AMER. ZOOL., 15:469-481 (1975).
Pattern and Instability in the Evolving Premaxilla of Boine Snakes
T. H. FRAZZETTA
Provisional Department of Ecology, Ethology and Evolution, University of Illinois,
Urbana, Illinois 61801
SYNOPSIS. Morphological evidence indicates that within the snake family Boidae the subfamily Pythoninae is ancestral to the Boinae. The python-boa transition in evolution involves a
peculiar rotation of the premaxillary bone. During rotation the ventral process of the
premaxilla, the processus palatini, is largely obliterated but reconstituted in later Boinae.
There exist indications that the pattern of the processus palatini is less controlled or stable in
boine snakes than in pythonines. Pattern instability can be the result of several factors which
include relaxed selection for precise form and a disruption in the developmental foundation
of the feature which has not fully been reversed. These possible factors, though fundamentally different, need not exclude each other. It is surmised that the pattern instability in
boines is related, at least in part, to the disruption of a morphogenetic paradigm affecting
premaxillary shape.
PYTHONS AND BOAS
INTRODUCTION
Major adaptations of animals often
characterize broad, taxonomic groupings.
They quite usually consist of a number of
components harmoniously integrated in a
suitable, functional relationship. Such
complex adaptations have rather seldom
received, in evolutionary studies, the analytic attention given simpler systems. This
tradition of neglect has not daunted several
very important investigators (e.g., C. H.
Waddington), and now in recent times
seems to be abating—growing numbers of
biologists (see Frazzetta, 1975, for examples) are considering the evolution of complex systems.
The present study deals with the evolution of a rather minor skeletal character in
snakes, but one which is probably structurally and developmentally organized within
the framework of several controlling
influences. This character, the palatine
process of the premaxillary bone, was
examined in pythons and boas.
I am grateful to C. J. Cole, Hyman Marx, and Ernest
Williams for permission to examine specimens in the
collections under their care. Points of criticism were
offered by Karel Liem, Alexa Clemans, Joshua Laerm,
Arthur Ghent, Harrison Ambrose III, and Clarice
Prange. I also appreciate a very brief discussion with
Carl Gans. The work was supported by the National
Science Foundations (GB-5831) and by the University
of Illinois Research Board.
The Boidae is a primitive snake family
containing several subfamilies. T h e
number and composition of these subfamilies seem not to have been settled to
everyone's satisfaction. I have not yet been
persuaded to adopt a view of boid classification greatly different from my earliest one
(Frazzetta, 1959).
The genus Exiliboa (Bogert, 1968) seems
perhaps related to Ungaliophis and should
be placed in whichever subfamily contains
Ungaliophis. For now I shall let that subfamily be the Boinae although this genus is
difficult to assign and may later on impress
me as best placed elsewhere. Loxocemus,
long regarded as a python, shows affinity
with the primitive snake families Aniliidae,
Xenopeltidae, and the extinct Dinilysiidae
(Haas, 1955; Romer, 1956; Estes et al.,
1970). To my mind this does not mean that
Loxocemus has thereby necessarily lost its
ranking as a member of the Pythoninae. It
fits comfortably with the pythons in terms
of most of its morphological features while,
at the same time, shows strong ties with
other primitive snake groups. Perhaps this
means that Loxocemus is indeed a primitive
representative whose close connection with
the Boidae (as with other primitive families)
adds assurance that boid snakes themselves
are quite primitive, and stemmed from a
469
470
T. H. FRAZZETTA
form not very unlike Loxocemus.
The subfamilies Pythoninae and Boinae
as I have defined them (Frazzetta, 1959)
each contain a spectrum of specialized
forms ranging through terrestrial, arboreal, and fossorial modes of life. The pythons
total about 8 genera and 20 or so species,
and except for Loxocemus are all confined to
the Old World. The Boas number perhaps
13 genera and roughly 30 species. Nine of
the genera with their nearly 20 species are
New World. The remainder are Old
World.
In general pythons and boas are quite
comparable in skeletal traits. Terrestrial
pythons resemble terrestrial boas, and arboreal pythons resemble arboreal boas in
general skull structure and in broad
parameters of cranial function. Fossorial
species are less readily matched. The rough
similarities which can be observed generally
in pythons and boas exist, nevertheless,
alongside differences in cranial structure
which form the basis for the taxonomic division of these two groups. All pythons possess a supraorbital bone, an element which
is absent in all boas (see Fig. 1). No boa bears
teeth on the premaxilla in contrast to all but
two pythonine genera (Aspidites and
Calabaria). There exist other premaxillary
differences which will be noted later on.
