Evolution, 4th Edition

382 CHAPTER 15

developmental-Genetic Bases of

Phenotypic Evolution

Because early data showed that the proteins of humans and chimpan-

zees are very similar, Mary-Claire King and Allan Wilson suggested that

the many morphological differences between the species are likely to be

caused mostly by regulatory differences rather than protein sequence

differences [31]. We now know that they were right: differences in gene

regulation underlie much morphological evolution. For example, differ-

ences in beak size and shape among the Galápagos finches in the genus

Geospiza are based on growth differences in the prenasal cartilage and

later in the premaxillary bone. In a series of studies, Arhat Abzhanov

and collaborators have shown that the expression of certain growth-reg-

ulating genes during beak development accounts for these differences

[1, 41]. The Bmp4 gene is expressed in the prenasal cartilage earlier and

at higher levels in the embryos of species that have deeper, wider beaks

(FIGURE 15.14). The calmodulin gene is expressed more highly in species

with elongated beaks. Later in development, differences in expression of

three other genes in the premaxilla correlate with beak differences. The

expression level of most of these genes has been experimentally altered

in chicken embryos and produces the same effects that are seen in the

finches. These genes encode transcription factors with well-known

functions in craniofacial development. As we will see, evolution of both

transcription factors and cis-regulatory sequences has been important.

Evolution by cis-regulatory mutations

Many of the mutations that affect morphological variation reside in

regulatory sequences [36, 61, 73]. Changes in cis-regulatory elements

can happen in several ways [64]. Deletion of an enhancer can prevent

a characteristic from developing. For example, the pelvic girdle and fins

have been reduced independently in many freshwater populations of the

three-spined stickleback (Gasterosteus aculeatus) that have independently

descended from marine ancestors. This change is caused by a recurrent

deletion of an enhancer of the Pitx1 gene (FIGURE 15.15) [10]. An exam-

ple closer to home is the evolutionary deletion of an enhancer of the

human androgen receptor gene that determines the gene’s expression

in the fetal penis. This enhancer is the developmental basis of minute

spines on the penis that are present in chimpanzees and many other

mammals but are lacking in humans [46].

Many changes in cis-regulation evolve by mutational changes in

the enhancer’s sequence. For example, the dark pigmented spots in

the wings of Drosophila guttifera correspond to the locations where

the wingless (wg) gene is expressed in the developing wing (FIGURE

15.16). The protein product of this gene affects the expression of many

other genes. The wings of D. melanogaster, which normally lacks dark

wing spots, expressed the D. guttifera pattern when a specific fragment

from the D. guttifera wg gene was transferred into the D. melanogas-

ter genome. Because this sequence differs only slightly between the

species, the researchers concluded that a small number of changes in a single

enhancer of the wg gene caused the expression of pigmentation genes in the

wings of D. guttifera [33].

Evolutionary changes in enhancers can increase or decrease their affinity for

certain transcription factors, and can sometimes cause them to bind different

Futuyma Kirkpatrick Evolution, 4e

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Bmp4 expression

pmx

G. scandens

G. magnirostris

G. fortis

Geospiza fuliginosa

G. conirostris

FIGURE 15.14 Among species of Galápagos finches

(Geospiza), differences in the depth and length

of the premaxilla (pmx) are determined largely by

differences in the expression the gene Bmp4 at a

critical stage in development. Darker staining in the

region indicated by red arrows shows higher gene

expression. The gene shows lower expression in

species with more slender, pointed bills (G. fuligi-

nosa, G. scandens, and G. conirostris) at the same

stage of development. (From [1]; skull images from

[7], reproduced with permission of University of

California Press.)

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