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Received: 13 October 2022 Revised: 5 December 2022 Accepted: 6 December 2022
DOI: 10.1002/ar.25142

RESEARCH ARTICLE

Endocast, brain, and bones: Correspondences and spatial

relationships in squamates

Rémi Allemand 1 | Jade Abdul-Sater 1 | Simone Macrì 2 | Nicolas Di-Poï 2 |

Gheylen Daghfous 3 | Mary T. Silcox 1

1
Department of Anthropology, University
of Toronto Scarborough, Toronto,
Ontario, Canada
2
Institute of Biotechnology, Helsinki
Institute of Life Science, University of
Helsinki, Helsinki, Finland
3
Biodôme de Montréal, Montréal,
Québec, Canada
Correspondence
Rémi Allemand, Department of
Anthropology, University of Toronto
Scarborough, Toronto, Ontario M1C 1A4,
Canada.
Email: remi.allemand@gmail.com
Abstract
Vertebrate endocasts are widely used in the fields of paleoneurology and
comparative neuroanatomy. The validity of endocranial studies is dependent
upon the extent to which an endocast reflects brain morphology. Due to the
variable neuroanatomical resolution of vertebrate endocasts, direct informa-
tion about the brain morphology can be sometimes difficult to assess and
needs to be investigated across lineages. Here, we employ X-ray computed
tomography (CT), including diffusible iodine-based contrast-enhanced CT, to
qualitatively compare brains and endocasts in different species of squamates.
The relative position of the squamate brain within the skull, as well as the
variability that may exist in such spatial relationships, was examined to help
clarify the neurological regions evidence on their endocasts. Our results indicate
that squamate endocasts provide variable representation of the brain, depending
on species and neuroanatomical regions. The olfactory bulbs and peduncles,
cerebral hemispheres, as well as the medulla oblongata represent the most easily
discernable brain regions from squamate endocasts. In contrast, the position of
the optic lobes, the ventral diencephalon and the pituitary may be difficult to
determine depending on species. Finally, squamate endocasts provide very lim-
ited or no information about the cerebellum. The spatial relationships revealed
here between the brain and the surrounding bones may help to identify each of
the endocranial region. However, as one-to-one correspondences between a
bone and a specific region appear limited, the exact delimitation of these regions
may remain challenging according to species. This study provides a basis for
further examination and interpretation of squamate endocast disparity.

KEYWORDS
brain, endocast, qualitative comparisons, skull, spatial relationships, squamate

1 | INTRODUCTION Allen, 2022; Schade et al., 2022; Weisbecker et al., 2021;

Cranial endocasts are used to investigate the neuroanatomy
of both extant and extinct vertebrates (e.g., Aristide
et al., 2019; Benoit et al., 2017; Beyrand et al., 2019; Iwaniuk
et al., 2020; Lautenschlager et al., 2018; Lynch &
Zhu et al., 2020). Virtual endocasts, generated by the
increasingly widespread use of computed tomographic
scanning, provide the potential to track evolution of brain
external morphology through deep time, and the possibil-
ity to infer cognitive and sensory abilities, as well as

Anat Rec. 2022;1–23. wileyonlinelibrary.com/journal/ar © 2022 American Association for Anatomy. 1


