AMER. ZOOL., 15:455-467 (1975).
Tetrapod Limblessness: Evolution and Functional Corollaries
CARL GANS
Department of Zoology, The University of Michigan, Ann Arbor, Michigan 48104
SYNOPSIS. Multiple lines of tetrapods show reduced limbs or their loss. Such patterns are in
diverse lines associated with multiple other characteristics. Only bodily elongation represents a common denominator. Analysis suggests that elongation for traverse of crevices in a
sheltering environment and for the utilization of undulatory locomotion may have provided
the initial selective advantage to the system. Limb reduction would then have been secondary. This hypothesis leads to several interesting implications about the process of diversification in tetrapods.
INTRODUCTION
Evolution sometimes has confronted us
with seemingly new structures (phenotypes). More often we see intermediate
stages, the "hypertrophy" or "atrophy" of
existing systems or organs. The reduction
of structures, or their atrophy, degeneration, or loss, has traditionally attracted
most attention among morphologists. Literally thousands of papers refer to so called
vestigial organs, their functional significance to the organism, and their presumed
phylogenetic significance. Obvious examples are the vermiform appendix, the nictitating membrane, and the coccyx. An
obvious aspect of the existence of such
structures is the functional reason for their
diminution. The selective advantage that
favored the reduction is a question of importance in biomechanical analysis, as biomechanics ultimately comprises a body of
techniques for analyzing the structural
meaning of animal systems. It permits analysis of the way in which some systems work,
and both why and how they achieved their
present configuration in evolutionary time.
However, the search for a particular selective mechanism responsible for the atrophy
or hypertrophy of a particular system in diverse organisms involves a basic fallacy,
I thank W. J. Bock, G. Haas, A. G. Kluge, P. F. A.
Maderson, F. Harvey Pough, and W. Presch for their
trenchant comments on the manuscript. Mr. J. Daniels
measured theskinks. This review derived from studies
under N.S.F. GB-31088X.
namely, the unwarranted assumption that
the syndrome was driven by the same selective force in each case. It also incorporates
the assumption that the aspect being
studied was indeed the primary target of
selection.
There should be no a priori reason for
such assumptions. Various authors have
shown that several different selective effects might well achieve superficially similar
transitions. The search for a presumptive
advantage is furthermore asked most often
for only a single aspect of the organism.
Examination of only a single aspect from
randomly assembled members of diverse
phylogenetic sequences would seem'to have
the spurious advantage that one may be
able to establish morphological generalizations independent of phylogeny. Yet we
know that natural selection acts upon the
totality of the organism. Pleiotropy will assure that the characteristic being viewed is
linked to other aspects and other life stages
of the organism (see Gans, 1965). Consequently, the structure being examined
not only bears the expression of direct
selection, but also of selection on other aspects or stages only indirectly associated
with the aspect being viewed. Theoretical
considerations thus assure that only a holistic view of adaptation will lead to conclusions with a significant degree of generality.
Many tetrapods lack limbs and limb girdles. Others show girdle remnants, short
stumps, paddle-shaped hands, or hands
with a reduced number of digits. Even a
cursory inspection of the place of such
455
456
CARL GANS
forms in vertebrate phylogeny indicates in ontogeny. Among the reptiles only the
that we are dealing with departures from superorder Squamata shows limbless
an initially limbed condition and that this forms. Members of the order Ophidia are
pattern of degeneration must have occur- always functionally limbless. Three of the
red numerous times independently. Such a four families of Amphisbaenia lack exterspectrum of cases might then provide a nal traces of limbs; the fourth has hypergood example for deriving some principles trophied anterior limbs but lacks posterior
about the general pattern of structural re- ones. Among the lizards four families conduction. Perhaps there are some general tain mostly reduced species, five or more
characteristics shared by the majority of families contain some reduced species, and
these animals. If so, analysis of such charac- 11 families are without limbless members
teristics might furnish clues to the selective (Table 1) (Camp, 1923; Grzimek et al.,
factors responsible. I will attempt such 1971; Schmidt and Inger, 1957).
