ArticlePDF Available

Differentiation of craniomandibular morphology in two sympatric Peromyscus mice (Cricetidae: Rodentia)



In the Santa Cruz Mountains of California, dietary partitioning is believed to allow Peromyscus californicus (California mouse) and Peromyscus truei (pinyon mouse) to occur sympatrically; P. californicus feeds primarily on arthropods, whereas P. truei feeds primarily on acorns. To better understand how these species partition resources, we examine if these dietary differences extend to differences in craniomandibular morphology. We use a geometric morphometric approach to test the hypothesis that P. californicus and P. truei exhibited size and shape differences in craniomandibular morphology, in particular, regions of the skulls that pertain to biting ability and mechanical advantage of the jaw adductor muscles. We found that P. truei exhibited relatively wider zygomatic arches, relatively broader, more robust masseteric fossa and coronoid process, and a higher mechanical advantage of the masseter jaw muscle. These craniomandibular traits suggested that P. truei exhibits a relatively stronger bite force that is more suitable to access hard-shelled acorns despite its smaller body size.
Differentiation of craniomandibular morphology in two sympatric
Peromyscus mice (Cricetidae: Rodentia)
Kaz Jones
&Chris J. Law
Received: 20 December 2017 /Accepted: 8 March 2018
#Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2018
In the Santa Cruz Mountains of California, dietary partitioning is believed to allow Peromyscus californicus (California mouse)
and Peromyscus truei (pinyon mouse) to occur sympatrically; P. californicus feeds primarily on arthropods, whereas P. truei
feeds primarily on acorns. To better understand how these species partition resources, we examine if these dietary differences
extend to differences in craniomandibular morphology. We use a geometric morphometric approach to test the hypothesis that
P. californicus and P. truei exhibited size and shape differences in craniomandibular morphology, in particular, regions of the
skulls that pertain to biting ability and mechanical advantage of the jaw adductor muscles. We found that P. truei exhibited
relatively wider zygomatic arches, relatively broader, more robust masseteric fossa and coronoid process, and a higher mechan-
ical advantage of the masseter jaw muscle. These craniomandibular traits suggested that P. truei exhibits a relatively stronger bite
force that is more suitable to access hard-shelled acorns despite its smaller body size.
Keywords Bite force .Dietary partitioning .Geometric morphometrics .Mechanical advantage .Skull morphology
Closely related species often share morphological and func-
tional characteristics that allow them to fall within the same
ecological guild and use the same resources in similar ways
(Root 1967; Schoener 1974; Dayan and Simberloff 1994).
However in zones of sympatry, high interspecific competition
is expected to drive resource partitioning between these eco-
logically similar species resulting in separation of ecological
niches such as space use, time, and/or diet (Pianka 1973;
Schoener 1974). Accompanying niche partitioning is differ-
entiation of the underlying morphology/physiology, behavior,
and performance that facilitates exploitation of specific re-
sources for each species (Verwaijen et al. 2002; Mori and
Vincent 2008;Žagar et al. 2017). This ecomorphological par-
adigm elucidates the interactions between sympatric species
and their environments (Wainwright 1991; Ferry-Graham
et al. 2002; Grant and Grant 2002), which in turn provides
better understanding of the mechanisms that shape species
As the most populous native mammals in North America,
deer mice (genus Peromyscus) range across a variety of eco-
systems and frequently share overlapping habitats between
two or three Peromyscus species (Kaufman and Kaufman
1989). Extensive studies on niche partitioning between sym-
patric deer mice have found that differences in dietary prefer-
ence may be one of the primary mechanisms that reduce in-
terspecific competition (Smartt 1978; Kalcounis-Rüppell and
Millar 2002;Reidetal.2013). Researchers have also exam-
ined the morphological, behavioral, and functional differences
that underlie differences in the exploitation of prey. In most
mammals, the ability to exploit particular prey is limited by
the biting ability generated by craniomandibular morphology
(Kardong 2014). Therefore, the ecomorphological paradigm
hypothesizes a strong link between craniomandibular mor-
phology and prey exploitation. Previous studies with lizards,
turtles, birds, and mammals have revealed that variation in
craniomandibular morphology can influence dietary profit-
ability by expanding/limiting the food items accessible to a
Communicated by: Joanna Stojak
Electronic supplementary material The online version of this article
( contains supplementary
material, which is available to authorized users.
*Chris J. Law
Department of Ecology and Evolutionary Biology, University of
California, Coastal Biology Building, Santa Cruz, 130 McAllister
Road, Santa Cruz, CA 95060, USA
Mammal Research
predator and increasing/decreasing prey handling time (Herrel
et al. 2001; Verwaijen et al. 2002;Herreletal.2006; van der
Meij and Bout 2006; Bulté et al. 2008). Furthermore, closely
related sympatric vertebrates exhibit different craniomandibular
morphologies that facilitate dietary partitioning by allowing each
species to specialize on different prey items (Verwaijen et al.
2002; Mori and Vincent 2008; Santana et al. 2010). These shifts
toward different craniomandibular morphologies, however, are
not only driven by evolutionary processes but may also be driven
by developmental plasticity. A plethora of studies have demon-
strated that differences in dietary consistency can affect the shape
of the skull and dental morphology (Watt and Williams 1951;
Myers et al. 1996;Makietal.2002).
In this study, we examine if the dietary partitioning ob-
served between two sympatric Peromyscus mice are accom-
panied by differences in craniomandibular morphology.
Peromyscus californicus (California mouse) and
Peromyscus truei (pinyon mouse) occur sympatrically in
the Santa Cruz Mountains and can be distinguished primarily
by mean body mass where P. californicus (43.04 g) is larger
than P. t r u e i (26.92 g) (SMURF, unpublished data). Recent
isotopic analyses revealed dietary differences between these
two species (Reid et al. 2013): P. t r u e i (misidentified as
Peromyscus boylii in Reid et al. 2013) primarily specializes
on tanoak acorns (Notholithocarpus densiflorus) during the
winter, spring, and summer monthsand Shreve oak (Quercus
parvula) and California live oak (Quercus agrifolia) acorns
in the fall. In contrast, P. cali fornicus feeds at a higher trophic
level and primarily consumes spiders (Araneae) in addition
to beetles (Coleoptera), crickets (Orthoptera), and some sup-
plementary acorns from N. densiflorus and Q. parvula (Reid
et al. 2013). To better understand the link between dietary
partitioning and craniomandibular variation, we test the hy-
pothesis that P. t r u e i and P. californicus exhibit differences in
craniomandibular size and shape as well as mechanical ad-
vantage of the jaw adductor muscles. We predict that P. t r u e i
will exhibit relatively wider zygomatic arches, more robust
mandibles, and greater mechanical advantage that can facil-
itate relatively stronger biting ability needed to specialize on
hard-shelled acorns.
