Download Sexual dimorphism of cranial suture complexity in wild sheep (Ovis

zoological ~7uuurnalof the Linnean Sociely (1989), 95: 273-284. With 3 figures
Sexual dimorphism of cranial suture
complexity in wild sheep (Ouis orientalis)
CAROLYN RENZULLI JASLOW*
Department of Anatomy, 'The Unitlersity of Chicago, 1025 E 57th St., Chicago,
Illinois 60637, U.S.A.
Received September 1987, accepted for publicataon M a y 1988
Sutural complexity (the degree of interdigitation) of 13 cranial sutures was compared betwern male
and female wild sheep (Ovls orientah) to investigate a morphological feature that is potentially
impokant with respect to stress transmission in the skulls of males during fighting. Most facial sutures
(four of six) were not sexually dimorphic, but two sutures, the maxillojugal and jugolacrimal, had
greater complexity in males than in females, suggesting that significant forces may be transmitted
through the facial region of rams, most likely during horn clashing. Most of the brainrase sutures (five
of seven) were more complex in males than in females, and different factors appear to underlie this
sexual dimorphism. In females, increased complexity of sutures during ontogeny was predicted best
by variables measuring growth of the skull, brain or face, while in males, changes in complexity were
predicted best by variables representing mechanical loading and frontal bone growth.
KEY WORDS:-Cranial
sutures
sexual dimorphism
~
Ovis
~
functional morphology
~
ontogeny.
CON'I'EN'I'S
Introduction . .
Methods . . .
Results
. . .
Discussion.
. .
Facial sutures.
Braincase sutures
Acknowledgements
References.
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273
275
278
280
280
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283
283
INTRODUCTION
Of all the horned Bovidae, the male wild sheep (Tribe Caprini; Subfamily
Caprinae) are the best known for their massive horns, and for the use of their
horns in intrasexual battles and displays (Geist, 1971; Schaller, 1977). During
highly ritualized battles called clashes, two males rush at one another and collide
horn to horn or horn to head (Geist, 197 1). The outcomes of these contests usually
determine a dominance hierarchy that is important to the fitness of the rams
because dominant individuals will breed with most of the females during the rut
(Geist, 1966a).
*Prrsrnt address: Biology Departmrnt, Rhodes Collegr 2000 N. Parkway, Memphis, ' I N 381 12
+
0024-4082/89/040273 12 $03.00/0
273
01989 The Linnean Society of London
274
C K JASLOW
‘I’he head-to-head clashes of male wild sheep are thought to exert considerable
forces on the horns and skulls of these animals. Theoretical values of impact force
during fighting have been estimated to be as high as 3 kN for sheep (Kitchener,
1988). These high impact forces, together with the weight of the horns themselves,
which can be up to 80/, of an animal’s body weight (Geist, 1971), represent
unusual loading conditions that are assumed to influence skull design in sheep.
Because the large horns and the fighting behaviour are sexually dimorphic,
comparisons of skull morphology between the large-horned males that fight often
and the small-horned females that rarely fight should help to highlight the cranial
features of male sheep that are adapted to withstanding these loads. Studies by
Schaffer (1968) and Schaffer & Reed (1972) identified enlarged horn cores and
sheaths, a ventral orientation of the occipital condyles beneath the horn bases,
and enlarged frontal and cornual sinuses as some of the cranial specializations of
rams thought to be functionally important when the head is loaded during
fighting. Yet there is one feature, the cranial sutures, that has been ignored in
studies of caprine functional craniology, even though the sutures are thought to
have important functions during skull loading in other vertebrates (Herring,
1972; Gans, 1960, 1974).
