der from amphibian to reptile, both the fossil record and
the study of modern vertebrate anatomy suggest an early branching of the
tetrapod trunk into two primary limbs--the Amphibia and the Amniota
(reptile, bird, and mammal).
And now, the point about pentadactyly
and its limits. The Amniota do, indeed, show the canonical pattern of five toes
upon each limb (or some modification from this initial state). But Amphibia, both
living and fossil, have five toes on the hind legs and only four on the
front limbs. Anatomists have known this for years but have always assumed that
this reduction to four proceeded from an initial and canonical five This conclusion
must now be challenged. If all the earliest tetrapods had more than five digits,
and if amniotes separated from amphibians so early in the evolution of terrestrial
life, why assume that the four toes of the amphibian forelimb descended from a
primary five? All modern stabilizations probably proceeded from more than five.
Perhaps the amphibian forelimb went from this higher number directly to four,
without any pentadactyl stage between. If so, then pentadactyly crumbles on two
grounds: (1) It does not represent the original state of tetrapods (as six-, seven-,
and eight-toed earliest forms show); and (2) it may not mark the canonical state
in one of the two great living lineages of tetrapods.A key to understanding
these new views may be found in a brilliant paper on the embryological development
of limbs, based on work done just down the hall from my office and published in
1986 by Neil H. Shubin (now at the University of Pennsylvania) and Pere Alberch
(now director of the Natural History Museum in Madrid)--"A Morphogenetic
Approach to the Origin and Basic Organization of the Tetrapod Limb," in Evolutionary
Biology, edited by M. K. Hecht, B. Wallace, and G. T. Prance, vol. 20, pp.
319-87 (New York: Plenum Press, 1986).Shubin and Alberch try to depict
the complexity of the tetrapod limb as the outcome of interactions among three
basic processes of branching (making two series from one), segmentation (making
more elements in a single series), and condensation (union between elements).
The limb builds from the body out--shoulder to fingers, thigh to toes. The
process begins with a single element extending from the trunk--humerus for
the arm, femur for the leg. A branching event produces the next elements in sequence--radius
and ulna for the arm, tibia and fibula for the leg. The branching (to wrist bones)
sets the distinctive pattern that eventually makes fingers. This key bifurcation
is markedly asymmetrical, as one bone cases to branch (and yields but a single
row of segments as the limb continues to develop), while the other serves as a
focus for all subsequent multiplication of elements, including the production
of digits. Oddly enough, the bone that does not branch is the larger of the two
elements--the radius of the arm and the tibia of the leg. The hand and foot
are made by branching from the smaller element--the ulna of the arm and the
fibula of the leg.These basic facts have long been appreciated. Shubin
and Alberch make their outstanding contribution in providing a new account of
subsequent branching. The classical view holds that a central axis continues from
the ulna (or fibula) and that subsequent branches project from it (much like the
persistent midvein and diverging lateral veins of a leaf). In this view, the roots
of the digits represent different branches. Under this model, largely unchallenged
for more than 100 years, debate focused on the identity of the main axis and its
position relative to the digits. T. H. Huxley, for example, argued that the main
axis passed through digit three; the British vertebrate paleontologist D. M. S.
Watson favored digit four, while the American W. K. Gregory advocated a position
between digits one and two.Shubin and Alberch do not deny the idea
of a central axis, but they radically reorient its position. Instead of passing
through a particular digit (with remaining digits branching to one side or the
other), Shubin and Alberch's axis passes through the basal bones of all
the digits in sequence, from back to front.
The elegant novelty of this switch may not be evident in the simple
change of position for the axis. Consider, instead, the question of timing.
Under the old view, one might talk about a dominant digit (focus of the
central axis) and subordinate elements (products of increasingly distant
branching), but no implications of timing could be drawn. Under Shubin
and Alberch's revision, the array of digits becomes a sequence of timing:
spatial position is a mark of temporal order. Back equals old, front is
young. The piggy that cried wee, wee, wee all the way home comes first;
the one that went to the market is last. The thumb and big toe may be
functionally most important in humans, but they are the last to form.
(As always in natural
history, nothing is quite so simple, or free from exceptions, as its cleanest
and most elegant expression. Actually, the penultimate digit always forms first--ironically,
the piggy that had none--and the sequence then proceeds from back to front
with one exception in a reverse branch to digit five. Moreover, this generality
meets a fascinating exception in the urodeles [the amphibian group of newts and
salamanders, although the other major amphibian lineage of Anura, the frogs, forms
digits in the usual back-to-front sequence]. Uniquely among tetrapods, urodeles
work from front to back [although they also follow the rule of penultimate first,
beginning with digit two and then proceeding on toward five]. Some zoologists
have used this basic difference to argue that urodeles form an entirely separate
evolutionary line of tetrapods, perhaps even arising from a different group of
fish ancestors. But most [including me] would respond that embryonic patterns
are as subject to evolutionary change as adult form, and that an ancestor to the
urodele lineage--for some utterly unknown and undoubtedly fascinating reason--shucked
an otherwise universal system in tetrapods and developed this "backward"
route to the formation of digits.)But why bring up this innovative
model for embryological formation of digits in the context of new data on the
multiplicity of fingers and toes in the earliest tetrapods? I do so (as did Coates
and Clack in their original article) because the Shubin and Alberch model suggests
a simple and obvious mechanism for a later stabilization of five from an initial
lability that yielded varying numbers of supernu-
Adapted
from Jarvik, vol. 2, p. 133
The
embryological development of a tetrapod hand proceeds along Shubin and Alberch's
axis (red arrow). 26 NATURAL HISTORY 1/91 |