And there are differences in the structural
mounting of the snout's nasal bones on the
braincase. Other contrasts exist too.
T h e type of naso-frontal (snoutbraincase) mounting, the form of the premaxilla and its possession of teeth in
pythons indicate, along with other morphological evidence, that the Pythoninae is
the more primitive (i.e., lizard-like) of the
two groups. It also seems evident that the
Boinae arose from an ancestor which, were
it alive today, or at hand as a well-preserved
fossil, would unhesitatingly be slipped into
the Pythoninae.
A tentative phylogenetic tree is given in
Figure 2. Parts of this scheme of relationships are crucial to the ensuing arguments,
and a detailed justification, based on skull
characters, is in preparation. Such justification is lengthy and well beyond the limits
which must be observed in the present article. But it should be said that the most cru-
FIG. 1. Skull and mandibles of the python Bothrochilus boa. d, Dentary; e, ectopterygoid; fr, frontal;
m, maxilla; na, nasal; pi, palatine; pm, premaxilla; po,
postorbital; pr, prefrontal; ps, parasphenoid; sm, septomaxilla; so, supraorbital; vo, vomer.
cial points in the phytogeny seem, on my
evidence, to be the least in doubt.
The pythons are shown arising from
some relative of Loxocemus and thence
radiating as several groups of modern
pythons. The genus Python contains species
ranging from moderate to very large sizes,
most of which are terrestrial or terrestrial
with semiaquatic tendencies. Calabaria, a
modified burrower, is quite likely a derivative from some now extinct Python. The remaining pythonine genera form a very
broad, related group, one of whose characteristics is a rounded, shortened, and
deepened snout. Within this assemblage
the genera Chondropython, Morelia, and
Liasis (specifically Liasis amethystinus) form a
BOINE PREMAXILLA
471
tighter group of pythons, apparently quite do they climb into branches (but often do so
closely related, and displaying pronounced to feed). The young individuals seem more
arboreal tendencies, lightly built and highly arboreally inclined. Acrantophis is probably
movable skulls, and long teeth on the maxil- entirely terrestrial. Candoia is peculiar in
lae, palatines and dentaries. It appears that that it appears to be a generalist, perhaps
a close relative of these snakes gave rise to mostly terrestrial, and Eryx, which I conthe Boinae. The justification for this con- sider to be a close relative of Candoia, conclusion is based upon several lines of inde- tains several fossorial species, some of
pendent evidence including straight mor- which are very highly modified.
phological comparisons: Liasis amethystinus, The New World Boinae include the
Morelia, and Chondropython are more boa- highly arboreal Corallus which, despite
like in skull features than any other many morphological specializations, appythons, and resemble in particular the ar- pears to be the most python-like genus of
boreal boas Corallus and Sanzinia which, the group. Boa and Epicrates are basically
significantly, are the most similar boa terrestrial snakes which are also able climbspecies between New (Corallus) and Old ers, and Eunectes, the largest boine snake,
(Sanzinia) Worlds. Moreover, on the is both terrestrial and aquatic. Charina and
strength of biomechanical considerations, Lichanura are two closely related forms, but
the boine diagnostic features are readily their connection to other boine species
derived through an arboreal ancestor (see seems unclear. Hoffstetter and Rage (1972)
Frazzetta, 1975).
and Romer (1956) group them with Eryx,
The Old World Boinae form a natural but although I feel there is no particular
group according to my evidence (although reason to deny such a relationship (except
this is not in agreement with Hoffstetter on the grounds of zoogeographic probabiland Rage, 1972). Sanzinia appears to be the ity) there is no compelling reason to accept
most primitive form, and has arboreal ten- it. Exiliboa and Ungaliophis are likewise
dencies which are noticeably weaker than in difficult to derive from other genera, althe python Chondropython or the boa Coral-though the skulls of Ungaliophis which I
lus. My living adult specimens behave in a have examined contain some definite boine
quite terrestrial manner, only occasionally features (e.g., premaxillary form). Xenoboa
(Hoge, 1953) and Exiliboa have not been
included in the figure for the reason that I
ChorDta
have not had the opportunity to examine
Uettamn UngoHeehi*
the skulls.
The most critical portion of this
phylogenetic scheme, so far as the following arguments are concerned, is the origin
of the boas from the Chondropython group of
pythons. Of some importance, although
secondary compared with the first point, is
the primitive position of Corallus and Sanzinia among the boas.