Materials and methods
Specimens and geometric morphometric superimposition We
quantified differences in the cranium and mandible by analyz-
ing three views of the skull with 2D landmark-based geomet-
ric morphometrics (Rohlf and Slice 1990;Zelditchetal.
2012). We obtained 41 adult P. californicus parasiticus skulls
(16 females, 25 males) and 33 adult P. truei dyselius skulls (15
females, 18 males) from the mammal collection at the
California Academy of Sciences (Supplementary Data 1).
Specimens originated from the Santa Cruz Mountains within
Santa Clara and Santa Cruz counties in California. All speci-
mens were fully mature, determined by the complete eruption
of all cheek teeth (Holmes et al. 2015).
Each specimen was photographed in three views: (1) cra-
nium in ventral view, photographed by orienting the palate
plane parallel to the photographic plane; (2) cranium in lateral
view, photographed by orienting the midsagittal plane parallel
to the photographic plane; and (3) mandible in lateral view,
photographed by orienting the long axis of the dentary parallel
to the photographic plane. Photographs were taken using a
Canon 70D DSLR camera affixed to a Kaiser 205513 RS-10
copy stand kit. Specimens were placed at a distance of 35 cm
away from the camera lens. A ruler with 1 × 1 cm grids was
used to ensure no distortion as well as serve as a scale bar.
Fig. 1 Landmarks (large black circles) and semi-landmarks (small red
circles) used for geometric morphometric analysis of skull shape and size.
Specimen is a male Peromyscus californicus (CAS MAM 12567). The
scale bar represents 1 cm of distance. aVentral cranial view: (1)
anteriormost point of the suture between nasals, (2) and (3) lateralmost
point of the alveolus of the incisor, (4) and (5) lateral tip of the incisor, (6)
and (7) anteriormost point of the incisive foramen, (8) and (9) exterior
ends of the premaxillary-maxillary sutures, (10) and (11) lateralmost ex-
tent of suture between the premaxilla and maxilla, (12) and (13)
anterodorsal tip of zygomatic plate, (14) and (15) posteriormost point of
the incisive foramen, (16) and (17) anteriormost point of the orbit, (18)
and (19) anteriormost point of the molar row, (20) and (21) lateral
paracone of first molar, (22) and (23) contact point between first and
second molars, (24) and (25) contact point between second and third
molars, (26) and (27) posteriormost point of the third molar, (28) and
(29) least post-palatal distance across the palatines, (30) and (31)
anteriormost point of the glenoid fossa, (32) and (33) posterior end of
squamosal root of zygomatic bar, (34) posteriormost extent of palate at
the midline, (35) and (36) suture between basisphenoid and basioccipital
at point of contact with the auditory bulla, (37) and (38) lateral margins of
the foramen ovale, (39) anteriormost point of the foramen magnum along
the midline, (40) posteriormost point of the foramen magnum on the
midline, (41) and (42) lateral margins of the foramen magnum, (43) and
(44) posteriormost margin of the mastoid process. bLateral cranial view:
(1) posteriormost point of the upper incisive alveolus, (2) inferiormost
point of the upper incisive alveolus, (3) interior most point of suture
between nasal and premaxillary, (4) anterior tip of the nasal, (5) curvature
at the limit between the occipital condyle and the occipital bone, (6)
inferior extremity on the boundary between the occipital condyle and
the tympanic bulla, (7) ventral-most point of the interior of the opening
to the tympanic bulla, (8) dorsal-most point of the interior of the opening
to the tympanic bulla, (9) posteriormost point of the molar row, (10)
anteriormost point of the molar row, (11) ventral extent of the suture
between maxilla and premaxilla, (12) anteriormost point of the orbit,
(13) anteriormost point of the glenoid fossa in the zygomatic bar, (14)
posterior end of zygomatic bar. cMandibular view: (1) anteroventral
border of incisive alveolus, (2) upper extreme anterior border of incisor
alveolus, (3) position of greatest inflection of the diastema, (4) Anterior
edge of the alveolus of first molar, (5) intersection between molar crown
and coronoid process in lateral view, (6) tip of the coronoid process, (7)
point of maximum curvature between the coronoid and condylar process,
(8) dorsal margin of the anterior edge of the articular surface of the
condylar process, (9) ventral edge of the articular surface of the condylar
process, (10) point of maximum curvature between condylar and angular
process, (11) tip of the angular process, (12) intersection between man-
dibular body and masseteric crest
Mamm Res
We then placed homologous morphological landmarks and
semi-landmarks on the lateral cranial, ventral cranial, and lat-
eral mandibular views. We used 14 landmarks and 26 semi-
landmarks on the lateral cranial view, 44 landmarks and 10
semi-landmarks on the ventral cranium view, and 11 land-
marks and 51 semi-landmarks on the lateral mandibular view
(Fig. 1) based on Maestri et al. (2016). Landmarks were cho-
sen for their potential to be recognized across a species; semi-
landmarks were generated at evenly spaced intervals between
landmarks. All landmarks were digitized using the program
tpsDig-v 2.30 (Rohlf 2005). We then aligned digitized speci-
mens using a generalized Procrustes superimposition (Rohlf
and Slice 1990) in the R package geomorph 3.0.1 (Adams and
Otárola-Castillo 2013) in R 3.2.1 (R Core Team 2017). During
the Procrustes superimposition, semi-landmarks on the curves
were allowed to slide along their tangent vectors until their
positions minimized bending energy (Bookstein 1997;
Zelditch et al. 2012). After superimposition, bilaterally homol-
ogous landmarks on the ventral cranium were reflected across
the midline and averaged using the geomorph function
Analysis of skull size and shape We first examined if sexual
dimorphism in skull size and shape was significant within
each species. For each species, we determined if the size of
each skull view was significantly different between the sexes
using separate analyses of variance (ANOVAs) on the centroid
size of each configuration of landmarks (the square root of the
39 40
13 14
Mamm Res
sum of the squared distances from each landmark to the geo-
metric center of the shape) (Bookstein 1997). Similarly, we
determined if skull shape within each species was significant-
ly different between the sexes using a Procrustes ANOVA
(Goodall 1991; Anderson 2001) with a factorial design on
each of the skull view datasets. For each skull view, we used
shape as the dependent variable, sex as the main factor, and
centroid size as a covariate.