A cranial suture is the joint between the bones of the skull, and it includes both
the connective tissue between the bones and thc adjacent edges of the bones
themselves (called the rutural area by Moss (1957)).T h e opposing bony surfaces
of a suture may be straight-edged (forming a butt-joint) or they may overlap
(forming a bevelled joint), and either type of suture may be secondarily modified
by the formation of interdigitations during ontogeny (Moss, 1957). Although
5ome general characteristics of sutures are intrinsic (i.e. genetically determined)
(Moss, 1957; Oudhof, 1982), in rats, the ontogenetic transformation of sutural
morphology from simple to complex (interdigitated) has been shown
experimentally to be determined by extrinsic forces acting on the sutures (Massler
& Schour, 1951; Moss 1957, 1961). While little is known about the magnitude or
the frequency of forces that would be necessary to cause this transformation,
relatively infrequent exposure to physiological loads has been shown to be
sufficient to produce substantial periosteal and endosteal bone deposition in limb
bones (Rubin & Lanyon, 1984). Consequently, forces that load the cranial
sutures infrequently and/or irregularly, such as the forces generated by head
butting, may be sufficient to induce bone formation and increase the complexity
of the sutures.
Regardless of whether complex sutures are induced by extrinsic forces, as
suggested above, or are simply the byproducts of developmental changes in the
skull, certain mechanical advantages are correlated with the transformation of the
sutures from simple to complex. Experimental tests have shown that increased
complexity provides a suture with greater bending strength, and allows it to
absorb more energy during an impact blow Uaslow, 1987). Associations between
inrrcased complexity of sutures and particular mechanical properties have been
used previously to analyse cranial morphology and function among diverse
species. For example, Herring (1972) used sutural morphology to interpret both
the intensity and the direction of stress in the skulls of the Suina (pigs and
peccaries), and Gans (1960, 1974) noted that the most complex cranial sutures of
amphisbaenid reptiles are oriented to resist the high torsional stresses that are
transmitted through the skull when an animal is burrowing.
SEXUAL DIMORPHISM IN SHEEP CRANIAL SUTURES
275
The goal of this investigation was to examine the ontogeny and distribution of
complex sutures on the skulls of male and female wild sheep to provide insight
into the relationships between cranial design and the forces that load the skulls.
Two approaches were used to assess the factors related to changes in sutural
complexity. First, I tested the hypothesis that sutural complexity was greater in
adult male than adult female sheep, and I identified significant differences in
complexity among the sutures of the rams' skulls. These comparisons of sutural
complexity between sexes, and among sutures within males, were used to generate
hypotheses regarding the relative magnitude of local stresses and the routes of
stress transmission through the skull. Second, I tested the hypothesis that sexual
dimorphism in sutural complexity is correlated with sexual dimorphism in skull
loading, as measured by horn size and fighting behaviour variables. Because male
and female sheep differ in rates of growth as well as the degree of mechanical
loading, I determined the best correlation between ontogenetic changes in sutural
complexity, and either growth rates or mechanical loading. This was done
indirectly by ( 1 ) assuming that certain ontogenetic changes in cranial
morphology were associated with either growth or mechanical loading, and then
(2) calculating which of these types of changes best predicted increased sutural
complexity.
METHODS
Ovis orienlalis, the urial from Asia, was the wild sheep species chosen for Chis
study because the cranial sutures of both males and females generally remain
patent (unfused) throughout the lifetime of an animal. Although there are only a
few observations of intraspecific fighting behaviour between urial rams (Schaller,
1977; Decker, 1972), this species, like all other sheep, engages in ritualized headto-head clashing (see Geist (1971) and Schaller (1977) for reviews of agonistic
behaviour in Ovis).
External complexity (the amount of interdigitation) was measured for each of
thirteen sutures on the dried skulls of 20 male and 22 female 0. orientalis. Sutural
complexity was defined as total sutural length, following the curves of the suture,
divided by its direct length, the shortest distance from start to end of the suture
along the surface of the bone (Fig. 1A). If the bone and suture were curved, direct
length was determined as the sum of the lengths of each straight section (Fig. 1B).
