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IR-14-029
Fast running restricts evolutionary change
of the vertebral column in mammals
Frietson Galis
David R. Carrier
Joris van Alphen
Steven D. van der Mije
Tom J. M. Van Dooren
Hans J.A.J. Metz (
[email protected])
Clara M. A. ten Broek
Approved by
Ulf Dieckmann
Director, Evolution and Ecology Program
June 2015
Interim Reports on work of the International Institute for Applied Systems Analysis receive only
limited review. Views or opinions expressed herein do not necessarily represent those of the
Institute, its National Member Organizations, or other organizations supporting the work.
Fast running restricts evolutionary change of the vertebral column in
mammals
Frietson Galis1, David R. Carrier2, Joris van Alphen1, Steven D. van der Mije1,
Tom J. M. Van Dooren1,3, Johan A. J. Metz1,4, Clara M.A. ten Broek1,5
1Naturalis
Biodiversity Centre, Darwinweg 2, 2333CR Leiden, The Netherlands
of Biology, The University of Utah, Salt Lake City, USA
Institute of Ecology and Environmental Sciences Paris, Université Pierre et
Marie Curie, 75005 Paris, France
4
IIASA, Laxenburg, Austria
5
Group of Evolutionary Ecology, University of Antwerp, Groenenborgerlaan 171,
2020 Antwerp, Belgium
2
Department
3
Keywords: body plans, evolutionary conservation, stabilizing selection, homeotic
transformations, mammals, locomotion
The mammalian vertebral column is highly variable, reflecting adaptations to a wide
range of lifestyles, from burrowing in moles to flying in bats. Yet, in many taxa the
number of trunk vertebrae is surprisingly constant. We argue that the latter constancy
results from strong selection against initial changes of these numbers in fast-running or
agile mammals, while such selection is weak in slower-running, sturdier mammals. The
rationale is that changes of the number of trunk vertebrae require homeotic
transformations from trunk into sacral vertebrae, or vice versa, and mutations towards
such transformations generally produce transitional lumbosacral vertebrae that are
incompletely fused to the sacrum. We hypothesize that such incomplete homeotic
transformations impair flexibility of the lumbosacral joint and, thereby threaten survival
in species that depend on axial mobility for speed and agility. Such transformations will
only marginally affect performance in slow sturdy species, so that sufficient individuals
with transitional vertebrae survive to allow eventual evolutionary changes of trunk
vertebral numbers. We present data on fast and slow carnivores and artiodactyls and on
slow afrotherians and monotremes that strongly support this hypothesis. The conclusion
is that the selective constraints on the number of trunk vertebrae stem from a combination
of developmental and biomechanical constraints.
Many mammalian taxa show a remarkable conservation of the number of presacral (cervical,
thoracic plus lumbar) vertebrae. For instance, carnivores almost invariably have 27 and
artiodactyls 26 presacral vertebrae. Yet, in some taxa, in particular afrotherians, there is
considerable interspecific variation1,2. In this study we investigate the causal importance for
this conservation of biomechanical problems associated with incipient homeotic
transformations3,4. To this end, we compare the frequencies of abnormal (i.e., non-modal)
presacral vertebral numbers in fast-running artiodactyls and carnivores versus slower-running
species in the same taxa and slower-running afrotherians and monotremes. We predict that
slower-running species harbour more abnormal presacral numbers and transitional lumbosacral
vertebrae than fast ones, both within and between taxa. Furthermore, assuming that there are
no other causes for variation, we predict that afrotherians are not more variable than similarly
slow species of other taxa.
