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Stabbing Slinkers: Tusk Evolution Among Artiodactyls

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Combat weaponry, including elaborate horns and antlers and complex dentition, evolved independently several times among mammals. While it is evident that tusk and tusk-like dentition have emerged primarily among males for intrasexual combat, it is unclear what ecological factors favor the retention or re-evolution of tusks. We investigated patterns of tusk evolution in artiodactyls while exploring specific ecological factors that might favor their use over other cranial weapons (e.g., antlers, horns). We show that among males, small (<15 kg), solitary species tend to retain well-developed canines, and more solitary species live in more closed habitats. These results suggest that tusks are a better weapon option for smaller, slinking artiodactyls in forested environments with low visibility, whereas larger taxa living in more open environment can bear the cost of elaborate headgear and are better served by communicating across distances an honest signal of fighting ability. Small species in dense habitats may also be more likely to be ambushed by predators and have a need to defend themselves; small, slicing daggers may be a better defensive weapon and allow more maneuverability and faster escape than cumbersome headgear in densely vegetated habitats.
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ORIGINAL PAPER
Stabbing Slinkers: Tusk Evolution Among Artiodactyls
Doreen Cabrera
1
&Theodore Stankowich
1
#Springer Science+Business Media, LLC, part of Springer Nature 2018
Abstract
Combat weaponry, including elaborate horns and antlers and complex dentition, evolved independently several times among
mammals. While it is evident that tusk and tusk-like dentition have emerged primarily among males for intrasexual combat, it is
unclear what ecological factors favor the retention or re-evolution of tusks. We investigated patterns of tusk evolution in
artiodactyls while exploring specific ecological factors that might favor their use over other cranial weapons (e.g., antlers, horns).
We show that among males, small (<15 kg), solitary species tend to retain well-developed canines, and more solitary species live
in more closed habitats. These results suggest that tusks are a better weapon option for smaller, slinking artiodactyls in forested
environments with low visibility, whereas larger taxa living in more open environment can bear the cost of elaborate headgear
and are better served by communicating across distances an honest signal of fighting ability. Small species in dense habitats may
also be more likely to be ambushed by predators and have a need to defend themselves; small, slicing daggers may be a better
defensive weapon and allow more maneuverability and faster escape than cumbersome headgear in densely vegetated habitats.
Keywords Tusks .Canines .Weapon s .Defense .Deer
Introduction
Elaborate weaponry has evolved multiple times among mam-
mals (Emlen 2008; Stankowich 2012) in both extinct (giant
armadillo (Doedicurus)tailspikes,Smilodon saber teeth), and
extant species (elephant tusks, rhinoceros horns, bovid horns).
These structures are used for both prey capture (Smilodon
saber teeth) and sexual combat (deer antlers, beaked whale
tusks), but among extant species, sexually selected weaponry
is most prevalent among the artiodactyls in the form of cranial
appendages and elongated tusks. Most studies focus on un-
derstanding the ecological, social, and phylogenetic underpin-
nings of horns (Bovidae) and antlers (Cervidae) (Clutton-
Brock et al. 1980;Packer1983;Estes1991b;Lundrigan
1996;Caroetal.2003; Bro-Jørgensen 2007; Stankowich
and Caro 2009;Goss2012;), while the factors promoting the
evolution, retention, and elaboration of tusks have received
little attention (but see Geist 1971;Raiaetal.2015). Here,
we investigate the patterns of tusk evolution in artiodactyls
while exploring specific ecological factors that might favor
their use over cranial weapons (e.g., antlers, horns).
Animal weapons and ornaments typically help their bearers
gain greater access to reproductive partners, but each are un-
der distinct selective mechanisms (Rico-Guevara and Hurme
2018): weapons are a product of physical battle during male-
male competition while ornaments arise from indirect visual
competition between males seeking female preference. As
suggested by McCullough et al. (2016), structures that result
from male-male competition can be modelled using a weapon-
signal continuum where at one extreme, weapons like
Significance Statement While the function and evolution of tusks in
elephants, walruses, and even narwhals have received a great deal of
scientific and public attention, we know little about what drives the
evolution and maintenance of tusks in several groups of artiodactyls (e.g.,
pigs, muntjac, musk deer). Most male artiodactyls have some sort of
sexual weapon (e.g., antlers, horns, tusks), but we dont know what
ecological factors promote the evolution of tusks in some and cranial
weapons in others. Using a comparative approach, we show that living a
slinking, solitary lifestyle in dense, closed habitats where long range
communication during sexual combat is not possible favors the evolution
of sharp, dagger-like tusks for combat during territorial disputes. We
discuss the sexual benefits of tusks over antlers considering species
ecology.