We found no significant sexual dimorphism in size or
shape of any skull view; therefore, we pooled males and fe-
males in our analyses of interspecific differentiation. For each
skull view, we examined differences in skull size and skull
shape using ANOVAs and Procrustes ANOVAs, respectively.
Procrustes ANOVAs were conducted with a factorial design
with shape as the dependent variable, species as the main
factor, and centroid size as a covariate. Procrustes ANOVAs
were performed with the procD.lm function in the R package
geomorph 3.0.1 (Adams and Otárola-Castillo 2013). We also
used a pairwise permutation test with the permudist function
in the R package MORPHO 2.4 (Schlager 2016)toquantify
shape differences (Procrustes distances) between the two spe-
cies and to determine if these differences were significant.
Lastly, we performed separate principal component analyses
on the Procrustes coordinates of each skull view to visualize
the tangent space (form) of the two species.
Mechanical advantage We assessed differences in biting abil-
ity between the two species by modeling the lower jaw as a
lever and calculating mechanical advantage (MA) of the
temporalis and masseter masticatory muscles (e.g., Tanner
et al. 2010; La Croix et al. 2011; Timm-Davis et al. 2015;
Law et al. 2016a). MA describes the proportion of jaw muscle
force transmitted to the bite point; relatively higher MA indi-
cates higher force-modified jaws (Kardong 2014). MA is cal-
culated as the ratio between the in-lever, the distance between
the mandibular condyle and the muscle insertion point, and
the out-lever (OL), the distance from the mandibular condyle
to the tip of the incisor. We used moment arm of temporalis
(MAT), measured from the tip of the coronoid process to the
condyle, and moment arm of masseter (MAM), measured
from the tip of the angular process to the condyle, as our
temporalis and masseter in-lever (moment arm) distances, re-
spectively. The out-lever was measured to the tip of the incisor
(Fig. 1d). ShapiroWilk tests indicated that MA exhibited a
normal distribution. Thus, we performed ANOVAs to deter-
mine whether there were significant sexual differences in MA.
Skull size and shape Skulls of the Peromyscus californicus
were significantly larger than skulls of the P. truei in the ven-
tral cranium (F
= 155.16, P< 0.001), lateral cranium
= 4726, P< .001), and mandible (F
= 4726,
P< 0.001). A principal component analysis of the Procrustes
coordinates revealed form of all three skull views largely sep-
arated out between the two species on PC1 (Fig. 2). Analyses
with both Procrustes ANOVAs and pairwise permutation tests
confirmed significant shape differences for all three skull
views (Table 1; Fig. 3). In the cranium, the P. truei exhibited
relatively longer tooth rows, relatively wider zygomatic
arches, and relatively longer dorsal cranial profiles (Fig. 3a,
b). In the mandible, the P. truei exhibited relatively broader,
more robust masseteric fossa and coronoid process but exhib-
ited a relatively shorter angular process (Fig. 3c).
Procrustes ANOVAs also revealed significant allometry
between shape and size in the crania of both species; however,
these allometric patterns do not significantly differ between
the two species (Table 1). The mandible, in contrast, does not
exhibit significant allometry between mandibular shape and
size (Table 1).
Mechanical advantage Feeding performance was measured as
the MA of the two primary jaw adductor muscles, the
temporalis and masseter muscles. MA of the temporalis did
not differ significantly between the two species (F
P= 0.508). In contrast, P. truei exhibited significantly greater
MA of the masseter compared to P. californicus (F
21.69, P<0.001).
Within the Santa Cruz Mountains, Peromyscus truei and
P. californicus are congeners that coexist in sympatric loca-
tions. Their ability to coexist is hypothesized to be a result of
dietary niche partitioning: P. truei specializes on hard-shelled
acorns, whereas P. californicus primarily feeds on arthropods
such as Araneae, Orthoptera, and Coleoptera (Reid et al.
2013). Consistent with these dietary differences, we found
craniomandibular differences that allow P. truei to be better
suited to process hard-shelled acorns compared to
P. c a l i f o r n i c u s . Specifically, we found that P. truei exhibited
relatively wider zygomatic arches and relatively longer ros-
trum in the cranium and relatively broader mandibular ramus.
These traits serve as attachment sites for the masticatory mus-
cles, particularly the masseter that originates at the zygomatic
arch, spans across the mandibular ramus, and inserts at the
angular process (Turnbull 1970;Cox2008). As the largest
of the masticatory muscles in rodents, the masseter exerts
the strongest force during jaw closure (Turnbull 1970) and
increases bite efficiency at the incisors (Druzinsky 2010).
Therefore, the relatively wider zygomatic arches and broader
mandibular rami found in P. truei suggest relatively larger
masseter muscles and thus relatively greater biting ability than
P. californicus.
Mamm Res
Our finding that P. t r u e i also exhibits greater MA of the
masseter further corroborates these morphological differ-
ences. Higher MA is typically associated with increased
force-modified jaws (Kardong 2014) that are adapted to pro-
cess hard-shelled prey. Unsurprisingly, relatively higher MA
of the masticatory muscles are found in several durophagous
vertebrates such as loggerhead musk turtles (Pfaller et al.
2011), some moray eels (Collar et al. 2014), and southern
sea otters (Law et al. 2016b).
Together, our analyses of the craniomandibular morpholo-
gy and mechanical advantage suggest that, for a given size,
P. t r u e i exhibits relatively greater bite force than
P. californicus. These biomechanical differences in the feed-
ing apparatus often correspond to realized dietary differences
in sympatric species (Verwaijen et al. 2002;MoriandVincent
2008; Santana et al. 2010). Because the force an animal can
generate by biting limits the range of prey items it can con-
sume, greater bite forces strongly correlate with reduced han-
dling times for both prey capture and consumption (Herrel
et al. 2001; van der Meij and Bout 2006; Anderson et al.