Fast versus slow
Variation in the number of presacral vertebrae in fast running artiodactyls and carnivores is
almost absent in our dataset (Table 1, <2%), both in sprinters (felids) and endurance runners
(canids and artiodactyls). We found only three abnormal numbers (≠26) in 161 artiodactyl
specimens (in Saiga tartarica, Eudorcas rufifrons, Kobus vardoni) and one (≠27) in 269
carnivore specimens (in Leptailurus serval). In contrast, variation is common in slower running
artiodactyls and carnivores ranging from ± 25% in badgers, muskoxen and bay duikers to >50%
in water chevrotains and Hippopotamus (Tables S1,S2). Most abnormal presacral numbers are
due to transitional lumbosacral vertebrae, i.e. to incomplete homeotic transformations (71.4%,
Table 1). Within the Artiodactyla the differences between fast and slower runners are
significant for transitional vertebrae and total abnormal presacral numbers (including
transitional vertebrae, Table S2). This also holds at the family level for the Bovidae and for all
non-bovid taxa together. Similarly, in the Carnivora, fast and slower runners differ significantly
as, at the family level, do short-limbed mustelids.
Fast carnivores and fast artiodactyls do not differ significanty, and neither do slow carnivores
and slow artiodactyls (Table 1). The slow carnivores, artiodactyls, monotremes and afrotherians
differ significantly, but, posthoc pairwise comparisons show that only the afrotherians differ
from slow carnivores and slow artiodactyls; the other differences are not significant (Table 1).
The afrotherians do not differ significantly from the slowest artiodactyls, Hyemoschus and
Hippopotamus (Tables S2,3). Hippopotamus has the highest frequency of abnormal presacral
vertebrae, a striking 70%. However, the range of variation (25.5-26) is smaller than in other
species, like Hyemoschus (24.5-26) and Elephas (28.5-31).
Flexible versus stiff trunk
The fast-running taxa with the lowest frequency of transitional vertebrae gallop at top speed
and are generally long-limbed (Fig. 1a,b, Table S1,2). The spine is dorsoventrally and laterally
flexible, the rigid ribcase rather short and narrow and the lumbar spine relatively long and
slender5-7. The mobility of the trunk is largest at the lumbosacral transition5,7-9. The laterally
projecting transverse processes are slender and point forward, clearly separated from the sacrum
and ilium (Fig. 2h-j). The dorsal spinous processes of the thorax point backward up to the
anticlinal vertebrae, which usually has a straight spinous process (Fig. 1a-c). Posterior to the
anticlinal vertebra the spinous processes point forward. This anticlinality, particularly
pronounced in fast carnivores, allows dorso-ventral flexion around the anticlinal vertebra. In
fast artiodactyls, anticlinality is less pronounced (Fig. 1a), especially in larger species, with
dorsoventral flexibility concentrated around the lumbosacral transition5. Dorsoventral
flexibility significantly contributes to speed as it increases stride-length5,9. Additionally, many
fast species are also agile, able to swerve and leap (e.g. servals, cheetahs and impalas), which
requires not only dorsoventral, but also lateral mobility of the lumbosacral spine. Incomplete
and asymmetric fusions of the lumbar spine to the sacrum necessarily reduce flexibility of the
lumbosacral joint (Fig. 2k-n). In wolves, dogs and humans transitional lumbosacral vertebrae
are furthermore associated with additional biomechanical problems in adjacent tissues, like
pressure on blood vessels and nerves, intervertebral disc degeneration, iliolumbar ligament
degeneration, scoliosis and hip dysplasia10-12. Hence, such transitional vertebrae dramatically
reduce survival in species that depend on speed and agility to catch prey or to avoid predation.
The taxa with the highest frequency of transitional lumbosacral vertebrae and/or abnormal
presacral numbers (> 47%, echidnas, afrotherians and slow artiodactyls) do not gallop and
locomotion is cautious with usually three or four and minimally two feet on the ground, thus
avoiding great transitory stresses on the joints8,13-17. The trunk has limited flexibility, due to a
long, robust and stiff thoracic region, a stiff lumbar spine of variable length and little mobility
at the lumbosacral joint (Fig. 1f and 2b-d). The stiffness of the lumbar spine can be realized in
different ways. In elephants and echidnas stiffness is provided by sturdy dorsal spinous
processes that all point backward (no anticlinality) (Fig. 1f). Additionally, the lumbar region is
short and wedged between the rigid ribcage and sacrum (Fig. 1f,2a). In aardvarks,
hippopotamuses and water chevrotains stiffness is provided by wide and long laterally
projecting transverse processes. The most caudal ones often touch the ilium and sacrum,
severely limiting mobility (Fig. 2b-d). In addition, ligaments and muscles interconnecting the
transverse and spinous processes and connecting the lumbar vertebrae with the ilium and
sacrum further stiffen the axial skeleton9,18. The restricted mobility of the lumbosacral transition
and the usually slow movements make that structural abnormalities will only minimally affect
performance so that indirect selection against change in vertebral numbers should be weak.