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s10914-018-9453-x) contains supplementary
material, which is available to authorized users.
*Theodore Stankowich
theodore.stankowich@csulb.edu
1
Department of Biological Sciences, California State University, 1250
Bellflower Blvd, Long Beach, CA 90840, USA
Journal of Mammalian Evolution
https://doi.org/10.1007/s10914-018-9453-x
artiodactyl tusks are used purely during combat and at the
other, signal structures are used solely to intimidate rival males
(e.g., stalk-eyed fly eye spans). At the center of the continuum,
however, are structures like deer antlers and bovid horns that
function to communicate strength before fights ensue.
Therefore, weapons may not only serve as honest signals of
fighting ability but also can inflict significant physical dam-
age. Here, we examine the ecological factors that favor the
transition between tusks as pure weapons and antlers/horns as
dual functioning structures.
The earliest most primitive artiodactyls, a group referred to
as the Dichobunoidea, consist of a rich record of extinct spe-
cies necessary for understanding the ancestral state and sub-
sequent evolution of Artiodactyla (Theodor et al. 2007).
Dental morphology of Diacodexis, the first documented artio-
dactyl that emerged in the early Eocene, and other
dichobunids suggest all had well-developed canine teeth, but
none possessed elongated tusks or headgear (Janis 1990). A
European radiation of artiodactyls lasting until the end of the
Eocene gave rise to several families, including
Cebochoeridae, a group of small- to medium-sized species
with caniniform first premolars and elongated canines useful
for grubbing, similar to extant pigs (Erfurt and Métais 2007).
Ruminants emerged during the middle Eocene as part of
the selenodont radiation in North America and Asia (Métais
and Vislobokova 2007). Early ruminants share several defin-
ing features, but unlike many extant artiodactyls, they lacked
cranial headgear (Gentry 1994). Modern forest-dwelling
tragulids (Tra gulus,Moschiola,Hyemoschus)morphological-
ly resemble these early taxa more than any other living rumi-
nants; however, due to a lack of fossil data, deep ruminant
phylogenetic relationships remain ambiguous. Evolutionary
history suggests that the earliest radiation of Ruminantia oc-
curred in conjunction to that of Tylopoda (camelids), while the
second radiation occurred in Central Asias early Oligocene
with the appearance of Pecora (bovids and cervids), tragulids
being the only primitive ruminant lineage to survive (Métais
and Vislobokova 2007). Extinct early ruminants are among
the smallest documented artiodactyls, and dental morphology
data indicate that primitive ruminants were herbivorous with
mostly browsing habits.
Climate change during the late Eocene promoted a shift in
biodiversity (Prothero 2017), and the sporadic availability of
high-quality foods in cold climates facilitated the radiation of
artiodactyl groups and the evolution of conspicuous structures
like large antlers, horns, and tusks (Geist 1966). Early
weapons were small and built to inflict maximum damage
(e.g., sharp horns and tusks), but structures would later in-
crease in size and complexity as they developed into status
symbols among males (Emlen 2008). Following the extinc-
tion of early ruminants, saber-toothed forms with duiker-like
bodies (Bslinkers^;Geist1998) arose in the Oligocene.
Slinkers were likely small (325 kg) and wove through dense
undergrowth with a body plan consisting of muscled haunches
and a long muscular back to aid in saltatory escape and loco-
motion. A number of extant species display the characteristic
Bduiker syndrome^that includes distinct weapons (tusks:
Tragulus,Hydropotes; short stabbing horns/antlers:
Cephalophus,Madoqua,Neotragus,Oreotragus,
Philantomba,Raphiceros,Sylvicapra,Tetracerus; or both:
Muntiacus) developed for stabbing combat, security, and for-
aging to support a solitary forest dwelling lifestyle (Barrette
1977;Geist1998). Dagger-like canines may provide slinkers
with the appropriate weapons to deliver quick pain inflicting
jabs as opposed to possessing elaborate cranial weapons that
increase their chances of entanglement. Barrette (1977)hy-
pothesized that the combination of small body size and the
need to live in closed habitats further promoted an inconspic-
uous slinker lifestyle dependent on quick cover when individ-
uals encounter threatening situations.