Sutures were traced onto pieces oftransparent tape which had been placed on the
skulls of the sheep. These traced lengths were then quantified using a digitizer
interfaced with a microcomputer. In this study of intact skulls, only external
sutural complexity was measured, even though sutural morphology may also vary
internally, and it is possible that the measures of the external surface do not
completely reflect the overall complexity of the entire suture. T h e sutures that
were chosen for study are shown in Fig. 2. Seven of the sutures were located on the
braincase, a region that is probably subjected to intermittently heavy mechanical
loading throughout the adult lifetime of a male sheep because of fighting and/or
inertial forces associated with movement of a head bearing large, heavy horns.
These sutures, the frontojugal, frontolacrimal, frontonasal, frontoparietal,
interfrontal, parietosquamosal, and parietosupraoccipital, were expected to be
sexually dimorphic and correlated with the differences in horn size and fighting
behaviour between males and females. The remaining six sutures (intermaxillary,
C. R. JASLOW
276
SL
~
A
DL
SL
B
Figure 2 . Measurrrnents used to calculate sutural complexity dcfined as the ratio of sutural length to
direct length. A, SL=sutural length; DL=direct length; B, D L = t h e sum of the lengths of each
straight section ( I 2 + 3 ) .
+
Figure 2. Skulls of adult male sheep ( 0 .orientals) in A, lateral (postorbital bar removed), B, posterior,
and C, ventral views showing the sutures measured. Abbreviations of cranial bones: f = frontal;
j =jugal; I = lacrimal; m = maxillary; n = nasal; pl =palatine; pr = parietal; sq = squamosal;
s u = supraoccipital.
SEXUAL DIMORPHISM IN SHEEP CRANIAL SUTURES
277
internasal, jugolacrimal, maxillojugal, maxillolacrimal, and maxillopalatine) are
located in the facial region. In contrast to the braincase, the facial region does not
bear the horns nor does it receive direct blows during fighting. Thus, the facial
sutures would be expected to have experienced similar forces in both males and
females.
Age was estimated for each sheep skull according to a key of tooth wear
patterns described for Turkish goats (Deniz & Payne, 1982). No differences were
found between the ages estimated using this key and ages estimated from counts of
horn rings in males and in females with clearly marked horns. Horn-ring counts
alone are accurate measures of age for male wild sheep, but cannot be used
consistently for both sexes because the rings are usually obscured on the horns of
older females (Geist, 196613).
For each skull, measurements were also made of five cranial features thought to
be important with regard to skull loading by either mechanical forces or skull
growth (Fig. 3 ) . A measurement of horncore length was chosen to estimate
mechanical loading by weight of the horns, and also by fighting, because sheep
with larger horns fight more often and more intensely (Geist, 1971). Four
additional cranial measurements were chosen to characterize the relatively
complex growth of the caprine skull. Skull length measurements were used to
estimate the influence of increased cranial size on sutural complexity, and to
determine if sexual dimorphism in sutural complexity occurred simply because
males tend to grow larger skulls than females do. However the skull can be
divided into two functionally different regions, the neurocranium (braincase) and
the splanchnocranium (facial region) (van der Klaauw, 1946), which have
different growth rates. Splanchnocranial or facial length was measured to
Horncore L
.*-.-a
'..
Faciol L.
-
1
Skull
L { -
I
Figure 3. Midsagittal view of the skull of an adult male sheep (0.07ien2alis) showing cranial
measurements. Brain V(o1ume) =volume of the region formerly occupied by the brain. Facial
L(ength) =distance from the posterior molars to the anterior edge of the premaxilla. Frontal
L(engthj = midline distance from the frontonasal suture to the frontoparietal suture. Horncore
L(cngthj = distance from horn base to tip along the anterior surface. Skull L(ength) =distance from
occipital condyles to the anterior edge of the premaxilla.