Species with an intermediate number of abnormal presacral numbers (24-33% in swine,
badgers, musk oxen and bay divers, Table S1,2) are also intermediate in speed, agility and trunk
stiffness (c.f. shape, size and position of transverse and spinous processes, relative lengths of
thoracic and lumbar regions, Figs. 1d,e and 2e,f). These species gallop, but only infrequently.
The variability in presacral numbers that we find in different taxa thus agrees well with the
hypothesized strength of selection against homeotic transformations.
Gallop versus half-bound
The fast short-limbed mustelids have a somewhat higher incidence of abnormal presacral
numbers than fast long-limbed carnivores and artiodactyls (~5% vs ~1%), notwithstanding the
flexibility of their lumbosacral spine (Figs. 1c and 2g). These mustelids do not gallop, but
employ a half-bounding gait with the left and right hind-limb simultaneously striking the
ground. The increased tolerance of abnormal lumbosacral transitions probably has to do with
this symmetric strike. Asymmetric striking of the hind-limbs should lead to greater torsional
strains on an asymmetric lumbosacral boundary, with longer limb lengths increasing the effect
(except for fully parasagittal strides); longer limb lengths also lead to higher parasagittal shear
stresses, further increasing the biomechanical adversity of abnormal lumbosacral joints.
Body size
Body size appears to matter less than stiffness of the lumbosacral spine, as we find highly
variable presacral numbers in large (elephants and hippopotamuses) and small species
(tragulids,bay divers, echidnas, Table S2-S4). Naturally, weight plays a role in that extremely
heavy mammals always have stiff lumbar spines, to prevent structural damage and minimize
muscular stabilization costs5,8,9.
Domestication and inbreeding
Domesticated species usually harbour high numbers of transitional lumbosacral vertebrae, also
those that originate from fast and agile wild counterparts (e.g. cats, dogs, horses)11,19,20 Human
care relaxes selection by increasing the survival of less adapted individuals. Inbreeding
probably also plays a role, as inbred wild wolves have higher numbers of transitional
lumbosacral vertebrae than outbred ones12,21. The Saiga tatarica with a transitional vertebra
may well be the product of the strong inbreeding in this endangered species22,23.
Developmental buffering and canalization
The incidence of abnormal lumbosacral transitions in slower-running species was higher than
we expected, with a quarter or more affected individuals. One possible cause is low
developmental robustness. That is, during the embryonic stage when the identities of the lumbar
and sacral vertebrae are determined as part of the A-P patterning of the embryonic axis,
buffering mechanisms are rather ineffective at neutralizing environmental and mutational
disturbances that cause some degree of homeotic transformation. The high frequency of
transitional lumbosacral vertebrae in inbred mammals supports this hypothesis as inbreeding
appears to weaken developmental stability24-26. In contrast, in fast running species the transition
at the lumbosacral boundary is sharp and vertebral shape is regular (Fig. 2g-j), suggesting strong
selection for robust and stable vertebral development. Any weakening of this selection in slow
and domesticated species, due to the mitigated fitness effects of lumbosacral abnormalities,
probably leads to a sharp decrease in robustness. This can in part be explained by the high
interactivity and low modularity of the vulnerable early organogenesis stage, when lumbosacral
vertebral identities are determined27,28. Moreover, the early irreversibility of the determination
of vertebral identity further limits the buffering potential3.