With the emergence of gregariousness and increased body
size (Brashares et al. 2000), weapons intended for maximizing
superficial damage would no longer be effective. Severe
wounds created by external protrusions might have attracted
predators to the group. Geists dispersal theory (1966,1971,
1974) suggested that as mammals evolved towards larger body
size, social ungulates could not afford to engage in life-
threatening altercations, creating selection against tusks. One
evolutionary solution would have been to reduce dagger-like
weapons and replace them with combat weaponry oriented to-
wards signaling fighting ability but also delivering less fatal
damage (Geist 1966). Specialized structures like horns and ant-
lers were a more effective fighting form because they visually
deterred competitors before engaging in costly fighting forms.
AsfamouslydiscussedbyJarman(1974), social behavior, as a
result, became increasingly prominent among grazers in open
landscapes, which have lost their combat teeth (non-tusked
cervids have either peg-like vestigial upper canines or lack them
entirely; bovids lack upper canines: Ungar 2010). Combat be-
tween males would have shifted from forced withdrawal by
quick blows to intimidation of the opponent into withdrawing
by wrestling with their newly developed headgear.
Parrying, the act of evading attacks with a counterblow,
likely initiated the development of deflecting structures in
the form of cranial bumps (Geist 1998). Usage of cranial
weaponry would have been significantly more successful at
delivering lasting pain to opponents and further promoted se-
lection for bone and dermal growths (horns and antlers).
Protruding dagger-like canines would have been no match
for head clubs and as a result were shortened to avoid detri-
mental blows. As slashing became less effective, intricate
headgear allowed parrying individuals to hold their opponents
head from striking with sharp canines. As used by extant
muntjacs (Barrette 1977), protoantlers in deer became the first
defensive cranial structures while canines remained the offen-
sive structure (Geist 1998).
J Mammal Evol
In this study, we examine the ecological factors that influ-
ence the evolution (retention, loss, and re-evolution) of tusks
in artiodactyls. We hypothesize that a solitary slinking lifestyle
promotes the elaboration and retention of tusks, while the
evolution of larger body sizes and movement into an open
habitat in larger groups favors the evolution of antlers and,
thus, the loss of tusks. We predict that species with smaller
body sizes, living in closed environments, and living a solitary
lifestyle would be more likely to have larger tusks.
Additionally, as body mass, habitat openness, and group size
increases, tusks should be lost. We use tusk measurements
from skulls of both sexes of a variety of artiodactyls and com-
parative phylogenetic analysis to test this hypothesis.
Methods
In our study, we considered all extant artiodactyl families and
included representatives (63 species) from each lineage bear-
ing tusks. Tusk measurements were taken from collections at
the Natural History Museum of Los Angeles County,
American Museum of Natural History, and the National
Museum of Natural History at the Smithsonian Institution
(Appendix). We measured ten specimens per species, five
female and five male skulls. Only adult skulls with intact
canines were used. We assumed that tusks on each side of
the jaw developed approximately symmetrically so we mea-
sured the most intact upper canine tooth and lower canine
tooth in each skull without regard for side. For all specimens,
we adopted six measurements used by Gittleman and Van
Valkenburgh (1997): upper canine height, upper canine
length, upper canine width, lower canine height, lower canine
length, and lower canine width. Canine height (H) was mea-
sured from the tip to the dentine-enamel junction. Uncurving
tusks were measured using digital calipers (mm). To compen-
sate for distortion caused by outwardly curving tusks (e.g.,
Suidae) when measuring height, we formed a flexible metal
wire from the tip to the dentine-enamel junction down the
midline of the lingual side of the tooth and then repeated this
measurement on the buccal side of the tooth; we then took the
average of these two measures as the total Bheight.^The
anteroposterior length (L) and the mediolateral breadth (W)
across the lingual sides of the upper and lower canines were
measured at the tooth base (dentine-enamel junction).
Measurements were averaged across specimens to obtain a
single representative value for each dimension (height, length,
width) for each sex for each species. We estimated tooth volume
using the formula for the volume of a four-sided pyramid:
Volume = (HLW)/3. We took measurements for both upper
and lower canines, for each species we selected the tooth (upper
vs. lower) with the largest average height and volume. For
groups with either small Bpeglike^canines, variably present
canines, or absent canines, we simply surveyed skulls in
museums and photographs of skulls online to assess their con-
dition, instead of actually measuring specific museum speci-
mens. Four species of cervids typically displayed Bpeglike^
upper canines in all individuals, but possessed incisiform lower
canines (Cervus albirostris, C. elaphus, C. nippon,
Hippocamelus antisensis). Upper measurements, in this case,
were scored as 1 mm in length, width, and height (volume =
0.33 mm
3
), but lower measurements were scored a volume of
0mm
3
. In five different cervid species, individuals varied in the
presence or absence of Bpeglike^upper canines (Mazama amer-
icana, M. gouazoubira, Ozotoceros bezoarticus, Rangifer
tarandus, Rusa unicolor); these species were scored as
0.5 mm in height, width, and length (volume = 0.04 mm
3
). In
species where tusks or tusk-like dentition was absent, all dimen-
sions were assigned a 0. Caniform canines were absent altogeth-
er for all species of Antilocapridae, Bovidae, and Giraffidae. All
measures of canine height and volume were transformed to
achieve normality assumptions using log
e
(X + 1) function.