analysis here, omitting fishes, many of
The conditions in caecilians, in snakes,
which became "limbless" without ever pass- and in most amphisbaenians would seem to
ing through a tetrapod stage, and birds and represent a high level of modification, and
mammals in which the reduction never the transitional members of each group beculminated in a completely limbless state. came extinct long ago (certainly the earliest
snake fossils do not provide much evidence
on such issues; see Estes et al., 1970; FrazDISTRIBUTION OF LIMBLESSNESS
zetta, 1970). These major groups have apAll members of one of the three orders of parently diversified after the initial loss of
Recent amphibians (Apoda, Caecilia) lack limbs and passed far enough beyond the
limbs, a second order (Urodela) contains initial transition to limblessness, so that the
some species with reduced limbs, while the selective advantages for the initial change
third (Salientia) shows limbless stages only are unlikely still to be operative in those
TABLE 1. Lizard limbs
Without
With
Pygopodidae
Gekkonidae
N. America, Africa, Asia, Australasia
"Feylinidae"
Scincidae
All degrees of reduction,
Front limbs lost first
Anniellidae
Dibamus
Anelytropsis
Cordylidae
Gerrhosauridae
Chamaesaura
Loss of forelimbs
Anguidae
3 lines each going to limblessness
"Microteiidae" (Gymnopthalmiini)
Many degrees of reduction
"Macroteiidea" (Teiini)
Helodermatidae
Lacertidae
Varanidae
Xantusidae
Lanthanotidae
Iguanidae
Xenosauridae
Agamidae
Shinisauridae
Chamaeleonidae
No tendency toward limblessness
TETRAPOD LIMBLESSNESS
groups in which the modification is well
established. These advantages might, on
the other hand, still be operative in such
lizard families as the anguids, microteids,
skinks and pygopodids where many structurally intermediate conditions occur. Indeed the current retention of diverse stages
of specialization is occasionally interpreted
to result from a process in progress,
perhaps as a general selective advantage
shifting animals toward limblessness, and
proceeding more rapidly in some taxa of a
family or order than in others.
Analysis of these partially limbless systems is complicated by two groups of factors. The first one is the rather abyssmal
state of the alpha taxonomy (definition of
species) in most of these groups of wideranging, generally tropical, forms. For instance the recent revision of pygopodid
lizards by Kluge (1974) more than doubles
the number of species recognized in the
family. Inadequate classifications obviously
complicate comparison, both in defining
the materials and characterizing samples.
The second problem is that we cannot, in
any one instance, know whether we are
looking (i) at a stage in a selective shift that
would lead the species further to limblessness in subsequent generations, or (almost
certainly) (ii) at a group that is currently in
equilibrium with a set of present environmental conditions, so that selection is
against further specialization. Opposed
selection may reflect the prior occupancy of
the theoretical "target" niche by another
limbless species that invaded earlier. While
the species is "intermediate" in terms of the
reduction of its external limbs it has
achieved a currently advantageous condition in terms of its overall phenotype. "Absolute" reduction of limbs is, after all, only a
philosophical construct.
These various limbless and reduced-limb
forms appear to have a wide distribution, at
least in the tropics. Urodela with reduced
limbs are restricted to southeastern portions of the United States. Caecilians are
found scattered throughout the very
humid tropics. They occupy the lower four
parallelograms of a Holdridge triangle
(1947), the most warm and humid regions.
Snakes also occupy this zone, but extend far
457
beyond it. Except for the extreme northern
and southern portions of the continents,
they occupy and have diversified on all of
the major land masses and most tropical
islands. More recent semicommensal
species, such as Typhlops braminus, have
even extended their overall range with the
help of man. Amphisbaenids range widely
over the African and South American continents, but during the Tertiary were
gradually excluded from most of North
America and Europe. Limbless lizards
show a range almost as extensive as that of
snakes.
If one combines these ranges they include all terrestrial regions except for the
vicinity of the Arctic Circle, Ireland, New
Zealand, Antarctica, and the southern tip of
South America, and even many tropical
oceans. Everywhere that amphibians and
reptiles show any diversity, limblessness or
at least the reduction of limbs has been a
successful strategy.
MORPHOLOGICAL CORRELATES OF LIMBLESSNESS
Elongation of body
Loss or reduction of limbs is generally
correlated with elongation of the body.
Limbed species also show drastic differences in relative body diameter. However,
individuals with limbs reduced or absent
always have a smaller body diameter for
equivalent length from snout to caudal tip
than do members of species in which the
limbs are reduced only slightly or not at all.