2 ALLEMAND ET AL.
behavior, of taxa (e.g., Balanoff & Bever, 2017; Dozo
et al., 2022; Holloway et al., 2009; Jerison, 1973;
Neubauer, 2014; Racicot, 2021). Nevertheless, despite the
capacity of endocranial studies to provide such valuable
information, inferring the external brain morphology from
an endocast can remain challenging as variable degrees of
neuroanatomical resolution may occur depending on taxa.
In this context, determining the degree of accuracy to
which an endocast reflects details of brain morphology
appears extremely important in order to avoid erroneous
interpretations based on endocast morphologies alone.
Discussion of the neuroanatomical resolution of ver-
tebrate endocasts has historically been centered on trying
to get an accurate estimate of brain size by considering
the percentage of the endocranial cavity filled by the
whole brain (e.g., Edinger, 1951; Hopson, 1979;
Jerison, 1973), this factor being measured through the
ratio between brain and endocast volumes (i.e., brain-to-
endocranial cavity [BEC] index, Balanoff et al., 2016).
Taxa in which the brain fills most of the endocranial
space (high BEC values) can be expected to produce an
endocast that reflects brain volume and morphology with
high fidelity (e.g., Dumoncel et al., 2020; Early, Iwaniuk,
et al., 2020; Early, Ridgely, et al., 2020; Iwaniuk &
Nelson, 2002; Watanabe, Gignac, et al., 2019). In contrast,
taxa in which the brain fills a relatively small portion of
the endocranial cavity (low BEC values) show a more
cylindrical endocast bearing less resemblance to the actual
brain (e.g., Hopson, 1979; Jerison, 1973; Watanabe,
Gignac, et al., 2019). The degree to which the brain actu-
ally fills the endocranial cavity varies greatly between and
within vertebrate lineages, and high BEC values have been
found in mammals (e.g., De Miguel & Henneberg, 1998;
Haight & Nelson, 1987; Jerison, 1969, 1973; Macrini
et al., 2007), birds (Iwaniuk & Nelson, 2002), osteichthyan
fishes (Bjerring, 1991; Giles & Friedman, 2014; Northcutt,
2002), amphibians (Clement et al., 2021), as well as squa-
mates (Kim & Evans, 2014). This suggests that endocasts
exhibiting good neuroanatomical resolution are potentially
found in diverse members of all major vertebrate groups
and not limited to some lineages. However, the faithful
reproduction of details of brain morphology on endocra-
nial surfaces does not exclusively depend on brain relative
size and the endocranial cavity fraction it occupies.
Indeed, endocasts, as internal molds of the braincase, also
include several non-neural components that share the
endocranial space with the brain, such as the meninges,
arteries, venous sinuses, cerebrospinal fluid, and the roots
of cranial nerves (Balanoff & Bever, 2017; Butler &
Hodos, 2005). These structures exhibit variable sizes across
vertebrates (e.g., thin meninges in birds compared to other
vertberates, Balanoff & Bever, 2017; Iwaniuk &
Nelson, 2002) and as such can significantly influence the
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reliability of endocasts for reflecting surface details of the
whole brain, or at least for some brain regions. For
instance, the thick meninges in mammals can sometimes
obscure surface features of the whole brain such as cere-
bral gyri and sulci (e.g., Falk, 2014; Holloway, 1978), and
the inflation of the occipital sinus in some archosaurs may
produce a prominent dural peak over the hindbrain,
obscuring details of the cerebellar region on the endocast
(e.g., McKeown et al., 2020; Witmer et al., 2008). Finally,
as cartilaginous elements inside the braincase can persist
until adulthood in some vertebrates (e.g., turtles,
Werneburg et al., 2021), the structural architecture of the
braincase itself may represent an obstacle to assessing
brain morphology using endocasts.
Depending on these factors, the neuroanatomical
resolution of endocasts varies greatly between and
within vertebrate lineages. Thus, direct information
about the brain morphology can be sometimes difficult
to assess from the endocast, challenging our under-
standing of the degree to which the endocranial mor-
phology correlates with the complexity of the brain
itself (Balanoff & Bever, 2017). In view of these difficul-
ties, partitioning the endocast into neurologically mean-
ingful regions has been attempted by using homologous
osteological landmarks (Balanoff et al., 2013, 2016;
Morhardt, 2016). Although such an approach appears
useful to delimit underlying general brain regions on
endocasts (e.g., cerebral hemispheres, olfactory bulbs,
optic lobes, pituitary, and cerebellum), such studies have,
so far, been limited to archosaurian brains (Balanoff
et al., 2013, 2016; Morhardt, 2016), and relationships
between bony landmarks and neuroanatomy require
verification in a broader sample of vertebrate lineages
(Balanoff & Bever, 2017).
This study aims to determine the extent to which
endocasts in Squamata (“lizards” and snakes) may reflect
brain morphologies. Jerison (1973) made the first attempt
at determining the level of resolution of squamate endo-
casts. By comparing the brain and endocast of the green
iguana (Iguana iguana), Jerison (1973) stated that the
mesencephalon would be incorrectly identified from the
endocast as it seems to lie posterior to its actual position.
Although Jerison (1973) did not discuss the degree of
endocast resolution for other brain regions, he concluded
that overall the endocast of Iguana iguana shows a brain-
like shape and is approximately twice the size of the
brain, whether or not cartilage is present (Jerison, 1973,
p. 29). Since then, several studies have shown that the
brain in squamates fits into the endocranial cavity in
ways that vary depending on taxa, and may occupy more
than 50% of the endocranial space (e.g., Kim &
Evans, 2014; Perez-Martinez & Leal, 2021; Starck, 1979;
ten Donkelaar, 1998; Triviño et al., 2018).