278
C KJASLOW
determine if growth in this cranial region could be correlated with increased
sutural complexity, especially among the facial sutures. Growth of the
neurocranium was more difficult to estimate because the frontal bones, which
make up much of the braincase of caprines, have large sinuses that widely
separate the inner and outer tables of bone. Expansion of the inner table of the
braincase (brain growth) was determined from measurements of brain volume,
which were transformed by taking the cube roots to render them metrically
compatible with the linear measurements. Frontal length, measured along the
midline from the frontonasal suture to the frontoparietal suture, was used to
estimate the expansion of the outer wall of the braincase, which supports the
horns.
t-Tests (program BMDP3D, Dixon, 1983) were used to compare the
complexity of each cranial suture between juvenile male ( n = 4 ) and juvenile
female ( n = 5) sheep (juveniles were classified as animals less than two years old) to
determine if sexual dimorphism in sutural complexity existed before the onset of
sexual maturity. Complexity of each suture was then compared between adult
male ( n = 9 ) and adult female ( n = 7 ) sheep (adults were classified as animals
greater than four years old), again using l-tests (program BMDP3D). Because
several t-tests were performed for each age group, a minimum significance level of
0.005 was used (approximately equal to 0.05 divided by the number of tests).
Sutures in adult males that were significantly more complex than those in adult
females were then tested for intersutural differences in complexity within males.
To do this, values of complexity for adult males were log-transformed to equalize
the variances, and a two-way mixed-model analysis of variance (ANOVA)
without replication was performed (Sokal & Rohlf, 1969). Subsequently, the data
were examined with an a poskeriori Student-Newman-Keuls (SNK) test (Sokal &
Rohlf, 1969) to find which sutures differed.
To determine which ontogenetic changes in skull morphology (related either to
growth or mechanical loading) best predicted sutural complexity for each sex, the
complexity of each cranial suture was regressed independently for males and
females against the log-transformed values for age and the five cranial variables.
All-possible-subsets regressions (program BMDP9R) were performed to obtain
linear combinations of variables to predict complexity. For each suture, the subset
of predictor variables that minimized the total squared error (Mallow’s Cp) and
also had statistically significant l-values for each regression coefficient, was
selected as ‘best’ (Dixon, 1983). Mallow’s Cp was chosen as a selection criterion
instead of the more familiar R2 (squared multiple correlation) because R2 is
highly dependent on subset size, and the C p value is not (Hocking, 1976). A
stepwise regression (program BMDP2R) was also performed to confirm these
results and to verify the significance of the regression coefficients. For each suture,
thc stepwise program produced a plot of the residuals versus the predicted values
that was visually inspected for obvious trends. A trendless plot indicated that the
regression equation adequately explained the patterns in the data.
KESULI’S
Sutural complexity among all sheep ranged nearly an order of magnitude from
a minimum value of one (essentially a straight line with no interdigitations) to a
maximum of about nine (sutural length= nine times the direct length). Juvenile
SEXUAL DIMORPHISM IN SHEEP CRANIAL SUTURES
'I'AHI.F,
279
1. (-'l'ests of'diffcrences in sutural complexity between adult male
aiid adult fcmalc shccp. \'alucs arc nicaiisk S.E. i n )
Males
Females
/-values
RrainraJe sutirrvs
Frontojug-al
Fr(riitolacrima1
Fronmnasal
Frorr t(rparict;il
I ntrrlroii tal
Pa rictosq uamosal
I'arirtosupraorcipital
3.28k0.33 (8)
2.24k0.18 (9)
l.6 6 f 0 .1 3 (9)
5.48k0.80 ( 7 )
5.41k0.49 (9)
1.77k0.09 (9)
2.23+0.15 (9)
2.74k0.23 ( 7 )
1.29k0.09 (7)
1.27k0.05( 7 )
2.29k0.23 ( 7 )
1.66k0.15 ( 7 )
1.23k0.03 (7)
1.29kO.10 (6)
1.32
4.22**
2.75
3.84*
7.25**
5.50**
4.49*
l.'acial .tuturuc
I ntcrmaxillary
Internasal
Jugolacrimal
Maxillojugal
Maxillolacrimal
Maxill(ipalatine
1.07 k 0.02
1.03+0.01
2.50&0.19
1.34f0.04
2.08+0.16
1.33k0.03
1.03+0.01 (7)
1.02k0.00 ( 7 )
1.36k0.05 ( 7 )
1.18k0.02 ( 7 )
1.66k0.12 ( 7 )
1.28k0.03 (7)
1.41
1.12
5.68**
3.66*
2.00
1.11
(9)
(7)
(9)
(9)
(9)
(9)