Elongation has been achieved in two
ways. The relative body diameter has been
reduced by lengthening either the distance
from snout to vent or the distance of the
body as a whole including the tail. A plot of
some 100 diverse specimens of scincid
lizards (Fig. 1) suggests, for instance, a good
correlation of body diameter with the
length of the whole trunk plus the tail,
rather than with the snout-vent length per
se. Some limbed lizards do approach the
limbless forms in the relative length of
snout-vent plus tail (measured against midtrunk diameter). In such species the tail is
always slender and its diameter sharply reduced just posterior to the cloaca; in con-
458
CARL GANS
20
Uj
6 10-
I5
oo o
oo ooo ooo
10
15
2O
BODY LENGTH - CM
25
FIG. 1. Scatter diagram of body proportions fora
series of skinks belonging to diverse genera.
trast, the tail of limbless forms is quite often
as thick as the more anterior trunk. The
good correlation between limb degeneration and relative body diameter suggests
that selection is for the elongation of a zone
of constant diameter (capable of exerting
bending forces) rather than for the elongation of the snout-vent distance.
Absolute size
Except for snakes, in which the diameter
may exceed 30 cm and the limbless
salamanders in which it may exceed 6 cm,
the diameter is less than 3 cm in the vast
majority of limbless lizards and amphisbaenians. While there are relatively few
data giving absolute weights of limbless
forms, the majority of these species are
clearly on the left-hand (low weight) side of
the various weight-metabolism curves for
lizard families presented by Pough (1973).
Vertebrae
The pattern of the cervical and postcervical vertebrae has not yet been shown to
exhibit clear tendencies (Gasc, 1961; Malnate, 1972). The number of vertebrae is
significantly higher in all species in which
limbs are reduced or absent than in limbed
forms (Hofstetter and Gasc, 1969). The
neck-body transition is variable and does
not show any clear tendencies, except that it
is mainly the trunk region that is elongated
(van Bemmelen, 1952). Amphisbaenians,
snakes, and caecilians all have vertebral
numbers far greater than those of any
quadruped lizard. In the lizard genus
Bachia the number of presacral vertebrae
correlates inversely with the length of reduced appendages (Presch, in litt.).
Some burrowing species show supplementary articular facets between their vertebrae; however, so do some limbed forms
(Bellairs, 1972; Camp, 1923). Sewertzoff
(1931a,6) and Edgren (1958) argued that
the total number of vertebrae (neck, body,
and caudal) was more or less constant (in
each kind of snake) with selection apparently influencing the position of the cloaca
and pelvic rudiment within the vertebral
series. Thus far there has been no evidence
confirming this suggestion (Gans, 1964).
Since the multiplication of axial segments
does not involve an addition in the caudal
region, but rather a transverse splitting and
resplitting of each somite (van Bemmelen,
1952), this would, by itself, argue against
the Sewertzoff (1931a,6) hypothesis.
Body muscles
The axial musculature of larger animals
is more complex than that of shorter ones;
there is a general tendency for complex
muscular linkages to span multiple segments. On the other hand there is no tendency suggesting parallel development
among the several lines showing degrees of
limb reduction (Waters, 1969; Gasc, 1974).
Thus Gasc (unpublished) indicated clearly
that the muscular arrangement is distinct in
snakes, amphisbaenians, and limbless
lizards. He also documented various kinds
of differentiation of the transverse,
spinalis, and intervertebral muscles of limbless lizards.
The axial musculature of caecilians is
clearly distinct from that of any of the other
groups (von Schnurbein, 1935; Gaymer,
1971; Gans, 1973). Most important is the
separation of the axial musculature, vertebrae and ribs from the more peripheral,
integument-associated muscles, as well as
from the viscera. Caecilians can curve the
axial mass for concertina movement, thus
widening portions of the trunk without
simultaneous curvature of the viscera (the
viscera do, of course, follow the long,
smooth curves of the body during lateral
TETRAPOD LIMBLESSNESS
undulation). Uropeltid snakes and some
amphisbaenians and lizards have their ribs
extending ventrad to surround the viscera
and consequently must curve the visceral
mass wherever the vertebral axis undergoes undulation.
Limbless species may show significant
local control of their axial musculature.
Thus, for instance, a snake can breathe locally, when portions of the trunk are immobilized by occupation with prey or a
plethysmograph (Rosenberg, 1973). Spectacular curves may be formed and controlled by arboreal snakes to match local circumstances.