2008) and the ability to expand dietary breadth by consuming
larger or more robust food items (Verwaijen et al. 2002;Herrel
et al. 2006; Bulté et al. 2008; Pfaller et al. 2011). In the Santa
Cruz Mountains, a relatively greater bite force allows P. truei
to consume hard-shelled acorns at a greater efficiency than
P. californicus despite its smaller body size. Nevertheless,
the phenomenon of many-to-one mapping of morphology to
function has demonstrated that different morphological traits
Table 1 Results from Procrustes
ANOVAs for species differences
in cranial and mandibular shape
1, 70
A. Ventral cranium
Species 0.014431 0.014431 0.216963 20.4789 0.001
Centroid size 0.003063 0.0030635 0.046058 4.3474 0.001
Species × size 0.000396 0.0003964 0.00596 0.5626 0.873
Residuals 0.048623 0.0007047
Tot al 0.0 66 5 13
B. Lateral cranium
Species 0.06164 0.06164 0.35627 41.5693 0.001
Centroid size 0.0064 0.0064 0.03699 4.3161 0.005
Species × size 0.001178 0.001178 0.00681 0.7943 0.517
Residuals 0.103797 0.001483
Tot al 0.1 73 0 14
C. Mandible
Species 0.025682 0.0256825 0.143532 12.1203 0.001
Centroid size 0.00385 0.0038498 0.021515 1.8168 0.064
Species × size 0.001073 0.0010731 0.005997 0.5064 0.859
Residuals 0.148327 0.002119
Tot al 0.1 78 9 32
Italicized Pvalues indicate significance (α=0.05)
SS sum of squares, MS means squares
Fig. 2 Principal components plot of skull form variation. Deformation grids display shapes at the ends of the range of variability along PC1 (red=
P. tr u e i , light gray = P. californicus). Shapes of all three skull views are significantly different between the two species (Table 1)
Mamm Res
will not necessarily translate to different functional traits
(Alfaro et al. 2005; Wainwright et al. 2005). Therefore, wheth-
er these differences in craniomandibular morphology between
P. californicus and P. truei results in actual differences in
in vivo bite forces will requires further investigation.
Here, we found that P. truei exhibits craniomandibular mor-
phology (relatively wider zygomatic arches in the cranium
and relatively broader mandibular rami) better suited to pro-
cess hard-shelled acorns along with higher mechanical
advantage of the masseter jaw muscle relative to
P. californius. Although these findings are consistent with
the dietary differences exhibited by P. truei (acorn specialist)
and P. californicus (arthropods), the underlying mechanisms
that led to these morphological differences are not yet clear.
Several confounding factors not analyzed in this present study
may drive these differences including differences in micro-
habitats, sensory adaptations, and/or random evolutionary his-
tory. Future work incorporating specimens across multiple
populations with allopatric and sympatric P. t r u e i and
P. californicus as well as dietary manipulation will elucidate
whether the relationship between craniomandibular and die-
tary differences arose through adaptations toward different
morphological optima or through developmental plasticity in
which different dietary items influenced the development of
the skull and mandible.
Acknowledgements We thank the many mentors, staff, and students of
the University of California, Santa Cruz (UCSC) Small Mammal
Undergraduate Research in the Forest (SMURF) program who have
worked with us and taught us about the natural history of deer mice.
We would like to thank Tina Cheng (UCSC), Karen Holl (UCSC), and
Gage H. Dayton (UCSC) for their support of this study.
Funding Funding for the SMURF program was provided by the UCSC
Department of Ecology and Evolutionary Biology, the Webster Chair
Fund, the Kenneth S. Norris Center for Natural History, and the UC
Natural Reserve System. CJL was funded by a National Science
Foundation Graduate Research Fellowship.
Adams DC, Otárola-Castillo E (2013) Geomorph: an r package for the
collection and analysis of geometric morphometric shape data.
Methods Ecol Evol 4:393399
Alfaro ME, Bolnick DI, Wainwright PC (2005) Evolutionary conse-
quences of many-to-one mapping of jaw morphology to mechanics
in labrid fishes. Am Nat 165:E140E154
Anderson MJ (2001) A new method for non-parametric multivariate
analysis of variance. Austral Ecol 26:3246
Anderson RA, McBrayer LD, Herrel A (2008) Bite force in vertebrates:
opportunities and caveats for use of a nonpareil whole-animal per-
formance measure. Biol J Linn Soc 93:709720
Bookstein FL (1997) Landmark methods for forms without landmarks:
morphometrics of group differences in outline shape. Med Image
Anal 1:225243
Bulté G, Irschick DJ, Blouin-Demers G (2008) The reproductive role
hypothesis explains trophic morphology dimorphism in the northern
map turtle. Funct Ecol 22:824830
Collar DC, Reece JS, Alfaro ME, Wainwright PC (2014) Imperfect mor-
phological convergence: variable changes in cranial structures un-
derlie transitions to durophagy in moray eels. Am Nat 183:E168
Cox PG (2008) A quantitative analysis of the Eutherian orbit: correlations
with masticatory apparatus. Biol Rev 83:3569
Dayan T, Simberloff D (1994) Character displacement, sexual dimor-
phism, and morphological variation among British and Irish
mustelids. Ecology 75:10631073
Druzinsky RE (2010) Functional anatomy of incisal biting in
Aplodontia rufa and sciuromorph rodentspart 2:
PD = 0.028*
PD = 0.058*
PD = 0.037*
Fig. 3 acDifferences in mean shapes (Procrustes distances) between
P. californicus (large white circles) and P. truei (small black circles).
Differences were magnified by a factor of 2 to display shape differences
between the two species. P
= Procrustes distance between mean shape of
California mouse and P. truei.AsterisksB*^indicate significant P
on pairwise permutation test
Mamm Res
sciuromorphy is efficacious for production of force at the inci-
sors. Cells Tissues Organs 192:5063
Ferry-Graham LA, Bolnick DI, Wainwright PC (2002) Using functional
morphology to examine the ecology and evolution of specialization.
Integr Comp Biol 42:265277
Goodall C (1991) Procrustes methods in the statistical analysis of shape. J
R Stat Soc Ser B Stat Methodol 53:285339
Grant PR, Grant BR (2002)Unpredictable evolution in a 30-yearstudy of
Darwins finches. Science 296:707711
Herrel A, Damme RV, Vanhooydonck B, Vree FD (2001) The implica-
tions of bite performance for diet in two species of lacertid lizards.