ALLEMAND ET AL.
In addition, Scanferla (2022) published the first com-
parative survey evaluating the endocranial resolution in
snakes. By comparing endocasts and corresponding
brains of different species, Scanferla (2022) qualitatively
showed that snake endocasts represent a realistic repre-
sentation of brain size and shape. It is worth noting that
the variable neuroanatomical resolutions in snake endo-
casts impact the identification of brain regions and may
result in different interpretations. For instance, the snake
cerebellum was reported as indistinguishable from snake
endocasts in Allemand et al. (2017) and Scanferla (2022),
but stated as easily identifiable in Segall et al. (2021). Up-
to-date, such discussions about the degree of endocranial
resolution remain limited to snakes. Indeed, as endocra-
nial studies in squamates have been, so far, mainly
focused on snakes (Allemand et al., 2017; Olori, 2010;
Scanferla, 2022; Segall et al., 2021; Triviño et al., 2018),
“lizard” endocasts remains largely unknown and have
been only documented for the genera Varanus and
Amphisbaena (Allemand, 2017). However, despite the
lack of information, Allemand (2017) showed that endo-
casts in “lizards” exhibit variable neuroanatomical reso-
lutions depending on species that may, similar to snakes,
impact the identification of brain regions. In this context,
determining the degree of accuracy to which a squamate
endocast reflects the brain morphology, and how this
may vary according across the whole clade, appears of
prime interest in order to investigate the reliability of
endocasts as proxies of brain morphology.
Here, endocasts and corresponding brains of different
squamates, including snakes and “lizards”, are qualita-
tively compared in order to outline what an endocast does,
and does not, capture in terms of the brain anatomy, and
how this may vary according to species and brain regions.
As varying levels of neuroanatomical resolution are
expected on squamate endocasts, the spatial relationships
between the skull and the different brain regions are estab-
lished to help the regional delineation of the endocasts.
2 | MATERIALS AND METHODS
2.1 | Species sampling
Ten extant species of squamates, representing each major
clade (Pyron et al., 2013; Singhal et al., 2021), were
selected in order to sample the phylogenetic diversity of
Squamata (Table 1 and Figure 1). Squamate cranial anat-
omy shows remarkable variability in terms of morphology,
presence/absence and fusion of the bones surrounding the
endocranial cavity (e.g., Watanabe, Fabre, et al., 2019).
The sample chosen for study here was selected to repre-
sent that cranial diversity in order to examine the spatial
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3
relationships of squamate brains, and specimens were also
selected to represent a variety of different habitats
(Table 1) that may impact the cranial bone conformation
(e.g., Barros et al., 2011; Da Silva et al., 2018).
2.2 | Data acquisition
Computed-tomographic scans of adult squamate heads
were obtained from different sources (Table 1). Eight speci-
mens were sampled from the previously published work of
Macrì et al. (2019) (Table 1). Specimens have been fixed
and conserved in 10% formalin (museum specimens) or
fixed in 4% paraformaldehyde (fresh specimens), and
stained with 0.3% phosphotungstic acid (PTA) or 1%
iodine solutions (Macrì et al., 2019). High-resolution 3D CT
scans were then performed at the University of Helsinki
(Finland) using a Skyscan 1,272. Tissue fixation and stain-
ing procedures were performed using optimized concentra-
tions of fixatives and contrast agents based on previous
work, thus limiting artifacts such as shrinkage of brain
tissues, including in museum samples (Macrì et al., 2019).
A ninth specimen, Sphaerodactylus caicosensis, was
acquired from the online database MorphoSource (Boyer
et al., 2016; http://www.MorphoSource.org/). This speci-
men was fixed in 10% formalin, stored long-term in 70%
ethanol and stained with a solution of Lugol's iodine. The
scan of Sphaerodactylus was performed at the University of
Florida (USA) using General Electric phoenix vjtomejx
m240. A tenth specimen, Thamnophis sirtalis, was acquired
by one of the co-author (GD). The fresh specimen was fixed
in 4% paraformaldehyde and scanned at the European Syn-
chrotron Radiation Facility (ESRF, Grenoble, France) using
third-generation synchrotron microtomography on beam-
lines ID19 and BM5 (resolution between 5.0 and 14.9 μm;
reconstructions performed using filtered back-projection
algorithm with the ESRF PYHST software).
Image segmentation and visualization were performed
using the software Avizo version 2019.1 (Thermo Fisher
Scientific, USA). The segmentation tools were used to man-
ually reconstruct the endocast for each species by segment-
ing the internal surface of the bones, or of the dura mater
when no bones surround the endocranial cavity. Addition-
ally, each bone showing a direct contact with the endocra-
nial space was segmented individually, as was the whole
brain, the cranial nerves, and the endosseous labyrinth.
2.3 | Terminology
Here, qualitative comparisons between the squamate
brains and corresponding endocasts, as well as spatial
relationships between brains and crania, are organized
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4 ALLEMAND ET AL.