Fast and inbred cheetahs
Unexpectedly, we did not find any abnormal lumbosacral transitions in cheetahs (Table S1),
despite their dramatically low genetic diversity29 and our (exceptional) inclusion of captiveborn specimens (9 of 38 specimens). Apparently, the extreme demands for high speed in this
fastest of all terrestrial species have resulted in the selective maintenance of a highly canalized
vertebral development, despite severe inbreeding. It will be of interest to study more cheetahs
in zoos, to see whether and after how many generations the canalized lumbosacral development
breaks down.
Developmental and biomechanical constraints
Our results indicate that the selective constraints limiting the evolution of mammalian presacral
vertebral numbers are due to a combination of developmental and biomechanical constraints.
Many genes (including Hox) are involved in determining vertebral identity, with initial
mutations for shifts of the lumbosacral boundary typically leading to incomplete homeotic
transformations (a developmental constraint), associated with later acting biomechanical
problems hampering locomotory performance (biomechanical constraints). The biomechanical
problems come from (i) incomplete and often asymmetric fusions of transitional lumbosacral
vertebrae with the sacrum and, (ii) correlated biomechanical problems, because many genes
that pattern the vertebrae also influence patterning of adjacent nerves and muscles
(developmental constraints). Fast and agile mammals, thus, provide a powerful example of the
potential importance of the interplay of developmental and biomechanical constraints in
evolution.
Methods (supplementary online info)
Specimens
We analysed skeletons of 753 wild-born and 9 captive-born individuals of 89 species of 14
different mammal families of 8 European natural history museums: Naturalis Biodiversity
Center, Leiden (Naturalis), The Natural History Museum, London (NNM), the Royal Museum
for Central Africa, Tervuren (RMCA), the Royal Belgian Institute of Natural Sciences, Brussels
(RBINS), the Natural History Museum of Denmark, Copenhagen (ZMUC), Naturhistorisches
Museum Wien, Vienna (NHMW), the Swedish Museum of Natural History, Stockholm (NRM)
and Museum für Naturkunde, Berlin (ZMB). To avoid the potentially confounding effects of
inbreeding, we excluded mammals that were born in zoos, except for 9 cheetahs (Acinonyx
jubatus) that were included for additional information on this extremely fast species.
Carnivora. We analysed 419 skeletons of Carnivora including 84 Canidae, 183 Felidae, 134
Mustelidae and 18 Procyonidae (Table S1).
Artiodactyla. We analysed 266 skeletons of Artiodactyla including 3 Antilocapridae, 165
Bovidae, 21 Cervidae, 10 Hippopotamidae, 33 Suidae and 34 Tragulidae (Table S2).
Afrotheria. We analysed 48 skeletons of Afrotheria including 21 Tubulidentata and 27
Elephantidae (Table S3).
Monotremata. We analysed skeletons of 30 Tachyglossidae of the Order Monotremata (Table
S4).
Vertebral formula
We have determined the vertebral formula of the skeletons by determining the number of
cervical, thoracic, lumbar, sacral and coccygeal vertebrae. Transitional vertebrae at boundaries
were counted as half for each of the neighboring regions, e.g. half thoracic and half lumbar.
The thoracolumbar boundary is sometimes difficult to establish with precision, because
transitional thoracolumbar vertebrae have one or two rudimentary ribs and these are often lost
and the detection of their small articulations on the vertebra is often difficult, especially when
the vertebrae are worn or damaged by strong maceration during preparation. Therefore, the sum
of the thoracic and lumbar vertebrae is more precise than the separate numbers, but this does
not affect the precision of the presacral number. We considered the most frequent whole
presacral number (mode) as normal. For carnivore species the normal number is 27 and for
artiodactyl species 26 (tables S1,S2). For Afrotherians, the normal number is 28 for
Orycteropus, 30 for Elephas and 31 for Loxodonta (table S3). For the monotremes it is 26 for
Tachyglossus and 27 for Zaglossus (table S4). Abnormal numbers were divided into two
groups: a) with a transitional lumbosacral vertebra (abnormal transitional) and b) without one
(abnormal non-transitional).
