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Many-to-one function of cat-like mandibles
highlights a continuum of sabre tooth
adaptions
https://doi.org/10.1098/rspb.2022.1627
Narimane Chatar1,*, Valentin Fischer1, Z. Jack Tseng2
1 Evolution & Diversity Dynamics lab, UR Geology, Université de Liège, Building B18, Quartier Agora, Allée
du Six Août 14, 4000 Liège, Belgium NC 0000-0003-0449-8574, VF 0000-0002-8808-6747
2 Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, CA
94720, United States 0000-0001-5335-4230
* Corresponding author: narimane.chatar@uliege.be
Abstract
Cat-like carnivorans are a textbook example of convergent evolution with distinct
morphological differences between taxa with short or elongated upper canines, the latest
being often interpreted as an adaptation to bite at large angles and subdue large prey.
This interpretation of the sabretooth condition is reinforced by a reduced taxonomic
sampling in some studies, often focusing on highly derived taxa or using simplified
morphological models. Moreover, most biomechanical analyses focus on biting scenarios
at small gapes, ideal for modern carnivora but ill-suited to test for subduction of large prey
by sabre-toothed taxa. In this contribution we present the largest 3D collection-based
muscle-induced biting simulations on cat like carnivorans by running a total of 1,074
analyses on 17 different taxa at three different biting angles (30°, 60° and 90°) including
both morphologies. While our results show a clear adaptation of extreme sabre-toothed
taxa to bite at larger angles in terms of stress distribution, other performance variables
display surprising similarities between all forms at the different angles tested, highlighting
a continuous rather than bipolar spectrum of hunting methods in cat-like carnivorans and
demonstrating a wide functional disparity and nuances of the sabretooth condition that
cannot simply be characterized by specialized feeding biomechanics.
Keywords: Finite element analysis, biting simulation, Felidae, Nimravidae, mandible
biomechanics, Carnivora
Cite as: Chatar, N., Fischer, V., & Tseng, Z. J. (2022). Many-to-one function of cat-like mandibles
highlights a continuum of sabre-tooth adaptations. Proceedings of the Royal Society B: Biological
Sciences 289:20221627. http://doi.org/10.1098/rspb.2022.1627
Introduction
A vast series of vertebrate clades have
independently evolved sabretooth
morphologies [1–4]. However, the
biomechanical consequences of this trait
is poorly known. In cat-like clades
(Felidae, Nimravidae, and
Thylacosmilidae) [5–10], both
sabretoothed and non-sabretoothed cat-
like carnivoran morphotypes are textbook
examples of convergent evolution with
their own suite of craniomandibular
adaptations [3,11–13], the sabretooth
morphology being often interpreted as an
adaptation for subduing large prey [5–
10]. However, functional anatomy
remains blur and, at first; similar
ecomorphologies were suggested for all
sabre-tooths clade before some authors
highlighted the functional differences
between scimitar-toothed and dirk-
toothed taxa and, besides, some lineage
are extremely convergent with modern
“conical” tooth felids (Metailurini and
Nimravini) [3,7,11,14,15]. Different
hunting behaviours were already
proposed for dirk- and scimitar-toothed
machairodontines based on FEA
simulations [15] but some species
considered as ‘mosaic taxa’ (e.g.,
Xenosmilus hodsonae [12]), complexified
those models linking form and function.
Lautenschlager et al. (2020) [16] recently
highlighted the diversity of mechanical
behaviours among sabretooth mandibles
suggesting that homotherins and
metailurins might have use a different bite
than smilodontins. Based on a
mandibular shape extremely similar to
that of extant felines it was also
suggested that primitive machairodontine
(Machairodus aphanistus and
Promegantereon ogygia) might also have
used a different bite than more derived
sabretoothed felids [17]. While long-
toothed taxa have been widely studied in
terms of bending resistance, tooth
morphology, gape, and post-cranial
anatomy [8,10,12,15,16], taxa with
shorter canines are often left out of
comparative analyses.
The very first study computing finite
element analysis including on cat-like
carnivorans was published by McHenry
et al. (2007) [18] comparing Smilodon
fatalis to Panthera leo and shown that
Smilodon head and neck were the most
efficient on a restrained prey and
concluded that prey had to be brought to
ground before bite. Then, a first attempt
of comparing numerous cat-like
carnivorous mammals mechanical
performances using FEA was made by
Piras et al. (2013) [19] using 2D spline
approximation reconstructed from
Procrustes coordinates from their
geometric morphometric analysis. They
found out that sabre-toothed mandibles
were more stressed than in modern
felines mainly in the ascending ramus
[19]. Later, a dirk- and scimitar-toothed
cats comparison was published by
Figueirido et al. (2018) [15] comaring
Smilodon fatalis and a Homotherium
serum skulls, highlighting high variations
between those two machairodontine
morphotypes. A comparison between
Smilodon and Thylacosmilus shown that
the placental sabretooth might not have
been the fearsome predator it was
thought to be but more of a scavenger
Janis et al. (2020) [20]. Finally,
Lautenschlager et al. (2020) [16]
published a large-scale 2D study
comparing all mammalian and non-
mammalian sabretooths based on two-
dimensional outlines using FEA, gape
analysis and geometric morphometric.