TABLE 1 List of the material analyzed

Collection Voxel
Families Species Source number Habitat modes References size (μm)
Sphaerodactylidae Sphaerodactylus Morphosource uf:herp:95971 Terrestrial Reynolds (2011) 10.8
caicosensis
Scincidae Melanoseps loveridgei Macrì et al. (2019) FS Cryptozoic Malonza and Bwong 10
(2011)
Scincidae Lepidothyris fernandi Macrì et al. (2019) FS Terrestrial Akani et al. (2002) 26
Blanidae Blanus cinereus Macrì et al. (2019) MS.1285 Burrower Gil et al. (1993) 10
Amphisbaenidae Leposternon scutigerum Macrì et al. (2019) MS.1196 Burrower Kearney (2003) 23
Anguidae Pseudopus apodus Macrì et al. (2019) MS.1586 Terrestrial Telenchev et al. (2017) 26.7
Tropiduridae Tropidurus torquatus Macrì et al. (2019) MS.1995 Semi-arboreal Siqueira et al. (2013) 22
Typhlopidae Xerotyphlops Macrì et al. (2019) MS.2033 Burrower Afsar et al. (2016) 12
vermicularis
Boidae Epicrates cenchria Macrì et al. (2019) FS Terrestrial Andrade-Junior et al. 20
(2020)
Colubridae Thamnophis sirtalis GD GD Unnumb Terrestrial Burger et al. (2004) 7.5

Note: Collection number: FS, freshly dissected sample from specialized retailers; GD, Gheylen Daghfous personal collection; MS, Finnish Museum of Natural
History; UF:herp, University of Florida Herpetology. Burrower and cryptozoic categories are defined as in Scanferla (2016). All voxels were isotropic.

according to major brain divisions (columnar model;
Puelles, 2009). We use the terms “endocast” and “brain”
to refer to two different structures. The term “endocast”
is used when we mean the internal space surrounded by
bones, and “brain” to refer to the organ contained in that
space. Each region of the endocast is referred to as the
cast of the corresponding brain structure (e.g., cast of the
cerebral hemispheres) to avoid any misunderstanding
when the two structures are compared.
avian reptiles in that it exhibits a tubular shape that is
longer than wide and has a smooth surface (Figures 2
and 3; Appendix S1). In lateral view, the squamate endo-
cast captures the variable cephalic and pontine flexures
observed on the brain, ranging from a nearly straight
(e.g., Blanus, Figure 2c,d; Thamnophis, Figure 2g,h) to a
more flexed structure (e.g., Lepidothyris, Figure 3j; Tropi-
durus, Figure 3n) in which the different regions are not
completely aligned on the same horizontal plane.