For all species for which we had sufficient tooth measure-
ments, we collected a variety of natural history data from
published (Nowak 1999; Wilson and Mittermeier 2011)and
online (UMMZ 2015) sources. We collected body mass data
for each sex separately and log
e
transformed it to achieve
normality. If more than one source provided a mass, we used
the average of those values as our mean sex mass. Mating
strategies were coded as 0 if monogamous and 1 if polygy-
nous (Caro et al. 2003). Following Stankowich et al. (2014),
we used collected habitat use data from IUCN (2017; Version
3.1) and assigned an openness score (01) to each habitat
type: Temperate Forest (0.2), Tropical Forest (0.1), Savanna
(0.7), Temperate Shrubland (0.6), Tropical Shrubland (0.5),
Tundra (0.9), Temperate Grassland (0.8), Tropical Grassland
(0.8), Wetlands (0.3), Rocky (0.8), Desert (0.95), Marine
(0.8), Artificial Grassland (0.8), Urban (0.8), Artificial
Marine (0.8), and Caves/Subterranean (0.05). We edited the
IUCN habitat list to only include the primary two to three
habitats inhabited per species giving preference to those in
which species spend the most time (Stankowich and Caro
2009). Finally, we coded sociality as the typical group size
for species: (1) solitary or pairs, (2) 310, (3) 1150, (4) >
50 (Caro et al. 2003). Blinded methods were not used in this
study as no behavioral data were recorded and/or analyzed;
other experimenters, however, collected different elements of
the dataset and compiled them together once completed. The
complete dataset can be found in the online Appendix.
To account for the effect of phylogenetic relatedness be-
tween species, we used phylogenetic general least squares
(PGLS) analyses to test for correlated evolution between traits
in R (R Core Team 2012). We used a composite Artiodactyla
tree downloaded from 10KTrees (Arnold et al. 2010) for all
analyses. To test for the effect of each natural history factor on
canine height and volume in each sex, we conducted PGLS
analyses using the caperpackage (Orme et al. 2012), where
JMammalEvol
lambda is computed using maximum likelihood methods.
Because group size was significantly correlated with each of
the other predictors, we analyzed its effects on tusk size sep-
arately; therefore, we tested each canine measure in two sep-
arate PGLS models: (1) with group size by itself and (2) with
habitat openness, body mass, and mating system combined in
a single model. Finally, we phylogenetically reconstructed the
evolutionary history of male canine height using the contMap
function in phytools(Revell 2012), which estimates the
maximum likelihood ancestral states of characters. All data
generated or analyzed during this study are included in the
supplementary information files.
Results
Results of PGLS statistical models of canine height and vol-
ume in males and females can be found in Table 1. Our anal-
yses showed that among artiodactyls, male canine height
(Fig. 1) and volume decreased as species increased in body
size (Fig. 2) and formed larger groups (Fig. 3), and smaller
solitary species have larger canines (Table 1). We found no
statistically significant effects, however, of body mass and
group size on canine size in females. We found no significant
effects of habitat openness or mating system type in either sex
for any measure of tusk size (Table 1).We did find, however,
that more solitary artiodactyls generally live in more closed
habitats (t=2.424,p= 0.018). This relationship suggests that
habitat openness is, indeed, related to tusk development.
Discussion
The deep ancestral relationships between the artiodactyl line-
ages are unclear; therefore our confidence in the accuracy of
tusk size reconstruction at deep nodes is limited, and
attempting to understand the loss of enlarged canines in ex-
change for cranial weapons (e.g., antlers, horns) remains a
difficult task. As predicted in our study, however, we found
that both body size and sociality strongly affected the
evolution of tusks in males; small solitary species tend to
develop larger canines. Though we did not find a direct rela-
tionship between canine size and habitat openness, additional
tests, however, show that solitary species tend to live in closed
environments, suggesting an ecological niche of being small,
solitary, living in closed dense forests, and using tusks to fight
over territory and/or mates. Similarly, one study found that
small-bodied slinkers primarily live in solitude amongst thick
tropical brush where large canines are favored for defending
small areas with low visibility over costly and cumbersome
headgear (Bro-Jørgensen 2008). Artiodactyls living in closed
habitats may not be able to detect or assess opponents from
afar; confrontations can quickly escalate and small slicing
weapons allow for better offense, maneuverability, and rapid
escape. Here, we discuss the general evolutionary transition
from stabbing tusks to displaying antlers and provide insight
into tusk evolution in each group that bears them.