Can J Zool 79:662670
Herrel A, Joachim R, Vanhooydonck B, Irschick DJ (2006) Ecological
consequences of ontogenetic changes in head shape and bite perfor-
mance in the Jamaican lizard Anolis lineatopus.BiolJLinnSoc89:
Holmes MW, Boykins GKR, Bowie RCK, Lacey EA (2015) Cranial
morphological variation in Peromyscus maniculatus over nearly a
century of environmental change in three areas of California. J
Morpho 277:96106
Kalcounis-Rüppell MC, Millar JS (2002) Partitioning of space, food, and
time by syntopic Peromyscus boylii and P californicus.JMammal
Kardong KV (2014) Vertebrates: comparative anatomy, function, evolu-
tion Boston: McGraw-Hill Education
Kaufman DW, Kaufman GA (1989) Population biology. In: Kirkland G,
Layne J (Eds) Advances in the study of Peromyscus Rodentia.
Lubbock, pp 233271
La Croix S, Holekamp KE, Shivik JA, Lundrigan BL, Zelditch ML
(2011) Ontogenetic relationships between cranium and mandible
in coyotes and hyenas. J Morpho 272:662674
Law CJ, Venkatram V, Mehta RS (2016a) Sexual dimorphism in
craniomandibular morphology of southern sea otters (Enhydra lutris
nereis). J Mammal 97:17641773
Law CJ, Young C, Mehta RS (2016b) Ontogenetic scaling of theoretical
bite force in southern sea otters (Enhydra lutris nereis). Physiol
Biochem Zool 89:347363
Maestri R, Patterson BD, Fornel R, Monteiro LR, Freitas TRO (2016)
Diet, bite force and skull morphology in the generalist rodent
morphotype. J Evol Biol 29:21912204
Maki K, Nishioka T, Shioiri E, Angle TTT (2002) Effects of dietary
consistency on the mandible of rats at the growth stage: computed
X-ray densitometric and cephalometric analysis. Angle Orthod 72:
Mori A, Vincent SE (2008) An integrative approach to specialization:
relationships among feeding morphology, mechanics, behaviour,
performance and diet in two syntopic snakes. J Zool 275:4756
Myers P, Gillespie BW, Zelditch ML (1996) Phenotypic plasticityin skull
and dental morphology in the prairie deer mouse (Peromyscus
maniculatus bairdii). J Morpho 229:229237
Pfaller JB, Gignac PM, Erickson GM (2011) Ontogenetic changes in jaw-
muscle architecture facilitate durophagy in the turtle Sternotherus
minor. J Exp Biol 214:16551667
Pianka ER (1973) The structure of lizard communities. Annu Rev Ecol
Syst 4:5374
R Core Team (2017) R: A language and environment for statistical
Reid REB, Greenwald EN, Wang Y, Wilmers CC (2013) Dietary niche
partitioning by sympatric Peromyscus boylii and P. californicus in a
mixed evergreen forest. J Mammal 94:12481257
Rohlf FJ (2005) TpsDig, digitize landmarks and outlines, version 25
Department of Ecology and Evolution, State University of New
York at Stony Brook New York, USA, Available at:
Rohlf FJ, Slice D (1990) Extensions of the Procrustes method for the
optimal superimposition of landmarks. Syst Zool 39:4021
Root RB (1967) The niche exploitation pattern of the blue-gray gnat-
catcher. Ecol Monogr 37:317350
Santana SE, Dumont E, Davis JL (2010) Mechanics of bite force produc-
tion and its relationship to diet in bats. Funct Ecol 24:776784
Schlager S (2016) Morpho: calculations and visualisations related to
Geometric Morphometrics R-package version 24
Schoener TW (1974) Resource partitioning in ecological communities.
Science 185:2739
Smartt RA (1978) A comparison of ecological and morphological overlap
in a Peromyscus community. Ecology 59:216220
Tanner JB, Zelditch ML, Lundrigan BL (2010) Ontogenetic change in
skull morphology and mechanical advantage in the spotted hyena
(Crocuta crocuta). J Morpho 271:353365
Timm-Davis LL, DeWitt TJ, Marshall CD (2015) Divergent skull mor-
phology supports two trophic specializations in otters (Lutrinae).
PLoS One 10:e0143236e0143218
Turnbull WD (1970) Mammalian masticatory apparatus Field Museum of
Natural History
van der Meij MAA, Bout RG (2006) Seed husking time and maximal bite
Verwaijen D, Van Damme R, Herrel A (2002) Relationships between
head size, bite force, prey handling efficiency and diet in two sym-
patric lacertid lizards. Funct Ecol 16:842850
Wainwright PC (1991) Ecomorphology: experimental functional anato-
my for ecological problems. Amer Zool 31:680693
Wainwright PC, Alfaro ME, Bolnick DI, Hulsey CD (2005) Many-to-one
mapping of form to function: a general principle in organismal de-
sign? Integr Comp Biol 45:256262
Watt DG, Williams CHM (1951) The effects of the physical consistency
of food on the growth and development of the mandible and the
maxilla of the rat. Am J Orthod 37:895928
Žagar A, Carretero MA, Vrezec A, Drašler K, Kaliontzopoulou A (2017)
Towards a functional understanding of species coexistence:
ecomorphological variation in relation to whole-organism perfor-
mance in two sympatric lizards. Funct Ecol 211:13361312
Zelditch ML, Swiderski DL, Sheets HD (2012) Geometric morphomet-
rics for biologists: a primer Academic Press
Mamm Res
... Females showed relatively longer moment arms of the ventral fibers of the superficial masseter and anterior deep masseter, which may increase the strength of incisor bite (Casanovas-Vilar & van Dam 2013;Jones & Law 2018). Subsequently, surface area of the vertical ramus (ascending ramus) of the mandible might be increased with respect to the longer mandibular body length in females, although oral (ManneWhitney U ¼ 83.0, P ¼ 0.071) and aboral (ManneWhitney U ¼ 79.5, P ¼ 0.053) heights of the vertical ramus of the mandible statistically did not differ between sexes. ...
... Subsequently, surface area of the vertical ramus (ascending ramus) of the mandible might be increased with respect to the longer mandibular body length in females, although oral (ManneWhitney U ¼ 83.0, P ¼ 0.071) and aboral (ManneWhitney U ¼ 79.5, P ¼ 0.053) heights of the vertical ramus of the mandible statistically did not differ between sexes. Considering only mandible, CVA also indicated that the sexes are highly discriminated by oral and aboral heights of the vertical ramus of the mandible, which may increase the surface area for masticatory muscles (Suzuki et al. 2011;Casanovas-Vilar & van Dam 2013;Jones & Law 2018). Therefore, ascending ramus of the mandible in females of P. leucogenys might have relatively more surface area for muscle attachment. ...