THE PREMAXILLA AND OTHER SNOUT ELEMENTS
The snout bones are a complex of seven
the single, median premaxilla,
elements:
UROPELTIDAE
and the paired nasals, septomaxillae, and
DinHy.ia
'
AN.LIIDAE
vomers. As shown in Figure 1 the snout is
joined to the frontal bones of the braincase,
SNAKE ANCESTORS
is partially covered laterally and dorsally by
FIG. 2. Tentative phylogeny of pythonine and boine the prefrontals, and lies between the maxilgenera.
lae which are the major tooth-bearing
tmoetmn
fXenoprltit
472
T. H. FRAZZETTA
bones of the upper jaw. Details of the snout backward as a blade which enters between
elements can best be seen after the prefron- the paired, vertical walls of the nasals. This
tals and maxillae (and associated bones) processus nasalis—or simply, nasal
have been removed. Figure 3 shows snouts process—of the premaxilla is thus clamped
thusly exposed in a python (Python sebae) by the nasals. In boas the nasal process apand a boa (Epicrates cenchris). The snout is pears so short as to be nearly nonexistent.
movably mounted on the frontals and its
Ventrally the premaxillae of both
movements are functionally important dur- pythons and boas possess aprocessus palatini,
ing the capture and swallowing of prey or palatine process, which is formed as a
(Frazzetta, 1966). In life the snout is tied by fork with a single pair of tines. The bony
fibrous connections to its surrounding tines lie in dense connective tissue that runs
bones (such as the maxillae and prefron- from the premaxilla to the vomers. Often
tals) and movements of these bones impart, the tines are bound sydesmotically directly
via the connections, motion to the snout. to the vomer tips.
The snout bones are joined together in firm
In boas, however, the premaxilla sends a
syndesmoses, but the bones themselves are spine-like extension upward to connect
thin and flexible.
with the anterodorsal corners of the nasals;
In pythons the nasals articulate with the this processus ascendens, or ascending proupper parts of the frontals, dorsal to the cess, is absent in pythons. The origin of this
horizontal suture dividing the frontals into peculiarity in boas will be dealt with in this
upper and lower portions. In boas the na- section of the present paper. But first some
sals join the lower parts. Perhaps the most remarks concerning premaxillary function
striking difference between the snouts of should be provided to form a background
boas and most pythons is the absence of for subsequent speculations.
premaxillary teeth in the boas. Yet there
The premaxilla forms the skeletal
are other important differences.
framework of the anterior contour of the
The pythonine premaxilla is extended snout; it forms a rigid, yet stiffly flexible
support. In most pythons it bears two or
four teeth which are relatively short. The
role of these teeth in prey capture has been
discussed (Frazzetta, 1966); they are possipm tr pr.
bly most important in holding—at least
pal.pr
momentarily—portions of the prey small
enough to slip between the rows of the
larger, maxillary teeth. When imbedded in
an active prey object the premaxillary teeth
will experience forces in a forward and
paLpr. na.pr.
downward direction, and these forces will,
of course, be transmitted to the entire premaxilla and to its connections with other
snout bones.
Other forces act on the premaxillae of
potpr
both pythons and boas. Flexible ties run
from the maxillary tips to the premaxilla
(see Frazzetta, 1966) and when the maxillae
ascpr.
are thrust forward, upward and outward
these ties pull on the premaxilla. The ties
FIG. 3. Ventral and lateral views of the snout bones are taut just before the collision between
in Python sebae (upper) and the boine Epicrates cenchrisjaws and prey during the strike, and the
(lower). Processes of the premaxilla are: asc. pr., as- undamped fraction of the impulse transcending process; na. pr., nasal process; pal. pr., mitted from the maxillae produces transpalatine process; tr. pr., transverse process. Other abbreviations as in Figure 1. See the text for further verse forces on the premaxilla.
details.
The prominently anterior position of the
BOINE PREMAXILLA
473
premaxilla exposes it to a variety of situations giving rise to forces upon the bone. In
burrowing forms especially, the premaxilla
must bear the forces generated as the head
is thrust into the soil.
ps
Perhaps the largest forces which the
premaxilla and its connections to other
snout bones must bear arise in a sloppy
attack on prey. I have, quite unintentionally, filmed by slow-motion cinematography
several missed strikes among which is a
painfully (to me at least, whenever I see the
film) spectacular collision between a python
and a cage wall. Apparently the snake misjudged its distance from che prey, and a
sudden motion of the prey added to the
possible confusion. The premaxilla took
much of the impact and the snout is easily
seen to be thrust—and perhaps bent—
downward during the collision. I should
judge that an average boid individual misses at least several hard strikes during a
lifetime, and I would guess that the
mechanical trauma suffered by the pre- FIG. 4. Snout bones of Python sebae (upper), Chonmaxilla through such episodes is greater dropython viridis (center), and Corallus caninus (lower).