Defenders of material resources need to be equipped with a
set of weapons that will allow them to quickly inflict maxi-
mum damage on competitors. When early forest-dwelling ar-
tiodactyls made the move to open arid zones, social behavior
allowed species to successfully exploit these new environ-
ments (Estes 1974). We found that tusk-bearing artiodactyls
are primarily solitary and live in closed habitats (temperate
and tropical forests; Table 2) where they are able to defend
small territories. However, movement into more open habitats
favored the evolution of larger body sizes that could support
elaborate forms of visual communication (e.g., large cranial
weapons, flashing of conspicuous rump patches; Estes 1991a;
Caro 2005;Raiaetal.2015). Though our results do not sup-
port a directrelationship between tusk loss and movement into
open habitats, our finding that artiodactyls increase in size and
become more social as they move into open habitats and sub-
sequently lose their tusks supports our hypothesis that moving
into open habitats favored the evolution of cranial appendages
that would serve both as signals to assess competitors and as
weapons in violent fights (i.e., they lie at the center of the
weapon-signal continuum, McCullough et al. 2016).
Our ancestral state reconstruction based solely on measure-
ments of male canine height (Fig. 1) from extant species
Table 1 Results of PGLS
statistical models of canine height
and volume in male and female
artiodactyls
Male Female
Height Volume Height Volume
tptptptp
Group size 2.958 0.004 2.662 0.010 1.656 0.103 0.943 0.349
Body mass 0.211 0.015 2.137 0.037 1.865 0.067 1.211 0.231
Habitat openness 0.155 0.878 0.441 0.661 0.408 0.685 0.592 0.556
Mating system 0.203 0.840 0.203 0.840 0.335 0.739 0.046 0.964
Results in bold signify factors that were statistically significant in explaining tusk retention in relation to canine
height and volume
J Mammal Evol
agrees with the fossil record and suggests that prominent but
not tusk-like male canines are the ancestral condition in artio-
dactyls. The entelodonts, one of the earliest pig-like artiodac-
tyls that emerged during the late middle Eocene, shared prim-
itive dental and skeletal features with other suoids including
canine tusks (Prothero 2017). Evidence from dental wear on
these early forms suggests that they were omnivores and scav-
engers (Prothero 2017). Suoids are separated into two families
that differ in canine morphology (Ungar 2010). In tayassuids,
canines grow vertically downwards, while suid canines often
emerge from the maxilla anterolaterally and curve upward
(MacKinnon 1981; Prothero 2017). True suids emerged and
diversified in the Miocene, which include the
kubanochoerines, a group of large pigs that developed a horn
between their eyes (Harris and Li-Ping 2007; Prothero 2017).
Interlocking canines of the tayassuids function in intraspecific
combat, while the Bout-turned^canines of suids function as
signals of status and rank prior to engaging in conspecific
fights (Herring 1972). The upper tusks of male babirusas are
the most extreme morphological example where they ascend
from the maxilla and curve onto themselves (MacKinnon
1981). This difference in tusk function between suids and
tayassuids supports our hypothesis in that suids (~88 kg
avg.) are larger in mass than tayassuids (~30 kg avg) (Smith
et al. 2003), although their openness of habitat score is similar.
The small hornless hypertragulids of the Eocene resembled
duikers but with highly arched bodies, slender dog-like front
legs, and blade-like canines used for territory defense, and
they hid amongst thick cover from predators (Métais and
Vislobokova 2007;Rössner2007). Tragulids (chevrotain or
Fig. 2 The relationship of log
e
(male canine height (mm) +1) and
log
e
(male body size (kg)) among male artiodactyls (N=63, t=0.211,
p=0.015)
Fig. 1 Phylogenetic tree (Arnold et al. 2010) of artiodactyls showing
ancestral state reconstruction of log
e
(male canine height (mm) +1).