3 | R E SUL T S 3.1 | Telencephalon

The brain in squamates is surrounded by several bones
including the frontal and the parietal from the skull
roof, and the osseous elements forming the braincase:
orbitosphenoid/tabulosphenoid (absent in snakes),
para-basisphenoid, basioccipital, prootic, otooccipital,
and supraoccipital (Figure 1). In snakes and amphis-
baenians, the cavity is almost completely surrounded
by these bones, and the external surface of the dural
meninges surrounding the brain lie directly on their
internal surfaces. In non-amphisbaenian “lizards,”
osseous walls delimit only the dorsal surface and the
posterior part of the brain cavity. In the latter case, the
antero-ventral portion of the cavity remains non-
ossified and is only surrounded by the dura mater,
reinforced by a complex cartilaginous scaffolding
(e.g., Bellairs & Kamal, 1981; Yaryhin et al., 2021).
The squamate endocast follows the general organiza-
tion of the corresponding brain and is typical of non-
The telencephalic brain in squamates includes several
structures: the main olfactory bulbs (MOB), the acces-
sory olfactory bulbs (AOB), the olfactory peduncles, the
evaginated cerebral hemispheres and an unevaginated
portion called the basal telencephalon (i.e., telencephalon
medium or impar, ten Donkelaar, 1998). The MOB and
AOB correspond to the anterior-most structures of the
brain and are attached to the rostral pole of the cere-
bral hemispheres by olfactory peduncles of variable
size according to species (e.g., Schwenk, 1993). As both
the external morphology of the brain and the endocast
in squamates provide little information to allow the
differentiation of the olfactory bulbs from the pedun-
cles, the different structures are here reported as a
whole (indicated as “olf” in Figure 2). Moreover, the
basal telencephalon could not be delineated from our
reconstructions and only the cerebral hemispheres are
considered here.
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5

Legend on next page.

ALLEMAND ET AL.