Integument
459
1:4 to 2:5 (Alexander and Gans, 1965). In
Amphisbaenia it seems to be 2:1 on the
body and 1:1 in the distal portion of the tail.
Some curious specific exceptions occur as
for instance in the genus Leposternon (Gans,
1971a). The functional basis of these ratios
remains obscure in spite of some numerical
studies on the issue (see Kerfoot, 1970).
The ratio of integumentary segments to
vertebrae is variable in the several groups
of lizards.
Viscera
Characteristic arrangements of the internal organs identify snakes, amphisbaenians, and lizards. The general tendencies
associated with bodily elongation are: (i) a
general elongation of all viscera; (ii) a staggering of the two sides of an organ (right
paired system anterior to left testes in most
amphisbaenians); and (iii) unilateral reduction. The side which is reduced may be
group specific; thus the right lung tends to
become lost in amphisbaenians and the left
lung in snakes and various lizards (Butler,
1895). Similar reductions occur in the
gonad-associated ducts of some forms (Fox,
1965; Fox and Dessauer, 1962).
The gut tends to be elongate and much
less convolute than in tetrapod forms. Extensive reverse (anteriad) looping is lacking. A caecum may or may not remain. A
very long convoluted and coiled small intestine is found among snakes only in Acrochordus (this has led to erroneous speculations that the species is herbivorous).
The entire visceral mass tends to be
characteristically mobile, particularly in the
post-cardiac zone. Major movements are
restrained by the variable mesenteric arrangements. Unfortunately, we lack a recent comparative study of mesenteries to
expand on the suggestive comments offered by Beddard (1905).
The integument is diverse. Caecilians
and salamanders have a highly mucous skin
that appears to possess a low frictional
coefficient with soil. The reptilian skin, in
contrast, is dry and variably keratinized.
That of amphisbaenians, many snakes, and
lizards is smooth, often covered with scales
provided with more or less overlapping
free edges that are directed posteriorly during forward locomotion. The smooth surface provides low friction all around the
circumference of the animal, keeps soil particles (and perhaps ectoparasites) from
sticking to the surface, and furnishes a
further protection in deflecting the
chelicerae of small arthropods. The scales
of other snakes and degenerate or limbless
lizards are centrally keeled or folded. This
may involve a different kind of friction control or wear resistance. The environmental
contact is then restricted to the narrow
central portion of each scale, which may
serve as a guide or runner when the animal
passes through grassy areas. The correlation here is very weak, for instance
Pletholax, the most strongly keeled
pygopodid, is a sand swimmer (A. Kluge,
personal communication). Geometry and
surface texture of scales are maintained by Limbs and girdles
a regular process of ecdysis.
It should not be surprising that the variThe ratio of integumentary scales or an- ous forms discussed show a complete specnuli to vertebrae has often been discussed trum of reduction (Cope, 1892; Essex,
(Camp, 1923; Gans, 1961a). In snakes it is 1927; Stokely, 1947; Gasc, 1965, 1966,
generally 1:1 except in the Typhlopidae I967a,b; see Camp, 1923, for a summary of
and related families where it varies from many earlier papers). Unfortunately, the
460
CARL GANS
assemblage teaches little except that the diverse elements tend to be lost centripetally
(distal to proximal) with the fingers becoming lost or restructured before more central
elements do. Some forms show intraspecific
variation in these characteristics (Dixon,
1973); this suggests some reduction of
selection for a particular configuration of
the foot similar to that producing high frequencies of polydactyly in some populations of domestic cats. It also suggests that
the degree of limb reduction within a
species must, in each case, be characterized
on the basis of adequate local and geographical samples.
The relative progress of reduction differs among species. Thus, most degenerate
lizards lost the pectoral before the pelvic
girdle as did the Amphisbaenidae and
perhaps the (primitive) snakes. In contrast,
the teiids, as well as the Trogonophidae and
Bipedidae first lost the hind limbs; the
former group retains internal pectoral
elements (Gans, 1961a) and the latter has
increased the complexity and effectiveness
of the forelimbs, which now show
polyphalangy (Pena, 1967; Zangerl, 1945).
cannot be characterized by a single adaptive
generalization.