Branch Bwarmth^indicates larger tusk heights where red represents the
most prominent canines (tusks) and blue is the absence of enlarged ca-
nines. Intermediate colors (yellow and green) signify species that retained
tusks but are smaller relative to the babirusa (Babyrousa babyrussa)that
develops the most elaborate form of tusks
R
JMammalEvol
mouse-deer) as we know today radiated later during the
Oligocene retaining much of their ancestral body plans
(Geist 1998), making them the most primitive extant ruminant
(Rössner 2007). Tragulids are largely solitary but may be
found living in small groups (310 individuals) and their long,
slender legs allow them to run through dense undergrowth.
Male chevrotain will engage in primitive territorial fighting
where they stand antiparallel, slashing at each othersneck
and sides often causing detrimental wounds (Dubost 1975,b;
Ralls et al. 1975). For this reason, tragulids develop a layer of
toughened skin on their backs to protect from intraspecific
attacks (Dubost and Terrade 1970; Dubost 1975b; Jarman
1989). Relative to body size, tragulid upper canines are short
and laterally oriented with a backwards curve much like the
muntjac, but the outward flare permits effective combat
(Aitchison 1946).
True antlers first emerged and diversified during the early
Miocene in cervids that bore thick upper canines (Geist 1998),
which were subsequently lost. This is supported by our ances-
tral state reconstruction, which suggests early ruminants did
possess small canine teeth (see light blue branches at the base
of the ruminant clade in Fig. 1). One of these forms,
Hoplitomeryx, strangely bore permanent pronged horns over
its eyes, a long horn on its nose, and long jutting canines
(Prothero 2017). Figure 1suggests that elongated tusks re-
evolved twice among cervids, first in muntjacs and tufted deer
(Muntiacus) and second in water deer (Hydropotes)asthese
groups reclaimed the slinker lifestyle. Muntiacus muntjak
and Hydropotes inermis are on average larger (24 kg
and 30 kg, respectively; Table 2) than tusk-bearing
tragulids and moschids but smaller than non-tusked ant-
lered cervids (average male mass = 114.64 kg). Muntjacs
are unique in that not only are the upper canines pre-
served but males also bear antlers. In this dual weapon
system, antlers are necessary for permitting the use of
widely divergent tusks (Janis and Scott 1987)during
combat (Barrette 1977), and indeed tusks are used as
secondary weapons (Aitchison 1946) during intraspecific
encounters (Yahner 1980). Further study of the evolu-
tionary transition from tusks to antlers in this group is
warranted.
While entirely devoid of cranial weaponry, Moschus and
Hydropotes bear large saber-like tusks with points directed
more downward (Janis and Scott 1987; Sánchez et al. 2010)
than the antlered muntjacs (Aitchison 1946). These long tusks
Fig. 3 log
e
(Canine height (mm) +1) as a function of increasing group size
among male artiodactyls (N = 63, t=2.958, p= 0.004). The outliers
(filled circles) in the 1150 column are all suoideans
Table 2 Results of measured
mean male and female canine
heights and natural history data
from literature searches on body
mass, sociality, and habitat
preference for species with
enlarged canines
Species Body Mass (kg) Canine Height (mm) Sociality Habitat openness
Male Female Male Female
Tragulus javanicus 1.9 1.9 14.81 4.36 1 0.40
Tragulus napu 4 4 15.26 2.92 1 0.45
Muntiacus muntjak 24 24 19.15 0 0 0.45
Muntiacus reevesi 14.5 12.5 26.82 8.08 0 0.53
Hydropotes inermis 30 30 25.09 9.12 0 0.37
Tayassu peccari 32.5 32.5 25.25 26.62 2 0.47
Pecari tajacu 21.5 21.5 30.84 27.87 2 0.58
Hylochoerus meinertzhageni 207.5 150 34.29 38.71 2 0.10
Moschus moschiferus 12 12 36.85 9.56 0 0.50
Sus scrofa 182 182 42.62 16.86 2 0.43
Babyrousa babyrousa 71.5 71.5 106.3 13.32 0 0.20
Sociality scores were assigned using the following: solitary or pairs= 1, 310 = 2, 1150 = 3, > 50 = 4. Openness
scores were obtained from habitat use data from IUCN (Version 3.1) and editing it to include the primary 23
habitats in which species spend the most time. Larger openness scores correspond to the most opened habitats
MMM (mean male mass), MFM (mean female mass), MCH (male canine height), FCH (female canine height)
J Mammal Evol
are used as sexual weapons when engaged in intraspecific
combat to inflict wounds (Aitchison 1946). Musk deer fiercely
slash at their opponents often piercing the skin and even punc-
turing vital organs (Zhang et al. 1970;Sathyakumar,1992).