than that from any other sort of event. For Abbreviations as in Figure 1.
example, forces on the premaxillary teeth
arising from vigorously struggling, im- ferent. The premaxilla is smaller and venpaled prey will produce impulsive forces tral relative to a very deepened snout. This
whose peak intensity can only be so great deeper and foreshortened snout has funcbefore the penetrating teeth break. Or tional implications correlated with the
perhaps equally likely, the teeth will tear longer maxillary teeth and the highly movthrough the prey surface before the peak able jaw bones (see Frazzetta, 1975). The
force resembles that which can arise by a foreshortening presses the snout backmiscalculated strike. I emphasize these ward, between the maxillae so that the
things because a major premaxillary distinction between nearly all pythons and maxillary teeth are relatively more anterior
boas involves the presence or absence of and have a greater chance to make initial
contact with prey items having irregular
teeth.
surfaces (as possessed by all conceivable
Another distinction concerns the boine prey). The vertically expanded snout acascending process. The evolution of the as- commodates the highly arched maxillae in
cending process seems to be more com- Chondropython, and the maxillary arching
prehensible than one might expect after is related to the elongated teeth on these
only a superficial comparison between bones.
pythons and boas, although there are inIn Chondropython the premaxillary shape
teresting peculiarities in the evolutionary and orientation is adjusted to the functional
transition.
requirements of the entire snout. But this
The problem of the boine ascending pro- orientation involves a rotation of the precess can be approached through considera- maxillary bone relative to the nasals. The
tions of a morphological series such as front of the premaxilla is rotated downshown in Figure 4. In Python the premaxilla ward and backward resulting in the nasal
is prominently in front of the other snout process becoming more vertical than horibones. But in Chondropython matters are dif- zontal. In some specimens this is carried so
474
T. H. FRAZZETTA
far as literally to expose the nasal process
from between the pairs of nasal walls (as
seen in Fig. 4). Chondropython is not far from
the ancestors of the Boinae and it thus appears likely that the boine ascending process is actually the pythonine nasal process
rotated 90° in evolution.
In Figure 5 I show a more complete morphological series of snouts which roughly
reflects a phylogenetic series. As drawn, the
series shows an increasing rotation of the
premaxilla, approaching the condition in
Chondropython, and then passing beyond
that to the primitive boa Sanzinia. The condition of the premaxilla in Sanzinia is an
easy and obvious continuation of the trend
illustrated.
This interpretation of the origin of the
ascending process calls attention to the
evolutionary rotation of the premaxilla.
The premaxillary rotation raises another
issue: What becomes of the palatine process
through all of this?
For simple reasons of geometry the
palatine process during the rotation had
either to shorten and finally vanish, or continually change its site of emergence from
the transverse part of the premaxilla. The
evidence suggests that the palatine process
shortened and approached exinction during the transition. Chondropython, with the
most rotated premaxilla of any python I
have seen, possesses very short palatine-
• « palpr.
FIG. 5. Proposed morphological series—reflecting a
phylogenetic sequence—showing the alterations in
shape and position of the premaxilla and nasals. The
small arrows indicate shape changes from the preceding form.
process tines when it possesses them at all;
there is much variation here. Sanzinia bears
little more than a morphological hint of this
bony process.
Despite the apparent loss—or near
loss—of the palatine process in the early
evolving boines, both Old and New World
boines later developed a palatine process
which closely resembles that of pythons.
Clearly then, I think, the palatine process in
later boas generally must have had a
reasonably great selective advantage.
These facts seem to suggest the fabric of
an interesting question: Is the boineprocessus palatini quite the same thing as the
Pythonine's? It has arisen from a different
part of the premaxilla, and for a time at
least, the development of such a process
was suppressed.
VARIATION AND PATTERN IN THE PALATINE PROCESS
The boine palatine process must have
undergone at least a minimal alteration in
developmental mechanics, and it is surely
possible that the system of epigenetic coordinations responsible for the production of
this process was nearly obliterated but later
reconstituted on somewhat different developmental foundations. At the outset
there is no compelling reason to assume
that the developmental pattern was ruined,
especially since there are known cases (e.g.,
Kurten, 1963) where phenotypic expressions change while underlying developmental foundations are preserved nearly
intact. However, the variable patterns seen
in boine premaxillae suggest that some sort
of developmental alteration did in fact occur.
By analogy with other systems whose developmental mechanics have been studied
directly through experimental approaches,
it is reasonable to assume that the palatine
process is not a discrete developmental entity. Its form is probably determined by a
meshwork of influences molding neighboring structures.