Classification of fast-running versus slower-running
Predictions regarding running speed and gait were based on references found in the literature
13-17,30-39
and surmised from the anatomy and observations. To avoid classification mistakes, we
selected as far as available the fastest and most agile of galloping, long-limbed species versus
the slowest and sturdiest species within the taxon. The slower-running species consist of those
that never gallop on land (the afrotherian Elephas, Loxodonta, Orycteropus and the artiodactyl
Hyemoschus and Hippopotamus, of which the latter only gallops under water) and those that
infrequently gallop (the artiodactyl Ovibos, Cephalophus and the suid species and the carnivore
Meles and Procyon), Classifications can be found in tables S1-S4 and were made before the
analyses of the vertebral columns. In total we classified 252 specimens of carnivore as fast
running and 51 as slower running. An exception was made for the family Mustelidae
(Carnivora), for which we included as fast species, exclusively for the analysis at the family
level, the fast, but short-limbed Martes foina, Mustela erminea and Mustela nivalis. The
rationale was that in this set of mustelid species there are no long-limbed and galloping fast
species, but only fast and agile elongate species that use a half-bound gait and have short limbs.
Statistical tests
We analyzed overall contingency tables of the different slow and fast running taxa and their
presacral numbers (normal, abnormal non-transitional or abnormal transitional) using Fisher’s
exact tests. Posthoc comparisons were performed by Fisher’s exact tests and p-values were
Holm-Bonferroni adjusted.
Legends
Figure 1. Skeletons of fast and slower running mammals, lateral views. (a-c) Fast-running
and agile species with slender vertebral columns with a relatively short thoracic region (ribs
provide rigidity), a relatively long lumbar region and a highly flexible lumbosacral transition:
long-limbed gallopers, Gazella dorcas (a), coyote (b, Canis latrans) and short-limbed and halfbounding marten (c, Martes martes). (d-f) Slower running species with more sturdy skeletons,
longer thoracic and shorter lumbar regions and stiffer lumbosacral transitions: badger (d, Meles
meles) and Babirusa swine (e, Babyrousa babyrussa) and Asian elephant (f, Elephas maximus,
juvenile specimen). Swine and badgers occasionally run fast, whereas elephants never uses the
gallop and have a particularly stiff lumbosacral transition. The stiffness of the elephant spine
comes from the dorsal spinous processes which are all backward pointing (no anticlinality) and
a particularly short lumbar region that is wedged between the long and sturdy ribcage and rigid
sacrum. For a comparison of fast-running and slower-running species within one family, cf. the
slender and flexible marten (c) and the sturdier and stockier badger (d). The spinous and
transverse processes are more robust in the badger, which provides rigidity in combination with
the attached ligaments. Additionally, in martens the thoracic region has one less vertebra and
the lumbar region one more vertebra, adding to the flexibility (see Fig. 2f-g for dorsal views of
the lumbosacral spines). Anticlinality is particularly pronounced in fast carnivores (b,c),
allowing dorsoventral flexibility at the end of the thoracic region. However, in fast artiodactyls
(a) this is less the case, with flexibility of the lumbosacral transition being especially important.
