MACROEvOLuTiON: EvOLuTiON AbOvE THE SPECiES LEvEL 525
into and out of the lungs. In plethodontids, these bones, no
longer used for ventilating the lungs, have been modified
into a set of long elements that can be greatly extended from
a folded configuration. This modification enables plethodon-
tids to catch prey by projecting the tongue, in some species to
extraordinary lengths at extraordinary speed (FIGURE 20.6).
Marc Kirschner and John Gerhart draw on cell and devel-
opmental biology in developing their hypothesis of “facilitated
variation” [53]. They suggest that the “core processes” of pro-
tein activity and cell and organ development have properties
of robustness and adaptability that cause some variation to
arise in ways that facilitate evolution. For example, developing
muscles, nerves, and blood vessels in a limb respond to sig-
nals from developing bone and dermis, and so grow into their
proper positions. Thus genetic changes in the limb skeleton
result in altered but functional limbs, without the need for
independent genetic changes in musculature and vasculature.
Discoveries in evolutionary developmental biology, such
as recruitment of genes and signaling pathways for new
functions, are helping biologists understand the origin of
novelties. For example, an entire developmental pathway
may be triggered heterotopically in a different part of the body. A Mexican plant,
Lacandonia schismatica, has perfectly formed stamens in the center of the flower,
surrounded by pistils—the reverse of the usual arrangement [56]. A fascinating
case is the anteriormost digit of a bird’s hand, which is morphologically equivalent
to digit 1 in the hand of related dinosaurs, and expresses the genes characteristic of
a first digit (or “thumb”). However, it develops in digit position 2 and is phyloge-
netically homologous to the dinosaur’s second digit. During the evolution of birds
from nonavian dinosaurs, the thumb was lost and digits 2, 3, and 4 underwent a
shift in developmental identity, taking on the features of digits 1, 2, and 3 (FIG-
URE 20.7) [110, 114]. In these cases, entire genetic-developmental pathways are
deployed in new locations on the body (heterotopy), and produce developmentally
coherent, functional phenotypes.FIGURE 20.6 A lungless bolitoglossine salamander (Hydromantes
supramontis) captures prey with its extraordinarily long tongue. The
rapid tongue extension is accomplished with a modified hyobranchi-
al apparatus, which in other families of salamanders plays an impor-
tant role in ventilating the lungs. (From [16], courtesy of S. Deban.)Futuyma Kirkpatrick Evolution, 4e
Sinauer Associates
Troutt Visual Services
Evolution4e_20.07.ai Date 12-27-2016(A)C1
C2
C3
C4
C5D1
D2
D3
D4
D5(B)C1
C2
C3
C4
C5D1
D2
D3
D4
X(C)C1
C2
C3
C4
C5D1
D2
D3XXAlligator Coelophysis Archaeopteryx GallusFIGURE 20.7 A “frameshift” in development of the hand in
birds is thought to have transformed the identity of the digits.
The ancestral state in archosaurs is illustrated by the alligator (A),
and the state in theropod dinosaurs by Coelophysis (B). The state
in Archaeopteryx and modern birds such as chickens (Gallus)
is shown in (C). The developing hand of the embryo has five
groups of cells that form cartilaginous digital condensations (C1
through C5). In (A), these differentiate into the digits D1 through
D5, which are distinct in form and therefore in identity (signaledby different colors). (B) In theropods such as Coelophysis, C5
failed to develop, and only digits D1 through D4 were formed.
(C) In birds, only condensations C2, C3, and C4 develop, but
the digits have the form and identity of D1, D2, and D3 (which
develop from condensations C1, C2, and C3 in the alligator and
theropod). The hypothesis is that the gene networks that specify
the form of digits D1, D2, and D3 are activated in different C con-
densations in birds, relative to their ancestors. (After [110].)20_EVOL4E_CH20.indd 525 3/22/17 1:44 PM