVOL4E_CH15.indd 383 3/22/17 1:30 PM