FIGURE 1

6 ALLEMAND ET AL.
Olfactory bulbs and peduncles. The olfactory bulbs
and peduncles in squamates are roofed by the frontal
(Figures 4 and 5), corresponding to a fossa on the ventral
surface of the bone, and may extend posteriorly to be
ventral to the anterior parietal in some species
(e.g., Blanus, Figure 4a). In both snakes and amphisbae-
nians (Figure 4), the olfactory bulbs and peduncles are
almost fully encapsulated within bones and delimited,
laterally and ventrally, by the lateral descending flanges
of the frontal (i.e., sub-olfactory process), which extend
either on its entire antero-posterior length (snakes) or
only its anterior half (amphisbaenians). In amphisbae-
nians, the posterior half of the whole structure is bor-
dered dorsally and laterally by the anterior parietal, and
ventrally by the anterior orbitosphenoid/tabulosphenoid
(e.g., Blanus, Figure 4a). In non-amphisbaenian “lizards,”
the olfactory bulbs and peduncles are not enclosed only
by bones (Figure 5) and their delimitation is defined, to
variable degrees, by a mix between the frontal cranial
crests, and the dura mater supported by the planum
supraseptale of the orbitotemporal chondocranium
(indicated as “ps” in Pseudopus, Figure 5c).
Although the anterior end of the olfactory bulbs
forms a distinct limit to the squamate brain, the delimita-
tion of the corresponding cast is less well differentiated
as it cannot be distinguished from the course of the olfac-
tory fila. In all species, the imprints left on the ventral
surface of the frontal may help to delimit the anterior-
most extent of the cast. Such a limit coincides with the
anterior end of the brain olfactory bulbs in most species
(e.g., Epicrates, Figure 4d). However, the correspondence
is not consistent across squamates, and the anterior-most
point of the endocast, reconstructed from the ventral
fossa on the frontal, extends further forward than the
anterior-most extent of the brain olfactory bulbs in
Thamnophis (Figures 4c and 7c,d) and Sphaerodactylus
(Figures 5d and 7q,r). It is worth noting that such a
feature may result from brain tissue shrinkage induced
by formalin fixation, exposure to iodine-based solutions,
as well as long-term storage ethanol (e.g., Buytaert
et al., 2014; Hedrick et al., 2018; Leonard et al., 2021;
Vickerton et al., 2013), and needs to be confirmed.
Posteriorly, the point of junction between the olfac-
tory peduncles and the posterior part of the telencepha-
lon is difficult to delineate in all squamates. As the
anterior part of the cerebral hemispheres in squamates
may overlap the posterior portion of the olfactory
F I G U R E 1 Schematic phylogenetic relationships of squamates sampled in the study (Modified from Pyron et al., 2013; Singhal
et al., 2021) associated with 3D renderings showing the crania of each species in lateral (left) and dorsal (right) views. Scale bars equal 2 mm.
Colored bones: Frontal (light green); parietal (light blue); Orbitosphenoid/Tabulosphenoid (light red) parabasisphenoid (dark blue);
supraoccipital (purple); Prootic (orange); Otooccipital (dark red); basioccipital (dark green); Otooccipital complex (yellow)
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peduncles (e.g., Anolis garmani, Armstrong et al., 1953;
Gecko gecko, Smeets et al., 1986), the exact position of
the junction cannot be established from the external
morphology of the brain or the endocast. In all squa-
mates studied here, the cast of the olfactory bulbs
and peduncles captures the overall morphology of the cor-
responding brain structure and displays a large range of
variability, from a short and stout aspect (e.g., Leposternon,
Figure 3a,b; Melanoseps, Figure 3g,h) to a more elongated
and slender one (e.g., Sphaerodactylus, Figure 3k,l; Tropi-
durus, Figure 3m,n). The medial limit separating the
paired olfactory bulbs and peduncles on the brain is only
indicated by a slight groove on the dorsal surface of the
endocast (e.g., Thamnophis, Figure 2e,f). This groove cor-
relates to the ventral bony ridge formed by the medial
suture between the two frontals, and in most species
separates the cast of the olfactory bulbs and peduncles
along its anterior–posterior length. In taxa in which the
two frontals are fused, such a groove may be less pro-
nounced (e.g., Sphaerodactylus, Figure 3k) or even absent
(e.g., Tropidurus, Figure 3m), challenging the medial
delineation of each olfactory bulbs and peduncles on the
endocast. In all species, both the relative proportions and
the orientation of the brain olfactory bulbs and peduncles
are reflected on the endocast (Figures 2 and 3). For exam-
ple, variations in the relative width of the brain structure
are comparable to the patterns that can be observed
from the endocast (e.g., the anterior part being as wide
[e.g., Xerotyphlops, Figure 3c] or wider [e.g., Lepidothyris,
Figure 3i] than the posterior part). Moreover, the anterior
part of the cast of the olfactory bulbs and peduncles,
similar to the corresponding brain, may be on the same
axis as the rest of the endocast (e.g., Epicrates, Figure 3f)
in lateral view, or it may project further ventrally
(e.g., Pseudopus, Figure 2k,l).
Cerebral Hemispheres. Posterior to the olfactory
peduncles, the squamate cerebral hemispheres and the
corresponding cast expand laterally and ventrally to form
the largest part of the brain and the endocast (“cer” in
Figure 2). In most species, the cerebral hemispheres
are roofed by the parietal (e.g., Thamnophis, Figure 4c;
Pseudopus, Figure 5c), whereas in both Lepidothyris
(Figure 5a) and Tropidurus (Figure 5e), the anterior part
of the structure is covered by the posterior part of the
frontal. The cerebral hemispheres in both snakes and
amphisbaenians are almost fully encapsulated by bones
(Figure 4). In Epicrates and Thamnophis, the structure is
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7

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ALLEMAND ET AL.