ECOLOGICAL CORRELATES OF LIMBLESSNESS
Environment
Except for snakes, almost all limbless
forms are shelterers or burrowers. They
hide under loose surface debris; they dig in
mulch or tunnel in soil. Some snakes follow
this pattern but many others have invaded
plains and forests, arboreal sites, riparian,
aquatic, and indeed oceanic environments.
T h e Amphisbaenia, Uropeltidae (Serpentes), and Caecilia are true burrowers,
even of hard soils. They are capable of tunneling to significant depth and establishing
permanent tunnel systems. The pygopodids and scincids lack good burrowers;
they contain members that are poor burrowers, others that are sand swimmers,
and many sheltering and crepuscular
species. The teiid Bachia frequents grass
root systems, leaf litter, and sandy soils.
Reduced-limbed anguid and cordylid
lizards are mainly shelterers. They and
some of the pygopodids appear to occupy
niches in grass tussocks, though some
species are semifossorial (Littlejohn and
Skull
Rawlinson, 1971). Anniellids are excellent
sand swimmers. Unfortunately, we lack
The skulls of limbless lizards show re- significant information about the behavior
markable similarity to those of limbed of Dibamus.
members of the same families, though the
head scales may be diversely modified (Es- Food and feeding
sex, 1928). Beyond this there are several,
All limbless or reduced-limbed species
sometimes conflicting, tendencies. Some
forms have compacted their skull, forming are carnivores. Included are snakes, ama solidly enclosed braincase, reducing ar- phisbaenians, caecilians, and elongate
cades and generally shifting the cranial salamanders. All of the lizards here studied
bracing. Examples here are the Caenophi- also share this syndrome. For the lizards
dia (Serpentes), the Amphisbaenia (Zan- one may associate the food habits with size
gerl, 1944), and, in a different way, the (Pough, 1973) and perhaps the habit of
Caecilia (Taylor, 1969). On the other hand hunting in tunnels. Snakes, in contrast, are
most snakes show extremely loosely articu- clearly specialized for capture and whole
lated skulls; their maxillary and palato- ingestion of large animal prey (Gans, 1965),
pterygoid arches have great mobility on the while the Amphisbaenia bite pieces out of
braincase, and not only is the mandibular the body of larger animals (Gans, 1969).
symphysis free, but the braincase some- The Gymnopthalminae show some adaptimes shows a curious fenestration as well tations to the ingestion of larger prey
(Haas, 1968). It is not quite clear where (MacLean, 1974).
these data point, except to suggest that
multiple selective influences appear to be at Sense and sense organs
work. Limbless and reduced-limbed species
Only most snakes and a few lizards (e.g.,
461
TETRAPOD LIMBLESSNESS
Lialis) among the organisms here compared have a large visual system with clearly
effective eyes (Underwood, 1970). Even in
these species the eyes appear to have been
restructured by the development of a brille
out of "fused" and transparent eyelids. In
the amphisbaenians the eye is quite generally reduced; in a few caecilians it may be
covered by a bony layer of the skull (Taylor,
1969). In limbless and reduced lizards it is
variably reduced (Mertens, 1970).
The sense of smell appears to have remained important or increased in importance. The external narial opening is often
convoluted or protected by internal plugs
that cause reversal of airflowinternal to the
nostrils possibly as an air-filtering or conditioning mechanism. Many of the lizards
with reduced limbs show various levels of
reduction of the external auditory meatus
(Mertens, 1971). This is always absent in
snakes and amphisbaenians.
In limbless lizards, hearing tends to be
reduced in comparison with the pattern in
surface-dwelling forms, however, with
good sensitivity to sounds in the lower and
middle frequencies (400-1,000 Hz). Snakes
have minimal hearing above 1,500 Hz
(Wever, 1967). The Amphisbaenia have
developed a new "middle ear" multiplying
system that accepts vibrations from the side
of the face and transmits them via cartilaginous or ossified tissues to the stapes
(Wever and Gans, 1973).
Caecilians have developed a tentacle apparently serving as an accessory sensory
organ (Taylor, 1968). Some snakes use
thermal sensory detectors that have clearly
developed independently twice (Barrett,
1970).
Reproduction
Limbless amphibians have specializations
the functions of which are still under study.
Viviparity occurs in a number of caecilians
and there are reports on curious modes of
development involving grazing of the
uterine lining (Parker, 1956).