* P < 0.005,
**P < 0.0005.
male and juvenile female sheep had very simple sutures, with mean complexity
values always between one and two (except for the frontojugal suture). No
significant differences between juvenile males and juvenile females were found for
any of the 13 sutures. In contrast, among adult sheep, seven of the 13 sutures
studied were significantly more complex in males than in females, and five of these
sexually dimorphic sutures were braincase sutures (Table 1). Adult females never
exhibited more complex sutures than did males.
While sutures of male sheep were more complex than those of females, their
P<O.OOl). Four ranges of
degree of complexity was variable ( F = 76.49,,,,,
complexity were statistically distinguished from one another using the a posteriori
SNK test (Table2). Although the two most complex sutures of males were
braincase sutures, a facial suture, the jugolacrimal, occurred in the group with the
second highest level of complexity.
TABLE2. Levels of complexity for
sexually dimorphic sutures of adult male
sheep ( w = 9) based on the (I posteriori
SNK test. Each level from 1 (most
complex) to 4 (Icast complex) contains
sutures that were not significantly
different at the 0.05 level
Level
Sutures (mean complexity)
Frontoparietal (5.48)
Interliontal (5.41)
2
Jug-olacrimal (2.50)
E'ronlolacrimal (2.24)
1'arietosupraocc.ipital (2.23)
3
l'arietosquamosal ( I .77)
4
Maxillojugal (1.34)
C. R. JASLOW
280
TABLE
3. Results of regressions r u n to predict sutural complexity in male a n d
ternale sheep. For each suture, only thc names of the independent variables i n t h e
“best” subset o f t h e regression a r e listed with t h r R 2value in parentheses. A d a s h
indicates that n o regression was significant a t the 0.05 level
__
Variables in “best” subsets
Males
Females
Braincase .sutures
Front njugal
Frontolacrimal
Frontonasal
Fronroparietal
lntcrfrontal
Parietosquaniosal
Parietosupraoc.c.ipital
Frontal L. (0.50)
Frontal L. (0.45)
Frontal 1.. (0.41)
Frontal L. (0.71)
Frontal L. (0.50)
Horncore L. (0.57)
Facial L., Horncore L. (0.60)
Brain V. (0.27)
Skull L. (0.21)
Age, Horncore L. (0.36)
Facial s u h r r s
Iritcrmaxillary
Internasal
,Jugolacrinial
.Maxillojugal
Maxillolacrimal
Maxillr)palatinr
Skull L. (0.33)
Horncore L. (0.44)
Horncore L. (0.39)
Age (0.20)
Age, Skull L., Brain V. (0.36)
Frontal L., Skull L. (0.42)
Age (0.29)
Facial L. (0.23)
Age (0.23)
Table 3 shows the results of the regressions run to predict sutural complexity
using age and the five cranial variables. In all cases, the results of the all-possiblesubsets and stepwise regressions coincided, and plots of the residuals exhibited no
apparent trends. Significant relationships between sutural complexity and at least
one independent variable were found for ten of 13 sutures in males and nine of 13
sutures in females. Only twice was complexity predicted by the same variable for
both sexes. Among females, complexity of most sutures was best predicted by age,
or by growth of the skull, brain or face. Among males, complexity was usually best
predicted by frontal length and horncore length.