Their results highlighted the high intra
and inter clade functional diversity among
sabretooths predators and is thus an
interesting starting point for further
analysis [16]. However, biomechanical
simulations on carnivorans are often run
at gape angle ranging from 25 to 30° a
classical angle for modern carnivora [21]
that is however ill-suited to test for
subduction of large prey by sabre-toothed
taxa.
For the first time we computed three
dimensional biomechanical simulations
on a large dataset testing different gape
angles including highly derived
sabretooth taxa (e.g. Barbourofelis fricki,
Babrourofelis loveorum, Smilodon fatalis,
Homotherium crenatidens or
Hoplophoneus primaevus) but also early
machairodontine taxa (e.g.
Paramachaerodus orientalis and
Machairodus aphanistus),
machairodontines/nimravines taxa which
have fairly short upper canines (e.g.
Yoshi minor) and a wide range of extant
felines, in a comparative framework. We
also tested different gape angles by
performing our analyses at three different
gapes: 30°, 60° and 90.
Here, we thoroughly analyse the biting
biomechanics of sabre-toothed and non-
sabre-toothed taxa by applying Finite
Element Analyses (FEA) on the largest
dataset ever assembled of cat-like
placental mandible 3D models, under a
variety of gape scenarios. We would have
expected taxa with the longest upper
canines to be more efficient at larger
angles and thus to observe an
improvement in the measured
performance variables. However, while
our results show a clear adaptation of
extreme sabre-toothed taxa to bite at
larger angles in terms of von Mises
stress, other performance variables
display surprising similarities between
sabretoothed and non-sabretoothed
forms. The similarities of some
performance variables show that the cat
like mandible is an example of ‘many-to-
one mapping’ of form-function
relationships where forms with obvious
morphological disparity produce the
same function.
Material and Methods
Taxonomic sampling
A total of 19 mandibles from 17 different
taxa were used to compute the analyses,
the complete list of specimens with their
metadata is available in Table 1.
Table 1: Specimens used to compute the FE analyses. Institutional abbreviations: AMNH American museum of Natural History (New York, USA), DNMNH Ditsong
National Museum of Natural History (Pretoria, South Africa), PMU Paleontological Museum Uppsala universitet (Uppsala, Sweden), UCMP University of California
Museum of Paleontology, FAVE Lab Functional anatomy and vertebrate evolution Lab (Berkeley USA), NHMLA: Natural History Museum of Los Angeles County
(Los Angeles, USA), NHMUK: Natural History Museum (London, UK), MNHN Muséum National d’histoire Naturel (Paris, France), NRM Naturhistoriska riksmuseet
(Stockholm, Sweden), UF University of Florida (Gainesville, USA). Upper canine ratio = length of the upper canine/cranial length.
Subfamily
Species
Upper canine ratio
Cranial length
(mm)
Specimen n°
Age
Holding institution
Felinae
Caracal caracal
0.12
110.01
A58401
Extant
NRM
Lynx rufus
0.13
81.51
FAVE09
Extant
FAVE Lab
Panthera pardus
0.15
175.25
AMNH 113745
Extant
AMNH
Panthera onca
0.17
217.53
MNHN-ZM-MO-2006-641
Extant
MNHN
Panthera tigris
0.17
315.68
MNHN-ZO-AC-1931-60
Extant
MNHN
Prionailurus rubiginosus
0.12
83.74
MNHN-ZM-MO-2012-54
Extant
MNHN
Machairodontinae
Amphimachairodus palanderi
0.26
271.98
PMU 21831
Late Miocene
PMU
Dinofelis barlowi
0.23
257.07
DNMNH-BF-55-23
Early Pliocene
DNMNH
Homotherium crenatidens
0.30
330.36
MNHN.F.PET2000
Early Pleistocene
MNHN
Machairodus aphanistus
0.28
336.27
NHMUK-PV-M37356
Late Miocene
NHMUK
Paramachaerodus orientalis
0.20
174.74
NHMUK PV M 8959b
Late Miocene
NHMUK
Smilodon fatalis
0.49
330.72
AMNH-14349
Late Pleistocene
AMNH
Yoshi minor
0.19
149.52
PMU 21766/2
Late Miocene
PMU
Nimravinae
Hoplophoneus primaevus
0.34
170.55
LACM-42890
Late Eocene
NHMLA
Dinictis felina
0.26
160.70
LACM-162986
LateEocene-Mid
Oligocene
NHMLA
Barbourofelinae
Barbourofelis fricki
0.74
289.09
UCMP-124942
Late Miocene
UCMP
Barbourofelis loveorum
0.35
258.04
UF-VP-36855
Late Miocene
UF
Preparation of the 3D data
Estimations of the insertion sites of the
three main masticatory muscle groups
(m. masseter, m. temporalis and m.