Figure 2. Lumbosacral spines of fast and slower running mammals, dorsal views. (a-d)
Relatively slow and cautiously moving species with a stiff lumbosacral transition. In Asian
elephants (a, Elephas maximus), stiffness is due to a short lumbar region that is wedged in
between a rigid ribcase and sacrum, in combination with a backward orientation of all spinous
processes of the trunk (see Fig. 1f). In aardvarks (b, Orycteropus afer), hippopotamuses (c,
Hippopotomus amphibius) and water chevrotains (d, Hyemoschus aquaticus), stiff lumbosacral
transitions are due to wide and long laterally projecting transverse processes of the lumbar
vertebrae, that are close to, or touch each other, or the sacrum and ilium. (e,f,) Babirusa swine
(e, Babyrousa babyrussa) and badgers (f, Meles meles) are species that occasionally run and
that have intermediately stiff lumbosacral transitions. The transverse processes of the lumbar
vertebrae are clearly separated from each other and less robust compared to those in (a-d), but
more robust than those of the fast species in (g-j). The most caudal transverse processes
generally do not touch the sacrum or ilium (e), but occasionally do so slightly (f). (g-j)
Lumbosacral spines of fast running species with flexible lumbosacral transitions: the shortlimbed half-bounding pine marten (g, Martes martes) and the long limbed gallopers, cheetah
(h, Acinonyx jubatus), coyote, (i, Canis latrans) and Gazella dorcas (j). These fast species have
flexible and slender lumbar spines with a sharp lumbosacral transition. The lateral transverse
processes are slender and forward pointing, clearly separated from each other and from the
sacrum and ilium. Asymmetrical transitional lumbosacral vertebrae in a badger (k, Meles
meles) and a Saiga tatarica (l) and symmetrical transitional lumbosacral vertebrae in an
aardvark (m, Orycteropus afer) and a water chevrotain (n, Hyemoschus aquaticus. The partial
fusions with the sacrum drastically limit the flexibility of the lumbosacral joint, which is
especially problematic in fast and agile mammals.
Acknowledgements
We thank Russ Lande, Leon Claessens, Jacques van Alphen, Rino Zandee and Reinhard Bürger
for discussion and comments. We thank Mogens Andersen, Nora Lange, Wim Wendelen,
Georges Lenglet, Daniela Kalthoff, Peter Mortensen, Peter Nilsson and Roberto PortelaMiguez, for making skeletons available. FG acknowledges EC Synthesys travel grants to visit
the Zoological Museum Copenhagen, the Natural History Museum of Berlin, the Royal
Museum for Central Africa, Tervuren, the Natural History Museum of Stockholm (BE-TAF1649, DK-TAF-2183, DE-TAF-2114, SE-TAF-3009), CtB and FG to the Natural History
Museum London (GB-TAF-2762 and GB-TAF-1659).
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Author contributions
FG and CTB analysed the skeletal patterns. CTB and FG analysed the data. FG, DC and CTB
formulated the predictions. FG, CTB and JAJM wrote the manuscript with contributions from
JVA, DC and SJVM. JVA and CTB made the Figures. All authors read and approved the final
manuscript.
Author information
The authors declare no competing interests.
Fig. 1
Fig.2
Table 1.
Normal number
presacral vertebrae
Carnivora
fast
fast half-bound
slow
Artiodactyla
fast
slow
Bovidae
fast
slow
Afrotheria (slow)
=
Abnormal number
non-transitional vertebrae
Abnormal number
transitional vertebrae
260 (99.6%)
95 (95.0%)
38 (74.5%)
1
2
4
(0.4%)
(2.0%)
(7.8%)
0 (0.0%)
3 (3.0%)
9 (17.6%)
158 (98.1%)
62 (59.0%)
2 (1.2%)
12 (11.4%)
1 (0.6%)
31 (29.5%)
134 (97.8%)
21 (75.0%)
15 (31.3%)
2 (1.5%)
2 (7.1%)
11 (22.9%)
1 (0.7%)
5 (17.9%)
22 (45.8%)
Table 2.
Fisher's exact tests
f a s t g a l l o p i n g v s f a s t h a l f - b o u n d Ca r n i v o r a
f a s t h a l f - b o u n d v s s l o w Ca r n i v o r a
f a s t g a l l o p i n g v s s l o w Ca r n i v o r a
f a s t v s s l o w Ar t i o d a c t y l a
f a s t v s s l o w Bo v i d a e
f a s t v s s l o w n o n - Bo v i d a e
f a s t Ca r n i v o r a v s f a s t Ar t i o d a c t y l a
s l o w c a r n i v o r a , a r t i o d a c t y l a , a f r o t h e r i a , mo n o t r e ma t a
Po s t h o c p a i r wi s e c o mp a r i s o n s
s l o w Ca r n i v o r a v s s l o w Ar t i o d a c t y l a
s l o w Ca r n i v o r a v s Mo n o t r e ma t a
s l o w Ca r n i v o r a v s Af r o t h e r i a
s l o w Ar t i o d a c t y l a v s Af r o t h e r i a
s l o w Ar t i o d a c t y l a v s Mo n o t r e ma t a
Mo n o t r e ma t a v s Af r o t h e r i a
P-value
<
<
<
<
<
<
0.