... Casanovas-Vilar & van Dam 2013;Law et al. 2016;Jones & Law 2018). The measurements of the incisor resistance arm (RI) and primary masticatory muscles, such as moment arm of the most dorsal fiber of the temporalis (MT), moment arm of the most ventral fibers of the temporalis (MT2), moment arm of the most dorsally inserting fibers of the superficial masseter (MSM), moment arm of the most ventral fibers of the superficial masseter (MSM2), moment arm of the most anterior fibers of the anterior deep masseter (MADM), were taken following Casanovas-Vilar & van Dam (2013)(Fig. ...
We examined sexual dimorphism and variability of craniomandibular morphology in the Japanese giant flying squirrel (Petaurista leucogenys) using different statistical analyses. Among 31 measurements using 33 adult skulls (19 males and 14 females), females showed slightly larger mean size for all traits. Univariate analysis revealed that females were significantly larger than males for the greatest length of skull, zygomatic breadth, and mandibular length. Discriminant functions indicated well distinctiveness between the sexes. Moreover, six additional mandibular measurements were taken for estimating the mechanical advantage of the primary masticatory muscles, of which females showed significantly larger incisor resistance arm and moment arms of the superficial masseter (most ventral fibers) and the anterior deep masseter than males. These traits could increase the surface area for the attachment of masticatory muscles and thus have a role in biting mechanism. These suggest that larger females have relatively greater absolute bite force, which may contribute to obtain more access for greater ecological resources. Additionally, the coefficients of variation did not differ significantly between the sexes. Patterns of variability tended to differ in the cranial dimensions based on longitudinal and transverse axes, but not obviously in the major subdivisions of the skull. The observed variability patterns suggest the existence of developmental factors and higher integration to maintain functional relationship related to their lifestyle. Finally, we identified craniomandibular dimorphism in P. leucogenys as a size related phenomenon mostly associated with resource benefits, despite similarities in variability caused by morphological constraint.
... Ecomorphology can be the product of several, at times opposing, selective processes that may not persist through the entire evolutionary history of deep lineages. At shallow timescales, different processes, including divergent ecological selection of morphology and behavior, hybridization, and interspecific competition, can be important initiators of ecomorphological diversity [1][2][3]. Hybrid zones representing secondary contact and hybridization between ecologically divergent species are practical arenas to investigate how these three different processes impact variation on ecomorphology at shallow timescales. In hybrid zones that span ecological transitions, differences in phenotypic variation between species is subject to the homogenizing effects of gene flow and its counterposing force, divergent selection [4][5][6]. ...
... Hybridization leads to novel epistatic interactions between differentiated genomes, which may allow for a change in morphospace occupation due to a relaxation of trait covariation [13,14]. Thus, hybridization can immediately lead to (1) hybrid phenotypes that are intermediate between the parental phenotypes [15,16]; (2) hybrid phenotypes that resemble one of the parental phenotypes, reflecting genetic dominance [17][18][19]; or (3) transgressive hybrid phenotypes that are more extreme than either parental phenotype [20][21][22][23][24]. The consequences of evolutionary forces on hybrid phenotypes are also varied and range from strong selection against hybrid morphologies [25] to selection that favors novel hybrid morphologies [2,3]. ...
Full-text available
Bite force can be a limiting factor in foraging and can significantly affect the competitive ability and lifetime fitness of mammals. Tamiasciurus squirrels feed primarily on conifer seeds and have a strong bite force to mechanically extract seeds from conifer cones with their mouths. In the North Cascades region, Douglas squirrels (Tamiasciurus douglasii) and red squirrels (T. hudsonicus) occupy ecologically different forests with different hardnesses in conifer cones. The ranges of these species overlap in a narrow hybrid zone where these forests meet near the crest of the North Cascades. We examined interspecific divergence in dietary ecomorphology in allopatry, in sympatry within the hybrid zone, and between hybrids and each parental species. We focused on three craniodental traits, including the incisor-strength index as a proxy measure for maximal bite force, cranial-suture complexity, and mandible shape. We find that these sister squirrel species differ in bite force and suture complexity in allopatry and sympatry and that mandible shape changes with the expected hardness of accessed food items, but is not significantly different between species. Furthermore, we find that hybrids display morphologies that overlap with hybrid zone red squirrels but not with hybrid zone Douglas squirrels. This work shows how important ecological processes at shallow evolutionary timescales can impact the divergence of morphological traits in taxa with extreme conservation of craniomandibular shape.
... Larger taxa can dive deeper and longer, display lower relative metabolic rates than smaller taxa [6][7][8][9][10] and can exploit a vaster diversity of prey by reaching greater depths. Skull traits can limit prey size and processing efficiency [4,[11][12][13][14], further influencing foraging dynamics [15][16][17][18][19]. Few studies have quantified the relationship between body size, feeding morphology and foraging ecology in co-occurring marine tetrapods (e.g. ...
Full-text available
Body size and feeding morphology influence how animals partition themselves within communities. We tested the relationships among sex, body size, skull morphology and foraging in sympatric otariids (eared seals) from the eastern North Pacific Ocean, the most diverse otariid community in the world. We recorded skull measurements and stable carbon (δ13C) and nitrogen (δ15N) isotope values (proxies for foraging) from museum specimens in four sympatric species: California sea lions (Zalophus californianus), Steller sea lions (Eumetopias jubatus), northern fur seals (Callorhinus ursinus) and Guadalupe fur seals (Arctocephalus townsendi). Species and sexes had statistical differences in size, skull morphology and foraging significantly affecting the δ13C values. Sea lions had higher δ13C values than fur seals, and males of all species had higher values than females. The δ15N values were correlated with species and feeding morphology; individuals with stronger bite forces had higher δ15N values. We also found a significant community-wide correlation between skull length (indicator of body length), and foraging, with larger individuals having nearshore habitat preferences, and consuming higher trophic level prey than smaller individuals. Still, there was no consistent association between these traits at the intraspecific level, indicating that other factors might account for foraging variability.