pterygoideus) requires the cranium and
mandible in articulation. However, the
cranium of some fossil species may be
missing, crushed, or incomplete. In these
situations where the cranial insertion
sites could not be unambiguously placed
on the associated skull, we used a
cranium belonging to another conspecific
or congeneric specimen to get the focal
coordinates of muscle origins (see Table
S1). As routinely employed in FE
analyses (e.g. [23–28]), we reconstructed
or retrodeformed some models of fossil
taxa. To assure transparency, a complete
description of the various reconstruction
and retro-deformation steps undertaken
is available in Figures S1-S9. We first
computed FEA on two CT-scan based
models and then compared our results to
those obtained on the same models from
which we cleared the internal anatomy to
simulate a surface scan-based model.
Our results on both type of models were
extremely consistent in terms of von
Mises stress, mechanical efficiency and
adjusted strain energy (see ESM, Table
S2, Figure S10-S11) therefore we used
only surface scan-based model for the
rest of our analysis, this also get in line
with some recent results showing that
surface scans might be a good alternative
for CT scans in FEA [29]. The CT-
scanned specimens used for the
comparison were Lynx rufus FAVE09 and
Panthera pardus AMNH-113745. The CT
scan for Lynx rufus FAVE09 was
obtained from the University at Buffalo
Clinical and Translational Science
Institute Imaging Center on a GE
Discovery 690 PET-CT scanner. The
scans of Panthera pardus AMNH-113745
and Smilodon fatalis AMNH-14349 were
initially published in [25] and were
scanned in the AMNH Microscopy and
Imaging Facility on a General Electric
high resolution X-ray micro-CT scanner.
For CT scanning parameters see Table
S3. Image stacks were imported in Avizo
lite 2020 (Thermo Fisher Scientific,
United States) and region of interest were
segmented and exported in STL
(STereoLithography) format. Most of the
surface scans were obtained with a
Creaform HandySCAN 300 laser surface
scanner with a resolution varying from 0.2
to 0.5mm (See Table S4). Raw surface
scans were then treated using the VX
Models software (Creaform, United
States) and GeoMagic wrap 2020 (3D
Systems, United states) then each part
was exported in STL. We measured
functional ratios that are commonly
considered as sabretooth features:
coronoid process height and the upper
canine length; using the GOM Inspect
suite 2018 (Gesellschaft für Optische
Messtechnik, Germany, 2018). (See
ESM and Figure S12).
Then, each 3D model was imported in
Geomagic Wrap 2020 (3D Systems,
United states) and processed. Mandibles
were decimated to approximately
150 000 triangles (see Table S5) and
their XYZ coordinate systems were
standardized. Models of the cranium and
mandible were articulated at 30°, 60°,
and 90° of gape angle, providing three
biting scenarios for each specimen. On
each mandible three muscles groups (M.
temporalis, M. masseter, and M.
pterygoideus groups) were drawn on
each side (6 muscle attachment regions
in total) using GeoMagic (Figure S13).
Meshing and FEA protocol
To estimate the forces (Newtons) pulling
each muscle insertion, the insertion area
(mm2) was multiplied by 0.3N/mm² based
on the maximum tension produced by
mammalian muscle fibres [30]. All biting
simulations were unilateral (left and right
side were simulated in different
scenarios) so to compensate the
balancing side muscle forces were
multiplied by 0.6 of working side muscles,
following [31]. All mandibles were
considered isotropic material; a young’s
modulus of 18 GPa and a Poisson’s ratio
of 0.3 were defined according to [32–35].