Complexly interwoven systems often
possess marvelous capacities to adjust
themselves to varying functional require-
BOINE PREMAXILLA
475
ments during evolution without upsetting between species on some broad basis of
their basic foundations of organization. I functional adequacy within fairly narrow
have discussed this matter in some detail limits of morphological consistency,
elsewhere (Frazzetta, 1975) and have ar- whereas in boas the premaxilla cannot adgued that such systems are relatively un- just to evolutionary change in the same way.
likely to originate in evolution. The most There are other possible explanations for
flexible systems can underlie a great diver- this observed distinction between pythons
sity of adaptive forms, and they manage and boas which will be discussed, but it
this by means of what should be an obvious seems reasonable to include this consideracapacity inherent in them. They possess, in tion when framing questions because of its
their abilities to adjust to changes, a "sense" importance in other morphological sysof the physicochemical realities with which tems. The remainder of this paper dean organism must deal. In this way de- scribes the methods and results of comvelopmental integrations which are adapt- parisons of the variation in the form of the
able are effectively analogous to equations palatine process between pythons and boas.
describing physical laws which, although
derived to solve some immediate set of
problems, are often extrapolatable to new
problems. I have termed this capacity of MATERIALS AND METHODS USED IN THE COMPARISONS
biological systems the "power of adaptive
extrapolation" (see Frazzetta, 1975) beDried skulls of pythons and boas were
cause of its importance in the evolution of examined in the American Museum of
new adaptive forms which, in some ways, Natural History, the Chicago Natural Hisare almost anticipated by the system (see tory Museum, the Museum of Comparative
Cohn, 1970) in the same ways that physics Zoology (Harvard), and in my own perequations can inadvertently anticipate sonal collection. Table 1 lists the species
novel applications.
examined. Specimens whose premaxillae
An exceedingly obvious biological exam- were covered by dried fibrous tissue, and
ple of "extrapolation" is displayed in the those which had any evidence of a fracture
ability of bony tissues to organize them- occurring during life or in postmortem
selves in mechanically appropriate fashion preparation were not considered. The
in response to external stresses. An adap- species within each subfamily were broadly
tation adjusting the form of bones to the categorized as arboreal, fossorial, or terpeculiarities of an individual animal's restrial (see Table 1).
unique experience is clearly a great boon to
The palatine process of each specimen
subsequent rapid evolution of new modifi- was sketched freehand as accurately as
cations affecting and depending upon skel- could be managed. Then for each sketch,
etal form, even though the extrapolative representing a single specimen, the
propensity was originally evolved as a by- palatine process form was described by a
product of a system which could manufac- numerical scheme for six characters. The
ture continual adjustments to suit an indi- left and right halves of the process were
vidual ontogeny.
evaluated independently, thus, in all, proThe premaxiallary evolution in boids viding 12 characters. Figure 6 illustrates the
might involve some sense of extrapolation, method.
The drawings of the palatine process aland the partial loss of it in boine evolution.
The variety of adaptive strategies in ways show a ventral view, with morphologipythons is perhaps as broad as that seen in cal right and left reversed from the obboas. Yet the form of the processus palatini server's vantage point. On the right side, as
changes very little from one python species on the left, the six characters are lettered
to the next, while in boas there is greater from A-F. The condition of each character
change. Perhaps, in some manner, the is given a number which indicates the
palatine process of pythons possesses some strength or weakness of that condition. In
integrative capacity to relate to differences the first example shown in Figure 6, for the
476
T. H. FRAZZETTA
TABLE 1. List of specimens examined, grouped according to subfamily and mode of life'.
Pythons (16)
Terrestrial species (10)
Bothrochilus boa
Liasis albertisi
Liasis childreni
Liasis fuscus
Python anchietae
Python curtus
Python molurus
Python regius
Python reticulatus
Python sebae
Arboreal species (3)
Chondropython viridis
Excluding Chondropython (2)
Liasis amethystinus
Morelia argus
Fossorial species (3)
With premaxillary teeth (1)
Loxocemus bicolor
Without premaxillary teeth (2)
Aspidites melanocephalus
Calabaria reinhardti
Excluding abberant Calabaria (2)
Boas (19)
Terrestrial species (10)
Acrantophis madagascariensis
Boa constrictor
Candoia aspera
Candoia bibroni
Candoia carinata
Epicrates angulifer
Epicrales cenchris
Epicrates inornatus
Epicrates striatus
Eunectes murinus
A'
70
o
O
GAS
.29
AWH
.36
AWV
.19
ABV
.20
.17
.40
.13
.08
1
3
3
1
1
15
3
5
14
-
.55
.41
.33
.30
.38
.23
.11
.05
.46
.22
.21
.56
.60
.20
.26
.68
.25
.16
.16
.61
.45
5
2
4
10
3
2
5
93
.73
.46
.44
1.00
.46
.38
.51
.27
.70
.98
.30
.58
.35
.29
.23
1
25
1
2
1
3
Q
O
2
5
14
Arboreal species (4)
Corallus caninus
Corallus enydris
Epicrates gracilis
Sanzinia madagascariensis
6
3
1
1
Fossorial species (5)
Charina bottae
Eryx conicus
Eryx jaculus
Eryxjohni
Lichanura roseofusca
5
2
1
9
3
a
The number in parenthesis following each group designation is the number of species examined. N is the
number of specimens. See text for explanation of other abbreviations.