In viviparous or ovoviviparous lizards
(Typhlosaurus, Anniella) and in Amphisbaenia, the egg is elongate and the embryo
complexly bent (Gans, 19716). There ap-
pears to be a clear developmental gradient;
the head and anterior trunk develop more
rapidly than the posterior trunk and tail
which remain curled into a circular rather
than oval spiral and reduced in size. Snakes
show an extensive spectrum of egg size and
embryo shape.
Locomotion
Table 2 shows the major locomotor patterns seen in various limbless forms (Gans,
1974). There is no question but that lateral
undulation represents the only common
denominator (and may of course represent
a primitive vertebrate characteristic). It is
clearly common to all limbless forms as well
as to the various more or less degenerate
species. Concertina motion is seen in
snakes, in amphisbaenians, and, as a special
variant, in caecilians. Thus far it has been
reported in only very few lizards. Rectilinear motion involves a major structural
rearrangement of the integumentary connections and is restricted to some snakes
and amphisbaenians. Sidewinding is an
exclusively ophidian method. Diverse limbless forms also use different burrowing
methods, based primarily on ramming
modifications as well as ram-and-widen alternations (Gans, 1974).
GENERALITIES
All of the above suggests multimodality
rather than a large number of common features characterizing tetrapods with degrees
of limb reduction. Indeed, each further
and more detailed analytical breakdown
leads to the recognition of increased diversity. Clearly we are not looking at a single
solution to a single problem but perhaps at
multiple solutions to several problems. Possibly we are seeing the effect of parallel
selection upon diverse genetic stocks (see
Bock, 1959, 1967).
There are, however, a few characteristics
that show up repeatedly, indeed almost
universally, in forms with reduced or absent limbs. The key common denominator
appears to be an elongate body; it is always
associated therewith. Other characteristics
are not universal and may be shown either
to be associated with or to derive from
462
CARL GANS
TABLE 2. Major locomotor methods of limbless vertebrates (after Gans, 1974).
Locomotor method
Vertebrate
Lateral
undulation
Elongate
fishes
Caecilians
Common
Common
Rare
Rare; special
variant used
—
Common
Common;
also special
variant
Common
Rare?
Common
—
Limbless
lizards
Amphisbaenia
Snakes
Concertina
Common
Sidewinding
Saltation
Rare
—
Common in
some species;
environmental
influence
important
elongation. It then seems appropriate to
start with the assumption that elongation
may indeed have been produced by the initial selective advantage and that it preceded
limblessness, and to consider the corollaries
of such assumptions.
Elongation means either a reduction in
the relative diameter for a given mass, an
increase in the relative length, or both. The
only mechanism that may plausibly have
required a limit on the relative diameter of
an animal is the ability to pass crevices. In
evaluating the many kinds of such crevices
we may consider them to be either absolute
or relative. An absolute crevice would be a
tunnel in rock, in gravel, or in a similar,
essentially incompressable substance. A relative crevice might be a tunnel in loose soil,
sand, or equivalent material that would be
compressed or displaced by the imposition
of a quantity of energy proportional to
some function of the diameter of the tunnel. Reduction of diameter for a given body
mass (e.g., elongation) would then incur a
selective advantage either by letting an
animal pass through a greater percentage
of the crevices encountered, or permitting
the passage of particular crevices with a
reduced investment of energy.
Once elongation (or diametric reduction)
had been initiated there are two factors that
would facilitate the transition to limblessness. It is immediately obvious that as long
Rare
Special
variant
Isolated
cases
Rectilinear
—
—
—
Common
Common in
boids, uropeltids,
viperids,
some colubrids
as the appendages project from the sides of
the body they will increase the body's effective diameter. The ability to fold them to
the sides, to reduce, or to lose them might
have a selective advantage equivalent to
that for diametric reduction. However, the
disadvantage of projecting limbs would not
have driven the overall selective balance
toward limb reduction until another
locomotor method were available.
Lateral undulation is the obvious candidate. However, only those species
sufficiently elongate to undulate would be
protoadapted to reduce their limbs. Lateral
undulation has intrinsic advantages that
may well have favored it once an animal
had achieved the minimal structural
change in this direction. The pilot studies
of Chodrow and Taylor (1973) indicate that
the lateral undulatory locomotor method,
though still more costly than swimming is to
a fish, is much more effective than is quadrupedal movement in terms of energy to
maintain a given velocity in an animal of
unit mass. The advantage probably derived
from the lack of necessity for lifting and
hence supporting the trunk during
locomotion. A shift toward undulation then
reduces selection for maintaining functional limbs.