0.
0. 01
0. 001
0. 001
0. 001
0. 001
0. 001
24
01
P- v a l u e ( Hol m- Bonf e r r oni a dj us t e d)
0. 44
0.40
< 0.001
< 0.01
0.69
0.40
Supplementary table 1.
Fast galloping Carnivora (N=267)
Slow Carnivora (N=51)
Fast half-bound Carnivora (N=101)
Family
Genus
Canidae
Canis
Chrysocyon
Lycaon
Family
Genus
Mustelidae
Meles
Family
Genus
Mustelidae
Martes
Felidae
Acinonyx
Caracal
Felis
Leopardus
Leptailurus
Lynx
Panthera
Prionailurus
Profelis
Presacral No.
0.0% abnormal
27
27
27
N
84
63
6
15
0.5% abnormal
27
27
27
27
26
27
27
27
27
183
38
17
20
8
1
28
22
30
11
27
8
Procyonidae
Procyon
Presacral No.
24.2% abnormal
25.5
26
26.5
27
27.5
N
33
1
2
3
25
2
27.8% abnormal
26
26.5
27
27.5
18
2
2
13
1
Mustela
Presacral No.
5.0% abnormal
27
28
26.5
27
27.5
28
N
101
36
1
1
60
2
1
Supplementary table 2.
Fast Artiodactyla (N=161)
Family
Genus
Antilocapridae
Antilocapra
Bovidae
Aepyceros
Alcelaphus
Antidorcas
Beatragus
Boselaphus
Capra
Connochetes
Damaliscus
Eudorcas
Gazella
Kobus
Litocranius
Nanger
Oryx
Pelea
Redunca
Rupicapra
Saiga
Taurotragus
Tragelaphus
Cervidae
Rangifer
Slow Artiodactyla (N=105)
Presacral No.
N
Family
Genus
0.0% abnormal
26
3
3
Bovidae
Cephalophus
2,2% abnormal
26
26
26
26
26
26
26
26
26
25
26
26
27
26
26
26
26
26
26
26
26.5
26
26
0.0% abnormal
26
137
3
4
10
1
3
1
4
4
5
1
19
27
1
2
2
9
1
14
1
10
1
2
12
Ovibos
Hippopotamidae
Hippopotamus
Suidae
Babyrousa
Phacochoerus
Potamochoerus
Sus
Tragulidae
Hyemoschus
21
21
Moschiola
Tragulus
Presacral No.
N
25.0% abnormal
25.5
26
27
25
25.5
26
26.5
28
2
11
1
1
2
10
1
70.0% abnormal
25.5
26
10
7
3
33.3% abnormal
26
25
26
25
25.5
26
26.5
25.5
26
27
33
1
1
2
3
3
16
1
2
3
1
50.0% abnormal
24.5
25
25.5
26
34
2
3
7
8
26.5
1
25
1
25.5
1
26
9
26.5
1
27
1
Supplementary table 3.
Afrotheria (N=47)
Family
Genus
Presacral No.
N
Elephantidae
63.0% abnormal
27
28.5
3
29
4
29.5
3
30
7
30.5
1
Elephas
Loxodonthas
Orycteropodidae
Orycteropus
31
2
29.5
1
30
2
30.5
1
31
2
76.2% abnormal
21
26.5
1
27
3
27.5
11
28
5
28.5
1
Supplementary table 4.
Monotremata (N=30)
Family
Genus
Tachyglossidae
Tachyglossus
Zaglossus
Presacral No.
46.7% abnormal
N
30
25.5
3
26
13
26.5
4
27
1
27.5
1
27
3
27.5
4
28
1