DISCUSSION
Facial sutures
Although four of the six facial sutures showed no sexual dimorphism in
complexity among adult sheep, the greater complexity of the maxillojugal and
jugolacrimal sutures in males suggests that part of the facial region experiences a
different loading regime in males than in females. There are several factors that
can produce forces in the facial region of ungulates which may be associated with
increased complexity of the sutures. Herring ( 1972) diagrammed hypothetical
stress trajectories in suoids (pigs and peccaries) that would result from
compressive loading of the posterior molars or from the pull of the masseter
muscles during mastication. Although both of these activities would produce
stress trajectories that intersect the maxillojugal and jugolacrimal sutures, it is
unlikely that male and female sheep have masticatory activities that differ
sufficiently to produce the observed sexual dimorphism in sutural complexity. I n
fact, all other facial sutures did not differ in complexity between male and female
SEXUAL DIMORPHISM I N SHEEP CRANIAL SUTURES
28 1
sheep, including the intermaxillary and maxillopatatine sutures that also had
been hypothesized by Herring (1972) to play a role in stress transmission during
mastication. More likely, the greater complexity of the maxillojugal and
jugolacrimal facial sutures in males is associated with the differences in horn size
and fighting behaviour between males and females. This was inferred from the
results of the regression analysis, which showed that horncore length, believed to
reflect skull loading by inertial forces associated with horn weight and size, as well
as by dynamic forces correlated with fighting, was the best predictor of complexity
for these two sutures in male sheep. I n contrast, any significant regressions for
other facial sutures of either males or females selected age or facial length as the
best predictors of complexity. These results indicate that the facial sutures of male
sheep not only receive stresses correlated with growth and probably mastication,
but that mechanical ioads from fighting, or perhaps bearing the weight of the
horns may be transmitted into the facial region of rams via the maxillojugal and
jugolacrimal sutures. Furthermore, because one of the facial sutures, the
jugolacrimal, had a relatively high level of complexity in adult male sheep
(Table 2 ) , local stresses experienced by this part of the face may be quite large
during an impact blow. This hypothesis remains to be tested.
Braincase sutures
Two types of extrinsic forces exist that may be expected to load braincase
sutures and cause an increase in their complexity. T h e first of these are forces
caused by the growth of local tissues. Massler & Schour ( 1951) claimed that brain
growth and concurrent expansion of the cranial vault were responsible for
producing normal transitions of rat coronal and sagittal sutures from a simple to a
highly interdigitated morphology. In humans with hydrocephaly, certain cranial
sutures show notably greater complexity (Walker, 1961). Under these conditions,
it has been hypothesized that forces load the periosteum of the sutures via the dura
mater during growth (Massler & Schour, 1951; Moss & Young, 1960). T h e
second group of extrinsic forces that may load the skull and cranial sutures are
those resulting from external mechanical loading. This is a broad category
because it includes forces caused not only by activities that are common to most
animals (e.g. mastication, muscle activity), but also by activities that are
specialized, and which represent unusual modes of skull loading (e.g. burrowing,
head-butting). Experimental data, again limited to rats, have shown that removal
of the temporalis muscles (Moss, 1961) or the temporalis and posterior neck
muscles (Washburn, 1947) produces cranial sutures that lack normal
interdigitation. In addition, extrinsic cranial trauma during development in
humans is thought to affect sutural complexity because skulls with particular
occipital deformations were observed to have more complex lambdoidal sutures
than did undeformed skulls (Gottlieb, 1978).
Five of the seven braincase sutures exhibited greater complexity in male than in
female sheep. This sexual dimorphism in complexity may reflect differential
mechanisms of loading the sutures (e.g. males fight and females do not), or
alternatively, that the sutures of males and females could be loaded by the same
mechanism but with differing intensity (e.g. different growth rates). Although
experimental data would be necessary to identify conclusively the appropriate
causes for increased sutural complexity in sheep, in the present study, comparisons
282
C R. JASI.OW
between males and females of the regression variables that best predicted
braincase sutural complexity were used to hypothesize causative relationships.
Because complexity was best predicted by different independent variables in
males versus females (Table 3 ) , differcnt mechanisms for loading the suturcs are
hypothesized to underlie this sexual dimorphism. T h e most likely difference
would be the presence or absence of extrinsic skull loading by inertial forces
associated with swinging the horns and/or impact loading during fighting.