The upper canines of females, however, are subtle at 1 cm and
do not extend beyond the lower lip. Moschidae includes seven
extant species (Prothero 2017) with a rich fossil record and all
also bear large, saber-like canines. The earliest known
moschid, Dremotherium, emerged in the late Oligocene but
the group was completely extinct by the end of the early
Miocene except for Micromeryx, which survived for the re-
mainder of the Miocene (Prothero 2007). While the deep an-
cestral relationships of cervids, moschids, and bovids are un-
clear, and our ancestral state reconstruction is dependent pure-
ly on extant taxa, Fig. 1suggests that the common ancestor of
these groups possessed small- to medium-sized canines but
lacked tusk-like weapons and both Hydropotes and early
moschids evolved robust tusks independently.
Bovids are among the most diversified group of artiodac-
tyls ranging in body size and occupying a variety of habitats.
The earliest bovid, Eotragus, arose in the late early Miocene
weighing about 18 kg and bearing straight horns roughly 8 cm
long (Prothero 2017). Bovids from the Ice Age, however,
were the most impressive; Pelorovis antiques particularly
weighed up to 2000 kg with horns spanning 4 m in width
(Prothero 2017). Bovid horns are commonly used in combat,
especially among bovines, and horns in antelope in particular
are used for both signaling and fighting(Gosling 1986). While
all bovids lack upper canine teeth (Ungar 2010), a number of
extant bovids displaying the characteristics of a slinker have
evolved short stabbing horns (Cephalophus,Madoqua,
Neotragus,Oreotragus,Philantomba,Raphiceros,
Sylvicapra,Tetracerus). While antlers and horns are used to
signal status and fighting ability, the pointed horns of these
territorial forest-dwelling species are likely pure weapons,
possibly the result of selection favoring a tusk-like weapon
in an animal that lacked canines to elongate but already had
horns that could be repurposed instead. In our analysis, we
only sampled a few species belonging to this peculiar group of
bovids; therefore, future studies are needed that include a
more comprehensive representation of duiker-like species.
From our analysis, we show that body mass and sociality
are important in explaining the retention and subsequent loss
of sexual weaponry among artiodactyls. Small, solitary spe-
cies that rely on close-quarter combat for material resource
defense and rapid escape through dense forest to evade pred-
ators are likely to carry enlarged canines. Our results suggest
that emergence from cover facilitated the evolution of com-
plex social strategies; fewer close-range encounters meant
tusks were no longer optimal and elaborate cranial structures
allowed artiodactyls to advertise their fighting ability to con-
specifics from afar (Geist 1966;Janis1982). Special cases like
the muntjac and Chinese tufted deer that not only retain tusks
but also develop antlers, however, warrant further investiga-
tion. Because slinkers live inconspicuously among thick cover
and tend to be solitary, it is difficult to observe their behavior
in nature. Future studies are needed that target the specific
ecological and behavioral factors of these special cases in
order to understand the evolutionary changes that result in
the retention of multiple combative weapons.
Acknowledgments We thank James Dines and David Janiger at the Los
Angeles County Museum of Natural History, and curators at the
American Museum of Natural History and the National Museum of
Natural History at the Smithsonian Institution for access to their collec-
tions and support. We thank members of the Stankowich Lab at California
State University Long Beach and two anonymous reviewers for com-
ments on previous versions of this manuscript.
Compliance with Ethical Standards
This research was supported by funds from California State University
Long Beach, College of Natural Sciences and Mathematics. For this type
of study formal consent is not required. This article does not contain any
studies with human participants or animals performed by any of the au-
thors; all subjects were previously collected specimens deposited in mu-
seum collections.
Conflict of Interest The authors declare that they have no conflict of
interest.