right side, the tine length is moderate separation of the tine from the midventral
(rated 2), the width of the single tine is line is moderate (rated 2). A similar rating
neither slender nor broad (rated 2), the tine procedure is used for the same six characis not hooked (3), and its juncture shape is ters on the left. Note character E which is
an inverted "v" (rated 4). Accessory tines the state of an accessory process. On the
are absent on the right (rated 4) and the right there is no such process (rated 4), but
BOINE PREMAXILLA
A
Tine l e n g t h
B
Tine width
C
Tins
short
•*
narrow
>
477
within a species to give a species asymmetry
score. These were then averaged for groups
(e.g., all terrestrial pythons, or all pythons) to
D Juncture shape
A -» n
n-»M
4-.0
E Accessory t i n e *
absent
*
targe
4.—»O
provide group asymmetry scores (GAS's).
F Tin
4
large
0—»3
2) Character averages and variances within
R I G H T
LEFT
species. These are computed for all speciA B C D E F I A B C D E F
B"^1"mens of each species where, for each
4 12 2 2.5
character (e.g., right "A," right "B," . . . left
"A," . . . ) , averages are taken and variances
computed.
The variances for all 12 charac|3 |4 |2
ters (2 x 6) are averaged to give an average
variance per species. These variances
FIG. 6. Characters and methods of analysis used in themselves may then be averaged within
the present study. See text for explanation.
groups (e.g., terrestrial pythons) to give average within-group variances (AWV's).
on the left a moderate development of one
3) Character variances between species. T h e
is seen (rated 2). The "E" squares are average score for each character within a
shaded because they show the character to species is compared with that of other
be asymmetrical when right and left sides species so that, for all species in a group, the
are compared. The numerical value of average scores provide a variance for each
this asymmetry is the difference between character. These variances are then averright and left "E" characters, which in this aged for all species and all characters in the
case is 2. But this is not the only asymmetry group to give average between-group varpresent in this example. The "A" squares iances (ABV's).
are also shaded. Character "A," tine length,
4) Average diversity within species. This calis noticeably different between right and culation is based on the Shannon-Weaver
left tines. The left tine is shorter but not so formula// = -S^jlog,,/^ where, in this case,
much shorter that it falls into a different pi is the frequency of the ith kind of score in
length class from the right tine. Both tines a set of s different kinds of scores. The
fall within the range of a "2" length, but the method finds H for a species by computing
fact that they nevertheless are visibly dif- H values for each character and averaging
ferent is recorded by the placement of a plus them (12 characters). These form the basis
sign in the left "A" box. Plus-sign differ- for calculating within group averages for//
ences are counted as V2 a point and, hence, (AWH's).
the total asymmetry value is figured as 2.5.
The first method utilizes all specimens,
This method of numerical description and considers the minor differences bewas adopted after other, seemingly more tween left and right sides which are desigobjective methods were attempted. Direct nated by plus signs (see Fig. 6 and remarks
measurements of different premaxillary above). These minor differences are disreparts possessed a serious, hidden subjectiv- garded in the remaining three methods
ity: in very different premaxillae, where do (e.g., in terms of Fig. 6, 2 and 2+ are reyou measure to take consistent and com- garded as identical in the last three
parable data? Also, shape differences often methods). Also, in the last three methods,
eluded the direct-measurement scheme. not all specimens are used since species
Comparison of areas, worked out by stan- represented by fewer than 2 specimens
dardizing sketch sizes and employing a cannot be included.
planimeter, was fleetingly considered. This
Diversity figures are based on the total
method could give identical numbers for number of characters (12) for each species
very different premaxillae.
having two or more representatives. PossiThe character scores were handled by bly diversity indices are more meaningful
than variances as calculated for AWV's
several methods:
1) Asymmetry scores. The scores for eachsince variances have a slight correlation
specimen were averaged for all specimens with the mean.
w
stroightness
straight
•
*
long
width
hooked
478
T. H. FRAZZETTA
Attempts to show relationships of premaxillary features to the size of the specimen yielded no correlation. However, it
should be noted that few juvenile specimens are present in museum skeletal collections.