... Ранее в ряде работ (Young et al., 2010;Anderson et al., 2014;Jones, Law, 2018) были предложены методы оценки функциональных изменений формы нижней челюсти млекопитающих, связанных с разной диетой, на основе применения мандибулярных индексов. Расчеты индивидуальных значений морфофункциональных мандибулярных индексов белобрюхой белозубки по аналогии с ранее использованными выполнили с помощью промеров нижней челюсти (см. ...
... For this reason, many organisms show a close association between morphology and ecology, i.e., ecomorphology (Bock, 1994), that reflects divergence and adaptation to different environments. Examples of this association abound across diverse taxa, from insects (Günter et al., 2019;Hughes & Vogler, 2004;Lemic et al., 2016) to fish (Baldasso et al., 2019;Buser et al., 2019;Jacquemin & Pyron, 2016), amphibians (Ficetola et al., 2016;Rebelo & Measey, 2019;Sherratt et al., 2018), reptiles (Kahrl et al., 2018;Kamath & Losos, 2016;Rivera, 2008), mammals (Alvarado-Serrano et al., 2013;Baier & Hoekstra, 2019;Jones & Law, 2018), and birds (Bravo et al., 2014;Phillips et al., 2020;Pigot et al., 2020;Vanhooydonck et al., 2009). The close connection between morphology and ecology is exemplified at different temporal scales, from rapid evolution in adaptive radiations (e.g., Darwin's finches, Hawaiian honeycreepers; Schluter & Grant, 1984;Tokita et al., 2016) to macroevolutionary change in deep time (Felice et al., 2019;Pigot et al., 2020; but see Phillips et al., 2020). ...
Full-text available
The relationship between ecology and morphology is a cornerstone of evolutionary biology, and quantifying variation across environments can shed light on processes that give rise to biodiversity. Three morphotypes of the Steller's Jay (Cyanocitta stelleri) occupy different ecoregions in western North America, which vary in climate and landcover. These morphotypes (Coastal, Interior, Rocky Mountain) differ in size, plumage coloration, and head pattern. We sampled 1080 Steller's Jays from 68 populations (plus 11 outgroups) to address three main questions using data on morphology , plumage, genetics (mtDNA, microsatellites), and ecological niches: (1) How do phenotypic and genetic traits vary within and among populations, morphotypes, and ecoregions? (2) How do population-level differences in Steller's Jays compare with other sister species pairs of North American birds? (3) What can we infer about the population history of Steller's Jays in relation to past climates, paleoecology, and niche evolution? We found substantial morphological, genetic, and ecological differentiation among morphotypes. The greatest genetic divergence separated Coastal and Interior morphotypes from the Rocky Mountain morphotype, which was associated with warmer, drier, and more open habitats. Microsatellites revealed additional structure between Coastal and Interior groups. The deep mtDNA split between Coastal/ Interior and Rocky Mountain lineages of Steller's Jay (ND2 ~ 7.8%) is older than most North American avian sister species and dates to approximately 4.3 mya. Interior and Rocky Mountain morphotypes contact across a narrow zone with steep clines in traits and reduced gene flow. The distribution of the three morphotypes coincides with divergent varieties of ponderosa pine and Douglas fir. Species distribution models support multiple glacial refugia for Steller's Jays. Our integrative dataset combined with extensive geographic sampling provides compelling evidence for recognizing at least two species of Steller's Jay.
... Lever arms have been used to provide a reasonable first approximation of MA in a number of previous studies (e.g. Casanovas-Vilar & van Dam, 2013;Renaud et al., 2015;Gomes Rodrigues et al., 2016;Jones & Law, 2018;West & King, 2018), but it should be noted that variations in mandibular morphology can rotate lever arms thus changing moment arms without altering the length of the lever arms. Secondly, the representation of a muscle insertion as a single point is a clear over-simplification as the temporalis, superficial masseter and deep masseter all have large attachment sites on the squirrel mandible (Cox & Jeffery, 2011. ...
Full-text available
Isolation due to habitat fragmentation can lead to morphological and functional variation between populations, with the effect being well documented in rodents. Here, we investigated whether such morphological variation could be identified between British populations of the Eurasian red squirrel (Sciurus vulgaris). This species was once widespread across Great Britain, but suffered a severe population decline across the 20th century, leaving a highly fragmented distribution. The aim was to test for morphological and biomechanical variation of the mandible between the remaining British red squirrel populations, and between British and continental European red squirrels. Linear and geometric morphometric methods were used to analyse shape in a sample of over 250 red squirrel hemi-mandibles from across Britain plus a sample from Germany representing the central European subspecies. Procrustes ANOVA identified significant shape variation between populations, with particularly distinct differences being noted between red squirrels from Germany and several British red squirrel populations, which may reflect their evolutionary history. Linear biomechanical measurements showed that the red squirrels from Formby and Jersey had a significantly lower mechanical advantage of the temporalis muscle than other British populations, suggesting they were less efficient at gnawing. This functional difference may be related to many factors, such as founder effect, potential inbreeding and/or past supplemental feeding with less mechanically resistant food items.
Two congeneric species of Japanese field mice, Apodemus speciosus and A. argenteus, differ considerably in their feeding strategies and habitat utilizations. Although both species are omnivorous, previous studies demonstrated that A. argenteus typically eats a wide variety of food items than A. speciosus. Moreover, A. speciosus is a ground dweller, while A. argenteus commonly shows arboreal movements. These dietary and lifestyle differences suggest potential disparity in morphological structure. In this study, we used geometric morphometrics to examine the skull shape differences are related to their feeding strategies and habitat preferences. We found that A. argenteus showed wider zygomatic arches and a broader mandibular ramus. These traits are linked to enlargement of the attachment sites for the masticatory muscles. We also found a relatively short mandibular diastema in A. argenteus, which may increase the mechanical advantage of the lower jaw by reducing the out-lever arm. These results suggest that A. argenteus has a greater relative bite force that is suitable for diversified diets as a more generalist feeder. Interspecific differences in the upper incisor, inter-orbital width, and auditory bullae might be associated with the lifestyles of these two species. Additionally, the presence of two distinct modules in the cranium (rostrum and braincase) and mandible (ascending ramus and alveolar region) may reflect similar patterns of intraspecific variation within both species. In conclusion, skull shape enables distinction between these two species and may favor adaptation to their ecology and lifestyle, despite the similarities in craniomandibular modules associated with common developmental factors.