Solid meshes of the mandibles were
generated in the Strand7 FE analysis
software (Strand7 Pty Ltd, Australia)
using four-noded tetrahedral ‘brick’
elements after an automated mesh
‘cleaning’ to remove any duplicated
nodes. For each specimen, we produced
three solid meshes with a coarse-, a
medium- and a fine-resolution,
respectively, following [26]. Forces were
distributed on the muscle insertions in a
tangential traction scenario implemented
in the Boneload MATLAB routine written
by [36] which we slightly modified to
adjust the pressure magnitude. The nodal
constraint created on the tip of each tooth
to simulate each bite scenarios was
restrained in the three axes. To avoid
free-body movement or over-constraint of
the models [37], a nodal constraint was
added on each of the temporomandibular
joints (TMJ) preventing any dorsoventral
or rostrocaudal movement but still
allowing a certain degree of bending of
both hemimandibles one towards the
other in the mediolateral axis. Then, the
linear static solver provided in Strand7
was used to solve the muscle loading
model. For model comparison we
extracted different performance
variables: the mechanical efficiency,
adjusted strain energy and von Mises
stress (see ESM for more details about
the performance variables and the
corrections applied to account for
allometric variation in the dataset).
Finally, the ‘graph’ tool in Strand7 was
used to measure VM stress values
across the mandibles by drawing a line
from the middle of the symphyseal region
to the base of the coronoid process on
both the balancing and working side to
obtain values over the whole bone while
avoiding areas of unrealistic high stress
values near nodal constraints. Then we
plotted the rolling mean with a window
width of 10 to visualise the evolution of
VM stress more smoothly. The elongation
of the upper canines and the reduction of
the coronoid process are key,
convergently evolved sabretooth
characters [3]. While elongated upper
canines is the most striking sabretooth
trait it implies a reduction of the coronoid
process for the animal to open its jaw at
a larger angle in order to clear the
elongated upper canines to bite. We
looked at the potential correlation
between those two typical sabretooth
features and the VM stress using linear
regressions (see ESM for more details).
The three different gape angles, using
three different mesh resolutions, as well
as on three to four different biting points
(depending on the number of teeth) on 19
specimens resulted in a total number of
analyses of 1,074. All the plots and
statistical tests were performed in the R
statistical environment version 4.1.0 [38]
using different packages [39–47] (See
ESM for more details).
Phylogenetic signal
To test for the presence of a phylogenetic
signal in our results and visualise the
distribution of some of the performance
variables measured in our analyses, we
built a composite phylogeny based on the
publications by [48–50]. See the ESM for
additional information on the construction
of the tree.
Results
Distribution and fluctuation of
stress
Our von Mises stress contour plots for a
bite simulated on the lower canine
(Figure 1 for von Mises contour plots of a
subset of our dataset and Figure S14)
show a clear difference between taxa
with long and short upper canines. For
each angle, regions of high stress are
larger (Figure 1) and stress is globally
higher (Figure S14) in taxa with shorter
canines within the same clade (see
Machairodus aphanistus vs
Homotherium serum; Dinictis felina vs
Hoplophoneus primaevus). At a 30°
angle, the lowest stress is observed in
Barbourofelis fricki – the most derived
taxa in terms of sabretooth characters[3]
– and the highest in the extant Caracal
caracal (Figure 1 and Figure S14).
Globally, felids display higher stress and
larger high-stress areas than nimravids.
In taxa with short upper canines, there is
a high stress area in the coronoid process
of the working side at a 30° angle, this
stress being better distributed on the
balancing side at 60°. Taxa with long
upper canines show a global decrease of
the stress at larger angles, yet without
important redistribution of stress in other
regions of the mandible, except in
Barbourofelis fricki where the stress is
projected more ventrally at larger angles
but remains on the working side. While a
decrease in global stress is generalised
in taxa with the longest upper canines
(Smilodon fatalis, Homotherium
crenatidens, Barbourofelis fricki, etc.), it
peaks at 60° in the others (e.g., Caracal
caracal, Panthera tigris, Prionailurus
rubiginosus, etc.) and drops drastically at
90°, although those taxa were not
mechanically able to open their jaw at
such an angle because of the high
coronoid process [13].
Figure 1: von Mises stress contour plots on nine different taxa at the three different angles for a canine bite.
This only show a subset of the complete dataset (17 taxa).
In that sense, early machairodontines
(Paramachaerodus orientalis and
Machairodus aphanistus) and taxa
considered as ‘cheetah-like’ taxa (Yoshi
minor) show a different, ‘intermediate’
mandibular mechanical behaviour: stress
is redistributed on the balancing side at
60° but remains constant on the working
side while decreasing on the balancing
one at 90°. We obtained little differences
when simulating biting on the lower first
molar (Figure S15 and Figure S16); the
high stress region on the ventral border of
the mandible is projected posteriorly on
the mandible. In that scenario also, the
stress constantly decreases from 30 to
90° degrees in sabretooth taxa while
showing a peak at 60° for taxa with
shorter upper canines before decreasing
at a 90° gape angle. Globally, the stress
is higher in smaller taxa and decreases
when body size increases within felines
(Figure 1; Figure S17-S18).