The four methods are intended to display tendencies in boas toward greater
asymmetry or greater variation than in
pythons. The results are shown in Tables 1
and 2.
It is difficult to perform statistical
analyses on the data for several reasons.
The numbers of specimens representing
some species is meager. The number of
species within groups must form the sample size in certain comparisons, even when
many specimens are involved, and this interferes with sharp statistical discrimination. I have attempted, nevertheless, some
simple tests using Student's "t" and "F" tests
(Table 2) which are fairly robust.
The considerable constraints affecting
this part of the study leave the major questions outside the perimeter of positive,
statistical resolution. Yet the data are
suggestive, largely consistent and, at times,
have at least some shreds of statistical support.
DISCUSSION OF RESULTS
My comparisons between pythons and
boas reveal that the palatine process in boas
TABLE 2. Results of comparisons between groups*.
Asymmetry (GAS)
Python vs. Python
Arboreal pythons
) Terrestrial pythons
Fossorial pythons
) Terrestrial pythons
Fossorial pythons (without premaxillary
teeth)
) Terrestrial pythons
Boa vs. Boa
All boas
) Arboreal boas
Terrestrial boas
) Arboreal boas
Python vs. Boa
All boas
All pythons
Terrestrial boas
Terrestrial pythons
Fossorial boas
All pythons
Fossorial boas
Fossorial pythons (without
premax. teeth, and excluding aberrant Calabaria)
Variance within species (AWV)
Python vs. Boa
All boas
Arboreal boas
Variance between species (ABV)
Python vs. Python
Fossorial pythons
Fossorial pythons (without
premaxillary teeth)
Fossorial pythons (without
premax. teeth, and excluding aberrant Calabaria)
Python vs. Boa
All boas
Terrestrial boas
.01
.03
.03
.08
.04
.01
.01
.04
.10
) All pythons
) All pythons
.05
.05
) Terrestrial pythons
.05
) Terrestrial pythons
.05
) Terrestrial pythons
.10
) All pythons
) Terrestrial pythons
.05
.01
a
Only those comparisons achieving no more than the . 1 probability level are shown. These levels are indicated
for each match on the right. The inequality sign (>) shows that the group on the left in each comparison has a
greater expression of the trait (e.g., greater asymmetry, greater variance, etc.) than the right-hand group.
BOINE PREMAXILLA
has a greater tendency toward asymmetry
and variation. For example Table 1 shows
group figures for the average asymmetry
and average diversity of premaxillary
types. I take the observed variations to
suggest some greater looseness in the developmental control of the palatine process
of boas. This latitude in premaxillary form
could presumably exist because selection
specifies no narrow limits on the palatine
process, or because the developmental
program does not have precise enough
heritability to permit a careful response to
selection pressure (e.g., see Kurten, 1957).
In either case, but for rather different
reasons, there is demonstrated an instability in pattern. A third possibility is that the
premaxilla is subjected to fluctuating selection pressures as in certain "patchy" environments (see Levins, 1968). This seems
highly unlikely.
Asymmetries in animals can often be the
capital for adaptive success, and examples
range from fiddler crabs to flounders. In
other instances there appears to be no obvious adaptive basis for asymmetries. This is
especially the case where the asymmetry is
mild and does not correlate with the functioning of the system. Any snake that strikes
from an S-shaped loop necessarily employs
an asymmetrical approach in attacking the
prey. But until it can be shown that individuals strongly favor a "right-" or "lefthandedness" in forming the loop, and that
such "handedness" relates to the premaxilla, and that other feeding functions
favor a strong left- or right-oriented procedure enhanced by or causing an asymmetrical premaxilla, it seems most reasonable
to regard asymmetry in this case as
nonadaptive. So long as the asymmetry
does not transcend certain limits, the system will not often shift significantly from
the nonadaptive to the inadaptive.
Table 1 shows that when all Pythons are
compared to all Boas, there is seen a noticeably greater asymmetry in boas. The same
tendency is present in the terrestrial and
two of the fossorial group comparisons.