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An article on the ecology and conservation of musk deer
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We propose a practical concept that distinguishes the particular kind of weaponry that has evolved to be used in combat between individuals of the same species and sex, which we term intrasexually selected weapons (ISWs). We present a treatise of ISWs in nature, aiming to understand their distinction and evolution from other secondary sex traits, including from ‘sexually selected weapons’, and from sexually dimorphic and monomorphic weaponry. We focus on the subset of secondary sex traits that are the result of same‐sex combat, defined here as ISWs, provide not previously reported evolutionary patterns, and offer hypotheses to answer questions such as: why have only some species evolved weapons to fight for the opposite sex or breeding resources? We examined traits that seem to have evolved as ISWs in the entire animal phylogeny, restricting the classification of ISW to traits that are only present or enlarged in adults of one of the sexes, and are used as weapons during intrasexual fights. Because of the absence of behavioural data and, in many cases, lack of sexually discriminated series from juveniles to adults, we exclude the fossil record from this review. We merge morphological, ontogenetic, and behavioural information, and for the first time thoroughly review the tree of life to identify separate evolution of ISWs. We found that ISWs are only found in bilateral animals, appearing independently in nematodes, various groups of arthropods, and vertebrates. Our review sets a reference point to explore other taxa that we identify with potential ISWs for which behavioural or morphological studies are warranted. We establish that most ISWs come in pairs, are located in or near the head, are endo‐ or exoskeletal modifications, are overdeveloped structures compared with those found in females, are modified feeding structures and/or locomotor appendages, are most common in terrestrial taxa, are frequently used to guard females, territories, or both, and are also used in signalling displays to deter rivals and/or attract females. We also found that most taxa lack ISWs, that females of only a few species possess better‐developed weapons than males, that the cases of independent evolution of ISWs are not evenly distributed across the phylogeny, and that animals possessing the most developed ISWs have non‐hunting habits (e.g. herbivores) or are faunivores that prey on very small prey relative to their body size (e.g. insectivores). Bringing together perspectives from studies on a variety of taxa, we conceptualize that there are five ways in which a sexually dimorphic trait, apart from the primary sex traits, can be fixed: sexual selection, fecundity selection, parental role division, differential niche occupation between the sexes, and interference competition. We discuss these trends and the factors involved in the evolution of intrasexually selected weaponry in nature.
Article
The elaboration and diversification of sexually selected weapons remain poorly understood. Here, we argue that progress in this topic has been hindered by a strong bias in sexual selection research, and a tendency for weapons to be conflated with ornaments used in mate choice. Here, we outline how male-male competition and female choice are distinct mechanisms of sexual selection, and why weapons and ornaments are fundamentally different types of traits. We call for research on the factors contributing to weapon divergence, the potential for male-male competition to drive speciation, and the specific use of weapons in the context of direct fights versus displays. Given that weapons are first and foremost fighting structures, biomechanical approaches are an especially promising direction for understanding weapon design.
Article
The savanna ungulate faunas of the North American Miocene were broadly similar to those of present-day East Africa in terms of overall morphological and taxomic diversity. However, the predominant ungulates of the African faunas are bovids, which possess bony horns that are primitively sexually dimorphic in their occurrence. The predominant ungulates of the North American Tertiary were equids, camelids and oreodonts, which all lacked horns. The limited number of horned ruminants were largely Miocene immigrants from Eurasia. Horns were also absent from the large-bodied herbivores in the endemic faunas of South America and Australia. Studies on living ungulates show that a strong correlation exists between habitat type, feeding behaviour, social behaviour and morphology. The importance of the post-Eocene climatic changes to the history of mammalian evolution is stressed. The primitive condition in eupecorans and protoceratids is the absence of horns. The first horned members of these divisions had horns in the males only. Small present-day antelope, where horns may also be present in the females of the species, are probably secondarily small. Horns were acquired independently in ruminant artiodactyls at least 3 times; a maximum number of 7 times is not unlikely. In each case, horns first appeared at a critical body weight of about 18kg, and in correlation with a change in habitat from closed to open woodland. Horns in living ruminants are associated with territorial defence by males holding exclusive feeding and reproductive territories in woodland habitats. Such behaviour in present-day antelope is correlated with a body size of greater than 15 kg and a folivorous diet. Perissodactyls never evolved sexually dimorphic bony horns of the type seen in ruminant artiodactyls because their foraging and digestive strategies necessitate a larger daily intake of food. Study of the morphology and paleoecology of oreodonts suggest that they were woodland herd-forming browsers with exclusively folivorous diets. Studies of the behaviour and morphology of of living members of the Ruminantia, and of the morphology and paleoecology of their fossil ancestors, suggest that they were primitively tree browsers living in closed woodland habitats. The radiation of the Bovidae into open grassy habitats in the Pliocene may have been dependent on the immigration of grazing equids into the Old World. During the Tertiary, the food resources in North America were more widely dispersed; this may have been the result of the trees being more widely spaced. A possible causal mechanism for this was the stable land mass of North American continent during the Tertiary resulting in a more continental climate, with more severe effect of the post-Eocene seasonality on the vegetation. Thus most endemic North American ruminants did not evolve horns because, at the critical combination of body size and diet seen in the evolution of horns in the Old World ruminants, the dispersal of the food resources within the vegetation was too great for an effective home range to be maintained as an exclusive territory. -from Author