Full-text available
1.We examined intra- and interspecific variation in functional morphology and whole-organism performance in a sympatric lizard species pair, Iberolacerta horvathi and Podarcis muralis, in the area with a high potential for competition. 2.The biggest variation between species was found in two functional traits, bite force and climbing speed, linked with corresponding morphological traits. 3.The species with larger and taller heads, P. muralis, exhibited correspondingly stronger bite forces. The other species exhibited smaller and flatter head. Both traits may potentially promote segregation between species in trophic niche (stronger bites relate to harder prey) and in refuge use (flatter heads allow using narrower crevices, hence, influencing escaping from common predators). Stronger bites and larger heads also provide one species with a dominant position in interspecific agonistic interactions. 4.Females had longer trunks that impacted negatively on climbing speed, which may lower anti-predator escape abilities of the more trunk-dimorphic species, but positively influence reproductive effort. 5.Our results exemplify how the joint examination of morphological and functional traits of ecologically similar and sympatric species can provide a mechanistic background for understanding their coexistence, namely syntopic populations that are frequent in the study area. 6.The identified roles of functional morphology in this system of sympatric rock lizards support the contribution of functional diversification for the complexity of community structure via coexistence.
Full-text available
The niche divergence hypothesis suggests that if a species exhibits intersexual differences in diet, selection should favor divergence in the feeding apparatus between the sexes. Recent work revealed that male and female southern sea otters (Enhydra lutris nereis) utilize different dietary resources in response to increased population density; females exhibit more specialized diets as a function of smaller home ranges, whereas males exhibit larger home ranges, potentially allowing them to expand their dietary breadths by feeding on prey items that are not found in female home ranges. These dietary differences suggest the potential for sexual dimorphism of the feeding apparatus (i.e., the skull). Here, we tested the hypothesis that male and female southern sea otters exhibit differences in craniomandibular traits directly related to biting ability. Univariate and multivariate analyses of 12 craniomandibular traits showed that size is the primary axis of skull variation, whereas only a handful of craniomandibular traits demonstrated significant shape differences between the sexes. Relative postorbital constriction breadth, masseter in-lever length, and cranial height differed significantly between the sexes. These 3 traits can increase the surface area of jaw muscle attachment sites and thus are directly linked to the mechanics of biting ability. Collectively, these morphological differences indicate that niche divergence may be an important mechanism maintaining sexual dimorphism in southern sea otters.
Full-text available
Sexual dimorphism attributed to niche divergence is often linked to differentiation between the sexes in both dietary resources and characters related to feeding and resource procurement. Although recent studies have indicated that southern sea otters (Enhydra lutris nereis) exhibit differences in dietary preferences as well as sexual dimorphism in skull size and shape, whether these intersexual differences translate to differentiation in feeding performances between the sexes remains to be investigated. To test the hypothesis that scaling patterns of bite force, a metric of feeding performance, differ between the sexes, we calculated theoretical bite forces for 55 naturally deceased male and female southern sea otters spanning the size ranges encountered over ontogeny. We then used standardized major axis regressions to simultaneously determine the scaling patterns of theoretical bite forces and skull components across ontogeny and assess whether these scaling patterns differed between the sexes. We found that positive allometric increases in theoretical bite force resulted from positive allometric increases in physiological cross-sectional area for the major jaw adductor muscle and mechanical advantage. Closer examination revealed that allometric increases in temporalis muscle mass and relative allometric decreases in out-lever lengths are driving these patterns. In our analysis of sexual di- morphism, we found that scaling patterns of theoretical bite force and morphological traits do not differ between the sexes. How- ever, adult sea otters differed in their absolute bite forces, revealing that adult males exhibited greater bite forces as a result of their larger sizes. We found intersexual differences in biting ability that provide some support for the niche divergence hypothesis. Continued work in this field may link intersexual differences in feeding functional morphology with foraging ecology to show how niche divergence has the potential to reinforce sexual dimorphism in southern sea otters.
Full-text available
For many vertebrate species, bite force plays an important functional role. Ecological characteristics of a species' niche, such as diet, are often associated with bite force. Previous evidence suggests a biomechanical trade-off between rodents specialized for gnawing, which feed mainly on seeds, and those specialized for chewing, which feed mainly on green vegetation. We tested the hypothesis that gnawers are stronger biters than chewers. We estimated bite force and measured skull and mandible shape and size in 63 genera of a major rodent radiation (the myomorph sigmodontines). Analysis of the influence of diet on bite force and morphology was made in a comparative framework. We then used phylogenetic path analysis to uncover the most probable causal relationships linking diet and bite force. Both granivores (gnawers) and herbivores (chewers) have a similar high bite force, leading us to reject the initial hypothesis. Path analysis reveals that bite force is more likely influenced by diet than the reverse causality. The absence of a trade-off between herbivores and granivores may be associated with the generalist nature of the myomorph condition seen in sigmodontine rodents. Both gnawing and chewing sigmodontines exhibit similar, intermediate phenotypes, at least compared to extreme gnawers (squirrels) and chewers (chinchillas). Only insectivorous rodents appear to be moving towards a different direction in the shape space, through some notable changes in morphology. In terms of diet, natural selection alters bite force through changes in size and shape, indicating that organisms adjust their bite force in tandem with changes in food items.
Morphometrics, a new branch of statistics, combines tools from geometry, computer graphics and biometrics in techniques for the multivariate analysis of biological shape variation. Although medical image analysts typically prefer to represent scenes by way of curving outlines or surfaces, the most recent developments in this associated statistical methodology have emphasized the domain of landmark data: size and shape of configurations of discrete, named points in two or three dimensions. This paper introduces a combination of Procrustes analysis and thin-plate splines, the two most powerful tools of landmark-based morphometrics, for multivariate analysis of curving outlines in samples of biomedical images. The thin-plate spline is used to assign point-to-point correspondences, called semi-landmarks, between curves of similar but variable shape, while the standard algorithm for Procrustes shape averages and shape coordinates is altered to accord with the ways in which semi-landmarks formally differ from more traditional landmark loci. Subsequent multivariate statistics and visualization proceed mainly as in the landmark-based methods. The combination provides a range of complementary filters, from high pass to low pass, for effects on outline shape in grouped studies. The low-pass version is based on the spectrum of the spline, the high pass, on a familiar special case of Procrustes analysis. This hybrid method is demonstrated in a comparison of the shape of the corpus callosum from mid-sagittal sections of MRI of 25 human brains, 12 normal and 13 with schizophrenia.