This set of arguments then makes it
plausible that selection acted primarily toward elongation and considers the reduc-
TETRAPOD LlMBLESSNESS
tion of limbs to be a secondary modification. One could attempt to differentiate
among the first group of specializations to
check which evolved for sheltering and
which for undulatory locomotion. At the
moment, this may be an unnecessary, indeed a spurious, effort. The two sets may
well have been associated and we are probably dealing with coadapted structures.
Such a shift toward a reduction of limbs
following a reduction of the limb's selection
coefficient could proceed fairly easily in diverse lines of lizards as it involved few other
modifications. After all, the basic motor
pattern, even of tetrapod lizards, still retains large undulatory components and
presumably the neurbmotor systems for
these (Daan and Beltermann, 1968). Boker
(1937) long ago documented that many
amphibians and reptiles have involved only
a relatively minor fraction of their somatic
musculature with the use of limbs and girdles; when these are dissected away they
still leave a fish-like body with an essentially
continuous axial mass.
It is now easy to characterize a whole
series of additional specializations that result directly from or are at least associated
with this primary change in the relative
diameter of the trunk. The first and most
interesting specialization appears to be the
multiplication in the number of trunk vertebrae. This is most interesting because it
documents the extent to which emphasis on
the supposed "atrophy" of one system has
diverted attention from the equally
ubiquitous and significant "hypertrophy"
of a different one. The complication of the
trunk musculature is clearly associated with
this increase of segment number and with
the selective advantage first to form the
body into at least two reversing curves leading to simple lateral undulation, and later
to more advanced undulant locomotor patterns. Consequently, many of the characteristics here "associated" with limb reduction probably preceded rather than followed it.
Developmental studies (Raynaud,
I972a,b) do yield some information about
the ontogeny of the changes above discussed mainly as they apply to adults. Most
evidence suggests that limb reduction sim-
463
ply involves the progressive loss of those
structures last to develop in ontogeny (Essex, 1927), though the exact method first of
formation and then of regression of diverse
Anlagen presumably varies between
species. Certainly selection need not act toward a uniform regression of all aspects of
an appendage (Steiner and Anders, 1946);
the particular utilization (function) of the
"degenerate" structure will obviously determine the rate and pattern of the process
and the stage of degeneration at which the
system stabilizes. Sewertzoff (1931a,6)
characterized these kinds of structural
changes as rudimentation (to a "degenerate"
state) and reduction (aphanisia) by which he
meant a total loss of the element ultimately
leading to disappearance of the Anlage as
well. Steiner and Anders (1946) added the
"third" category of adaptive reduction implying the shift to a structurally reduced, but
selectively advantageous, stage. The present analysis would suggest that most cases
of rudimentation are actually adaptive and
that total reduction most often represents
the end point of a historically old process.
Matters like visceral elongation, staggering of visceral organs, their complex suspension, and indeed the folding and headto-tail development of the embryo are all
specializations that may be associated with
elongation, rather than with the relative
reduction of the diameter, of the trunk.
The scincid solution facilitates lateral undulation by thickening of the caudal portion,
rather by keeping the body's absolute
diameter constant relative to the propulsive
portion of the trunk. Such a change of the
animal's, mainly relative, diameter by adding
a muscular tail is also seen in fishes, species
in which an increase in absolute crosssectional dimensions might be disadvantageous as it would involve an unacceptable
energy cost per unit of progression due to
increase in contour drag. The general
celomic, rearrangement seen in elongate
vertebrates is then a complex of modifications that permits undulant deformation of
the visceral cavity without undue stress on
the contained organs.
The caecilian structural pattern poses
some special problems. It is clear that it
shares only the most general parallel to the
464
CARL GANS
arrangements seen in any of the squamates.
It seems plausible to suggest that the body
wall musculature represents a specialization for support of the viscera in animals
that lack long ribs for sheathing this cavity.
Might the initial shifts to elongation and
lateral undulation have occurred in the water? If so, the structural pattern would
reflect specializations associated with a secondary shift of essentially aquatic animals
toward terrestriality. Alternately, might the
muscular body wall represent a secondary
specialization of animals deriving from a
group that breathed by pulse pumping
(Gans, 19716)?