The evolution of stress across the
mandible is somewhat similar for a
canine or a molar bite although
sometimes slightly higher in molar bite
scenarios (e.g., Figure S14A and Figure
S15A). Nimravids clearly exhibit lower
stress value than felids and felines
display higher stress values than
machairodontines. The two exceptions in
our dataset are Yoshi minor, displaying
some of the highest stress values
recorded (Fig. 2) and Paramachairodus
orientalis, which shows stress values
comparable to those of Yoshi minor but
solely on the balancing side, at a 30° (see
Figure 14B and Figure S14B). The
highest stress is usually measured at the
base of the coronoid process Figure S14
and Figure S15). In some taxa however
(felines, Yoshi minor and Dinictis felina),
stress peaks in the third quarter of the
mandible corresponding to a position
somewhere below the third lower
premolar. While stress is generally
extremely low in Barbourofelis spp. at a
30° angle it approaches zero at a 90°
angle (e.g., minimum measured on the
balancing side at 90° for a canine bite
0.18782315). Contrary to what could
have been expected the symphysis
region does not concentrate lots of stress
during the bite; this could be explained by
our modelling approach since we did not
consider symphyseal material properties,
which can have an influence on
biomechanical behaviour [51].
Regressions between the stress
measured and functional ratio
We test how the von Mises stress
correlates with these traits (Figure 2,
S19-S21). There is a negative relation
between canine length and the mean von
Mises stress measured across the
mandible for canine (Figure 2) and molar
bites (Figure S19); unusual taxa such as
Yoshi minor and Prionailurus rubiginosus
undeniably lower the adjusted R squared.
There is also a discernible positive
relation between coronoid height and von
Mises stress, even if again Yoshi minor
reduces the adjusted R squared (Figure
S20 and Figure S21).
Figure 2: Regressions between the log canine length and the mean von Mises stress measured across the
mandible at 30° (A-B), 60° (C-D) and 90° (E-F) for a canine bite in both the balancing (A, C and E) and the
working side (B, D and F).
From those plots it is also clear than the
mean stress tends to increase at larger
angles on the balancing side while it
decreases on the working side
suggesting an increasing torsion
resulting in a destabilisation of the jaw
during the bite as previously suggested
by [52]. The Phylogenetic generalized
linear models shown that the ML estimate
was not significantly different from 0, nor
from 1 for all the angle tested, on both the
balancing and working side. Overall,
there is indeed a correlation between the
stress in the mandible and the sabretooth
trait measured that is not simply due to
share ancestry.
Mandible performance
At all the angles measured, both the
adjusted strain energy (SE) and
mechanical efficiency (ME) are stable in
our dataset (Figure S22 and Figure S23).
At a 30° angle (Figure S22A-B and Figure
S23A), Barbourofelis fricki displays the
lowest adjusted strain energy in the
dataset (below 0.05) while the highest
was measured in the machairodontine
Yoshi minor (from 0.12 to 0.15). Taxa
with longer upper canines tend to show
lower values of adjusted SE although
some extant felines also occupy the low
adjusted SE values on the plots
(Panthera tigris, Prionailurus rubiginosus,
Caracal caracal, and Lynx rufus).
Mechanical efficiency is relatively stable
in our dataset but it can still be noted that
Smilodon fatalis explored the widest
range of values. At a 60° (Figure S22C-D
and Figure S23B), the highest and lowest
adjusted strain energy are measured in
felines, Panthera pardus, and
Prionailurus rubiginosus, respectively,
while there is no clear tendency for the
mechanical efficiency. Finally, at the
largest gape angle tested (90°) (Figure
S22E-F and Figure S23C), the highest
adjusted strain energy is measured in
Yoshi minor and the lowest in the
nimravine Hoplophoneus primaevus. The
nimravine Dinictis felina exhibit the
highest mechanical efficiency. MANOVA
performed on the adjusted strain energy
and mechanical efficiency at the three
different angles could not recover
statistical differences between the
families (Felidae and Nimravidae) (p-
value at 30° = 0.9718, p-value at 60° =
0.2777, p-value at 90° = 0.0956). Overall,
both the adjusted strain energy (Figure
S24 and Figure S25) and mechanical
efficiency (Figure S26 and Figure S27)
decrease at larger gape angles whether
for a canine (Figure 3, Figure S24 and
Figure S26) or a molar bite (Figure S25
and Figure S27). Furthermore,
performance variables (SE and ME) do
not correlate with upper canine length
(symbolized by the point size on Figure
S22 and Figure S23).