The regression results revealed that in female sheep, ontogenetic changes in
several variables, such as age or growth of the brain, skull and face, were the best
predictors of increased sutural complexity. I n contrast, only two morphological
variables, frontal length and horncore length, best predicted increased complexity
of the braincase sutures in rams. Since frontal length was the single best predictor
of increased complexity for most of the male braincase sutures, factors affecting
the size or shape of the frontal bones may also play key roles in altering sutural
morphology. T h e frontal bones bear the horns in sheep, so when the rams’ horns
enlarge rapidly in length and circumference with increased age, the frontal bones,
which are fused to the horncore bases, grow rapidly as well. This growth of the
frontal bones and horn bases in male sheep may itself stimulate increases in
braincase sutural complexity, or may simply correlate with the increases in
external mechanical loading that occur during a ram’s lifetime. In addition, these
external mechanical forces, which are generated by the weight of the heavy horns
or by impact blows to the horns and skull, must produce considerable stresses in
the frontal bones of the male sheep. Because stress is generally believed to induce
osteogenesis and remodelling of bone (see Currey, 1984), this mechanical loading
may itself cause some growth in the frontal bones that correlates with the increases
in braincase sutural complexity. Whether increased complexity is actually
induced by forces experienced throughout a n animal’s lifetime, or is merely a
developmental change that has been genetically programmed over evolutionary
time, complex sutures are still stronger, and capable of absorbing more energy,
than simple sutures Uaslow, 1987). Both of these properties are probably
advantageous during mechanical loading of the skull.
The frontojugal suture on the postorbital bar was the only braincase suture of
adult sheep that showed no sexual dimorphism in complexity. This would
indicate that male wild sheep probably do not transmit significant forces from
fighting through the postorbital bars, although there may be another source of
loading common to male and female sheep that is great enough to mask the effects
of skull loading during fighting. Because the frontojugal suture was relatively
complex in adult and juvenile sheep of both sexes, it may likely experience
considerable skeletal stresses from other activities, such as mastication, that are
common to males and females of all age groups, and which may transmit forces
through the postorbital bars (e.g. Greaves, 1985).
The observed sexual dimorphism in complexity of most braincase sutures is
thought to reflect differences in overall skull loading between male and female
sheep. Moreover, the variation in complexity among the sutures of male sheep
suggests that the patterns of skull loading are not uniform. Assuming that all
sutures respond the same way to particular loads, differences in complexity may
show that the sutures have experienced different types of loads (c.g. tensile us.
compressive) and/or different levels of stress. If the magnitude of stress is
important, this would suggest that the interfrontal and frontoparietal sutures are
SEXUAL D I M O R P H I S M I N SHEEP CRANIAL SUTURES
283
those most highly stressed on the skull, because these sutures were the most
complex. Following this line of reasoning, other braincase sutures which have
lower complexities may not have encountered such high stresses because they lie
further from the horns, or because they have a different orientation on the skull
relative to the direction of loading. These hypotheses concerning the magnitude of
stress transmitted through the skull need to be tested by direct measurements of
strain (local deformation) in the cranial bones and sutures during in vilro loading
of the horns. With this information, a much clearer picture may be obtained of the
functional significance of sutures and of cranial design in sheep during impact
loading of the skull.
ACKNO~YLEL>(:EMENTS
I wish to thank R . Timm, B. Patterson, M. A. Rogers, and R. Izor at the Field
Museum of Natural History for their help and for the use of their specimens.
G. Lauder and W. Bemis graciously allowed me to use their computers and
digitizing pads. Statistical advice was provided by N . Thomas and M. Handcock.
Special thanks go to J. Bertram, A. Biewener, S. Emerson, S. Herring, A. Jaslow,
M. LaBarbera, G. Lauder, L. Radinsky, S. Swartz, P. Wainwright, and two
anonymous reviewers for their helpful comments. Computer time was paid for by
Biological Sciences Division Computer Subsidy Funds from the University of
Chicago. This research was supported by a Dee Fellowship from the Field
Museum of Natural History, and NSF grant BSR81-00827 to L. Radinsky.
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