ASSOCIATED MODIFICATIONS
Animals with these initial specializations
for the passage of crevices clearly would be
protoadapted (Gans, 1974) for burrowing;
both elongation and limblessness are
specializations in this direction. The observed specializations of the sensory functions and sense organs may also be associated with burrowing. Here we are dealing with numerous modifications that arose
much later than the general trends (toward
elongation and limblessness) here discussed. These modifications account for the
diversity of solutions observed in different
species. One must consequently deal with
several lines, each including one or more
groups of animals with limbs reduced or
absent.
The first group includes those limbless
forms that apparently passed through a
sheltering adaptation during a transitional
stage leading to a burrowing mode. The
amphisbaenians, the caecilians, and such
odd snakes as the uropeltids have completed the transition and are now entirely
subterranean. Their ancillary specializations are clearly associated with the subterranean environment they occupy. Certainly they followed rather than preceded
the development of limblessness.
A large number of snakes and lizards
remain in the sheltering environment or
occupy such facies thereof as the tuft grasses (the South African lizards of the cordylid genus Chamaesaura, and apparently
some pygopodids). Keeled scales are an ob-
vious adaptation for some such habitats.
Indeed grass tufts and very dense vegetation such as spinifex, provide a kind of microhabitat in which numerous elongate and
reduced-limbed lizards may be observed.
Perhaps this represents one variant of the
"crevice"-rich habitat in which the
elongation-limblessness syndrome started
to develop.
Then there are the sand swimmers, including many lizards and some snakes.
These species move by undulation through
loose sand but may often feed on the surface (Schmidt and Inger, 1957) and otherwise become modified for this curiously intermediate environment (see Gans 1974;
Norris and Kavanaugh, 1968; Pough,
1969aA 1971).
Finally there are snakes. These seem to
have utilized the sheltering behavior as an
entry to a subterranean mode of life. They
have then reemerged, apparently after
specialization had proceeded quite far.
This view was initially proposed by Walls
(1942), who documented that the ophidian
eye differed fundamentally from that of all
other vertebrates, interpreting this as
reflecting a history of reduction followed by
restructuring. This interpretation has recently found support in the observation
that the optic cortex and other portions of
the ophidian central nervous system also
reflect these changes (Senn, 1966; Northcutt and Butler, 1974). As some burrowing
snakes have recently been shown to climb
when tracking prey by olfaction,
reemergence is plausible (Vanzolini, 1970).
Snakes apparently emerged earliest from a
burrowing existence, before most of the
other limbless forms. They were thus able
to radiate into and occupy a wide range of
environments and exclude other forms
from these.
A major quaternary specialization of
snakes seems clearly to have been that of
expanding the gape to encompass ever
larger prey items. A 1% increase in gape
will lead to a 3% increase in a spherical mass
ingested, while a 10% increase in gape will
increase the volume of the ingested material by 33%. This provided an obvious advantage to specialization toward cranial
kineticism. Increased gape not only pro-
TETRAPOD LIMBLESSNESS
vides the snake access to a larger range of
prey objects, but also reduced the number
of search-stalk-kill-ingest operations per
gram of food intake. Those snakes that developed other locomotor methods might
have become coadapted by a reversed selection back to a stouter body configuration.
Similarly, the trogonophids have reversed
the trend toward bodily elongation (Gans,
1961a, 1969) seen in other families of amphisbaenians. The shift toward oscillatory
burrowing reversed selection and the more
derived trogonophids are both shorter and
stouter than are the less specialized members of the group.
465
When a particular functional demand affects several phylogenetic lines, selection
will probably produce more than a single
solution, each reflecting the particular genetico-developmental background of the
species undergoing selection. To the extent
that structures or conditions being studied
are phylogenetically old, there will be an
increased probability that they will subsequently have been modified in response to
changes in the direction, indeed to reversals, of selection. Probability statements about the mechanisms underlying the initial
changes clearly demand a parallel examination of multiple members in as many as
possible of the multiple lines that incurred
these changes. Even so, it is impossible to
CONCLUSION
achieve in this manner certainty about the
We have now seen that specialization in actual sequence of evolutionary changes in
one direction, in this case toward the de- any particular line; probability statements
generation or loss of limbs, was a secondary will have to serve.
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