The phylogenetic signal for the
mechanical efficiency is insignificant for a
bite at 30° and 60° but slightly increases
at a 90° gape angle. The phylogenetic
signal is negligible for the adjusted strain
energy at a 30° and 60° bite and remains
weak at the 90° bite (Pagel’s Lambda and
p-values can be seen in Table 2).
Discussion
Our analyses indicate that the
sabretooth/non-sabretooth dichotomy is
actually weak for mandibles which was
already suggested in previous
biomechanical simulations [15,16].
Indeed, a first study highlighted functional
differences between Homotherium and
Smilodon suggesting different hunting
behavior for dirk- and scimitar-toothed
cats [15] which is supported by
biomechanical analyses on post cranial
bones [53]. An even more recent one
dealing with a larger dataset [16]
highlighted an even greater functional
disparity in the cat like mandible showing
that metailurins had a mechanical
behavior somewhere in between
homotherins and pantherins. Globally,
species with the longest upper canines
are better suited for a bite at larger angles
(decreasing von Mises stress values, see
Fgure 1 and Figure S15-S17) as
previously inferred, but more importantly
our new data demonstrate there is no
clear dichotomy between ‘long upper
canines’ and ‘short upper canines’ with
instead a continuum of biomechanical
responses. Part of this continuum of
biomechanical responses is driven by
varying stress distribution in the working
and balancing side in our dataset
highlighting the importance of using both
hemimandibles for FEA in order to detect
such differences in balancing-working
side stress response.
Figure 3: Phylogenetic relationships between the taxa studied with a continuous color scale on the branches indicating the relative
coronoid process height on a logarithmic scale, point size indicating the relative upper canine size and a heatmap showing the evolution
of mechanical efficiency.
Table 1: Results obtained with the phylosig function for the mechanical efficiency and adjusted strain
energy. Phylogenetic signal: None (Low Pagel’s Lambda and non-significant P-value), Weak (High Pagel’s
Lambda or significant P-value), Strong (High Pagel’s Lambda and significant P-value)
Pagel´s Lambda
logL Lambda
p-value
Phylogenetic signal
Mechanical efficiency
30°
6.6107e-05
38. 6404
1
None
60°
0.102307
35.4671
0.857013
None
90°
6.6107e-05
26.3708
0.0464958
Weak
Adj. strain energy
30°
6.6107e-05
36.1021
1
None
60°
6.6107e-05
31.6723
1
None
90°
0.661484
41.0728
0.385862
Weak
Mandibular stress is reduced at higher
gape angles
The canine shear bite has been accepted
as the typical sabretooth killing method in
opposition to the feline killing bite [6].
However, biomechanical simulations and
morphological analyses suggested the
existence of an additional, somewhat
transitional, and pantherine-like killing
method for homotherines and
metailurines [16], as well as for the early
machairodontines Machairodus and
Promegantereon [17]. Our results
demonstrate that some taxa belonging to
typical sabretooth clades clearly differ
from one another in terms of mandibular
von Mises stress, suggesting that some
taxa deviated from the canine shear bite
and from the feline bite. Distinct
mechanical responses are seen in
sympatric taxa [54], such as
Hoplophoneus primaevus + Dinictis
felina; Yoshi minor + Amphimachairodus
palanderi, possibly suggesting niche
partitioning in feeding mechanics. Also,
while the larger gape of sabretooths is
usually interpreted as a hunting
adaptation to use the elongated upper
canines stabilising the prey with the lower
canines and incisors [3,6], a consistent
drop in stress for lower carnassial bites
could suggest that feeding mechanics in
sabretooths is also more favourable at
higher gapes. In other words, mandibular
modifications of sabretooths may also
have passively favoured carnassial food
processing at larger gapes as well, not
solely canine killing bites.