The fossorial pythons are treated in several ways. In one, all fossorial species are
lumped together. A second treatment
excludes Loxocemus to leave those forms
479
lacking premaxillary teeth. These two remaining genera (Aspidites and Calabaria) are
the only pythons lacking these teeth, and it
is important to set them out for comparison
with the boas. The asymmetry score for this
group is .60, considerably higher than for
most other pythons and comparable with
that for fossorial boas (.58). Small sample
size makes the group score sensitive to
single aberrant members. The group
members overall display low degrees of
asymmetry, but one member {Calabaria
reinhardti, CNHM 31372) possesses a conspicuously aberrant premaxilla. When this
individual is removed from the sample, the
asymmetry score for the group drops to
.25. Obviously, it is inappropriate to eliminate a specimen because doing so smoothes
the results, but neither is it correct to disregard the influence of a single, unusual
specimen has on the analysis.
Arboreal pythons are grouped in two
ways, one which includes Chondropython and
one which does not. This was done because
Chondropython adds tremendous asymmetry
to the group; it is at the point of extreme
premaxillary rotation, and the palatine
process shows signs of serious disruption.
Among the boas the arboreal group
shows the least asymmetry. This is a peculiar result, not only because there are no
obvious functional grounds suggesting why
in arboreal boas a symmetrical premaxilla
has a high adaptive priority, but because
other measures of instability are not corroborative. Arboreal boas seem to constitute a singular example in this regard.
Table 2 shows the results of comparisons
made according to methods given in the
preceding section of this paper. Only those
comparisons where boas can be shown to be
more unstable in premaxillary pattern by
no more than a .10 probability level are
indicated. The small sample sizes in many
of the groups robs many comparisons of
statistical confidence, and leaves only these
relatively few matches for consideration.
This factor, the broad probability level, the
need for multiple usage of certain groups,
and other limitations already noted gravely
trouble attempts to draw conclusions. The
information in Table 2 can thus only be
suggestive, but it is aligned with a strong
480
T. H. FRAZZETTA
consistency which is evident in most of the
entire array of data.
The broadest statement suggested is that
there is greater pattern of instability in the
boine premaxilla. When the aberrant
specimen of Calabaria is eliminated from
the python group lacking premaxillary
teeth, it is barely within the acceptable limit
as more stable than fossorial boas. However, when the most variable fossorial boine
specimen is removed from that sample, the
comparison falls just outside of the . 1 level.
There are thus no strong indications that
"toothless" fossorial pythons have greater
stability than boas although many of the
relevant data lean in this direction.
Boa groups display a greater betweenspecies variance in many comparisons with
pythons suggesting that, for boas more so
than for pythons, the evolution of each
species required a pattern revision of the
premaxilla. If this interpretation is correct,
it carries the possible implication (consistent with others) that the form of the boine
premaxilla is under firm selection in the
boas. Another possibility, perhaps an alternative, is that the complex of developmental influences on the premaxilla changes
with each newly evolved species, and the
form of the bony process is effectively buffeted about. In either case there is a general
difference between boas and pythons.
The premaxillary-toothless pythons are
unusual among the pythonines surveyed in
their high between-species variance. This
feature might be related to their lack of
premaxillary teeth, or to the fact that, as
burrowers, the premaxillary bone performs functions unlike those in other
pythons. There exist enough such points of
confusion that speculations related to the
premaxillary differences between pythons
and boas must be framed with deliberate
caution.
However, the total array of evidence,
though not particularly strong in any one
spot, seems not to support solidly the interpretation that the differences are simply
due to the presence or absence of premaxillary teeth. This point could be settled more
conclusively were there more than two
species of premaxillary-toothless pythons.
But casting some further doubt on an ex-
planation focusing narrowly on the presence
or absence of teeth is the consideration,
noted above, that premaxillae must resist
far greater forces than those associated
with the function of teeth.
It thus appears that a basic factor in the
differences studied is possibly that the
boine premaxilla, in its early evolution, suffered significant disruption in the developmental program affecting the
palatine process. The program in pythons
is likely one of very longstanding, present
in remote snake ancestors, whereas in boas
the reconstituted program is relatively recent. Had there been strong selection for
stability in boine premaxillae it is indeed
possible that much greater pattern stability
would have been attained (but this need not
be so as shown by Kurten, 1957). The fact
that arboreal boas have low asymmetry
scores may be a case in point (although their
primitive position raises interesting conjectures in this regard).
Greater pattern stability in the pythons
does not necessarily suggest a firmer guidance by natural selection. There is probably nothing very inadaptive in the minor
pattern deviations studied in this paper, but
the python premaxilla and premaxillary
region, having been under selection for a
very long time could have achieved a greater refinement in developmental stability
nevertheless. This could have come about
by continued selective elimination, through
many generations, of rare deviant individuals whose unstable developmental
program transcended the limits of selective
tolerance. This mechanism could lead
slowly toward a precise canalization.
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