Shorter coronoid process means
larger gape and less stress
Within felines, the von Mises stress
measured in the mandible was higher in
smaller taxa within the same clade, which
is not especially the case in other
previous FEA studies, e.g., in otters [26],
ungulates [55], or lizards [56]. It was
already noted [11] that the largest amount
of skull shape variation in felines is driven
by allometry over functional or
phylogenetic factors while in sabretooths
the best predictor was canine length over
body size [11]. Extant felids are mostly
solitary ambush predators (except for the
lion, Panthera leo) that bite their prey
either in the throat, neck or sometimes
the skull [57,58]. In this context, larger
gapes expand the range of possible prey
size, although field studies show that
large species do not focus exclusively on
large prey [59]. In extant taxa, gape angle
tends to increase non-linearly with body
size; the largest species appearing
‘overbuilt’ [60], in order to allow
submission of large, energetic prey. Our
results followed the same allometric
relationship, as the crania of large feline
taxa handle stress better than the smaller
ones. Indeed, in our dataset smaller
felines (e.g., Prionailurus rubiginosus,
Caracal caracal) have more gracile
mandibles than the largest ones (e.g.,
Panthera tigris, Panthera onca) which
clearly have an impact on the
biomechanical behaviour of the mandible
as seen in our von Mises stress contour
plots (Figure 1). There is a visible
relationship between von Mises stress
and upper canine height or coronoid
process height (Figure 2 and Figure S19–
S21), whose R squared values are
affected by a couple of unusual taxa [11].
This actually contradicts a previous study
using 2D biomechanical simulations on
cat like mandibles that shown that stress
is higher in sabretoothed in the coronoid
process but this could be explained by
the different models used (2D data
extracted from pictures or 3D models)
[19]. Also, sabretoothed taxa better
handle the torsion induced when biting at
large gape with low values of stress on
the balancing side which may be
explained by the reduction of the size of
the coronoid processes and general
mandibular shape (Figure 1). However,
our dataset is not suited to fully test this
assumption and specific tests would have
to be done by including the modelling of
mandibular symphysis materials, which
are key to understand how torsional
forces are transferred between
hemimandibles [61]. Interestingly, the
presence and development of the
mandibular flange do not seem to affect
any of the performance variables
measured in our analyses, thereby
questioning its functional importance in
biting. It was suggested quite early (see
[62]) that those flanges protected the
upper canines from lateral pression when
the jaw was closed. Our analyses
showing that it has no implication during
biting could support this assumption
although this still does not explain why
taxa with extremely elongated upper
canines like Smilodon do not exhibit such
flanges. Surprisingly, the von Mises
stress values of felines strongly
decreases at a 90° angle while this gape
is mechanically impossible in this clade
due to the size of the coronoid process
and the curvature of post glenoid
processes. The decline in stress values in
all taxa at a 90° can be perhaps simply
explained by the position of the biting
points and the orientation of the muscle
pulling the mandible resulting in a
moderate stress in the mandibular corpus
due to the poor lever arm. At 90°, the
muscle vectors have a better alignment
with the long axis of the mandible. Thus,
sabretooths did not necessarily need
specialized morphology to make the
mandible any stronger at high gape; the
main morphological change was instead
to reduce the coronoid process to allow
such jaw opening.
Efficiency and strain energy are
insensitive to sabretooth morphology
It is almost impossible to differentiate
clades (Felines, machairodontines,
nimravines, or barbourofelines), families
(Felids or nimravids), and morphotypes
(sabretooth vs non sabretooth) based on
their adjusted strain energy (adj SE), their
mechanical efficiency (ME), at the
different angles or in the pattern of
evolution of ME and adj SE from 30° to
90° (Figure 3 and Figure S21-S26; see
MANOVA results above ). A weak
phylogenetic signal is present in our
mechanical efficiency and adjusted strain
at a 90° bite (Table 2) possibly due to the
particularly high ME in barbourofelines at
this gape. This means in effect that
mandibular performance is insensitive to
sabretooth morphology or phylogenetic
relationships.
This unexpected result is particularly
important because a wide series of
unrelated clades have evolved elongated
upper canines, ever since the Permian.
When carnivorous, these taxa are often
called sabretooth (e.g., thylacosmilids,
gorgonopsians, biarmosuchians,
anteosaurid dinocephalians) but many
other clades have evolved comparable
dental morphologies, such as the extant
musk deer, chevrotains, the walrus, the
Eocene, rhino-like Uintatheriidae
[2,4,16,63–67], even bony fish [68]. The
potential functions of elongated canines
or caniniform teeth range from display,
defence, intraspecific aggression, sexual
selection, manipulation of food, and the
hunting of large prey items [2]. While the
exact function remains obscure for some
clades, especially in herbivorous extinct
taxa [69], the presence of sabre teeth in
carnivorous animals is often presented as
an adaptation to kill large prey [2,3]. This
wide array of possible functions indicates
that multiple evolutionary drivers
channelled the acquisition of elongated
canines. Our results markedly add to this
complexity by demonstrating a functional
decoupling between canine elongation
and mandible performance in the iconic
sabretoothed carnivoran mammals.
Finally, as predicted by [70] the ‘many-to-
one mapping’ of form-function
relationships can be applied to various
complex biological systems; the cat-like
mandible now appears as a striking
example of such a phenomenon,
displaying a high morphological disparity
with little mechanical variation in terms of
mechanical efficiency and adjusted strain
energy. This was not expected after the
results published by [16] were all the
analysed functional parameters (actual
and effective gape angle, bending
strength, bite force) shown a continuum
distribution of results between the two
morphotypes. The similarities in terms of
mechanical efficiency and adjusted strain
energy could be due to similar canine
clearance during the bite. Indeed, forms
with smaller upper canines biting at a 30°
angle might have a similar canine
clearance to extremely derived
sabretooth like Smilodon fatalis or
Barbourofelis fricki at a 90° gape angle.
Still, our results highlighted a continuum
in terms of stress distribution in the cat
like mandible possibly suggesting a wide
range of hunting methods in those
carnivorans.
Conclusions
We thoroughly analysed the
biomechanical behaviour of mandibles of
cat-like taxa, extant and extinct, under
multiple biting scenarios. Our analyses
show a better stress repartition in taxa
with long upper canines with a global
stress decreasing at larger gape angles
which corroborate that those species are
adapted to bite at larger angles.
However, we show a continuous
spectrum of mechanical responses in
terms of mechanical efficiency and
adjusted strain energy in the cat like
mandibles rather than a discrete
difference between sabretooth and non-
sabretooth forms. Despite striking
morphological differences within felines,
machairodontines, nimravines, and
barboroufelines, their mandibular
architectures react similarly in a
mechanical efficiency and strain energy
framework. This indicates a spectrum of
hunting methods in cat-like carnivorans
rather than a two-peaked adaptive
landscape, as forces involved in those
different hunting scenarios were not
drastically variable. Also, this points out
that the cat-like mandible in its non-
sabretooth forms was already
mechanically strong and able to endure a
bite at an extremely large angle (90°)
meaning that all the morphological
variations associated with the sabretooth
ecomorphs are only meant to make that
bite possible and not to build a stronger
mandible to support that bite.
Authors’ contributions
NC, VF, and ZJT designed the study. ZJT
collected CT scan data. NC collected
laser scan data. NC processed the 3D
models, carried out the FE analyses,
analysed the data, and drafted the figures
and manuscript. All authors contributed to
writing the manuscript and gave final
approval for publication.
Data availability statement
All 3D models used to perform the finite
element analysis are available on
MorphoSource (Project ID: 000473875,
https://www.morphosource.org/projects/
000473875/)
Excel files containing the model
properties, raw results, calculation of the
adjusted strain energy and mechanical
efficiency, final Strand7 loaded files, the
modified MATLAB code as well as the R
script used to create the plots and
perform the statistical tests are provided
as supplementary files and are available
on Orbi, the ULiège Open Repository
(https://hdl.handle.net/2268/296076).
Funding
NC is supported by a grant of Fonds de
la Recherche Scientifique F.R.S.–FNRS
(FRIA grant number FRIA FC 36251). VF
is supported by a grant of Fonds de la
Recherche Scientifique F.R.S.–FNRS
(MIS F.4511.19). ZJT is supported by
NSF DBI 2128146.
Acknowledgments
We are extremely thankful to all curators,
collection managers and staff, whose
help and support was fundamental to
collect all the scans we needed to
perform this study. Especially, we would
like to thank: Geraldine Véron (MNHN,
Paris, France), Daniela Kalthoff and
Thomas Mörs (NRM, Stockholm,
Sweden), Benjamin Kear (PMU, Upssala,
Sweden), Roula Pappa and Pip Brewer
(NHMUK, London, United Kingdom),
Patricia Holroyd (UCMP, Berkeley, USA),
Samuel A. McLeod and Xiaoming Wang
(NHMLA, Los Angeles).
We would also like to show our gratitude
to Florent Goussard and Christine Argot
(MNHN, Paris, France) for providing us
structured light scan and CT scans of
Homotherium crenatidens. For access to
the surface scan data of Dinofelis barlowi,
we thank the Ditsong National Museum of
Natural History, South Africa, and Justin
Adams of the Department of Anatomy
and Developmental Biology, Monash
University, Australia. We are also
extremely thankful to Jeanette Pirlo and
Sierra Steely for the surface scans of the
holotype of Barbourofelis loveorum from
the University of Florida.
We are immensely grateful to Romain
Boman from the Aerospace & Mechanical
Engineering department in the University
of Liège for his help to improve the forces
distribution in the “Boneload” MATLAB
routine. Finally, we would like to thank
John Hutchinson as well as three
anonymous reviewers for their
constructive comments on a previous
version of the manuscript.
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