FIGURE 2
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8 ALLEMAND ET AL.

surrounded by the parietal and its lateral downgrowths
(Figure 4c,d). In both species, the antero-ventral part of
the cerebral hemispheres, located at the level of the optic
fenestra between the frontal and the parietal, is bordered
by only the dural membrane (Figure 4c,d). In Xerotyphlops,
Blanus, and Leposternon, the parietal surrounds only the
dorsal and lateral margins of the cerebral hemispheres
(Figure 4a,b,e). In Xerotyphlops (Figure 4e), the ventral mar-
gin of the cerebral hemispheres is encompassed by both the
postero-ventral process of the frontal (anteriorly) and the
parabasisphenoid (posteriorly), whereas in amphisbaenians
(Figure 4a,b), the structure is bordered ventrally by the orbi-
tosphenoid/tabulosphenoid. The cerebral hemispheres in
non-amphisbaenian “lizards” extend between the lateral
cranial crests of the parietal (i.e., crista cranii parietalis,
Evans, 2008), and in contrast to snakes and amphisbae-
nians, the osseous elements surrounding the structure are
limited (Figure 5), both the lateral and ventral margins of
the structure being only delineated by the dural envelope.
The dural membrane is supported by several parts of the
orbitotemporal chondrocranium including the postero-
ventral part of the planum supraseptale, the taenia medialis
(“tm” in Figure 5c), the taenia marginalis (“tma” in
Figure 5c), and the pila accessoria (“pacc” in Figure 5c).
In some of these taxa, the orbitosphenoid may border
the antero-ventral corner of the cerebral hemispheres
(e.g., “os” in Lepidothyris, Figure 5a).
The anterior limit of the cerebral hemispheres in
squamates, which corresponds to the anterior olfactory
nucleus (Armstrong et al., 1953; Halpern, 1980; Smeets
et al., 1986), is undiscernible from the external morphol-
ogy of the brain. Although a distinct, shallow transversal
groove is visible on the dorsal surface of the brain in
Blanus (Figure 2a), Leposternon, Xerotyphlops, as well as
Melanoseps (Figure 3a,c,g), this feature marks the transi-
tion between the dorsomedial cortex and the dorsal cor-
tex (ten Donkelaar, 1998) and cannot be used to delimit
the cerebral hemispheres anteriorly. According to Arm-
strong et al. (1953), Halpern (1980), and Smeets et al.
(1986), the rostral end of the cerebral hemispheres coin-
cides with the lateral and dorsal expansion of the brain
margins in squamates. Based on the observations made
here, such expansion of brain tissues is the only criterion
allowing a possible delimitation of the anterior cerebral
hemispheres. In snakes, as well as in Sphaerodactylus,
the artificial limit is located at the level of the fronto-
parietal suture (Figures 4c–e, and 5d). However, such a
correlation is not consistent across squamates, and the fronto-
parietal suture can be located more anteriorly (e.g., Blanus,
Figure 4a) or more posteriorly (e.g., Lepidothyris, Figure 5a)
than the possible anterior end of the cerebral hemispheres.
Similar to the brain, the artificial anterior limit of the
cerebral hemisphere cast remains difficult to locate and is
only indicated by changes in the width of the endocast.
In dorsal view, the posterior limit of the cerebral
hemispheres in squamates is easily discernable from the
external morphology of the brain (Figures 2 and 3). In all
species, the dorso-median point at which the paired cere-
bral hemispheres diverge is more anteriorly located than
the lateral ends of the hemispheres. In both Thamnophis
and Epicrates, the postero-lateral end of the cerebral
hemispheres correlates with the medial parietal pillars
(Scanferla, 2022; Zaher & Scanferla, 2012), whereas the
posterior dorso-median end of the structure displays
no specific relationships with the surrounding bones.
In Xerotyphlops, the postero-lateral end of the cerebral
hemispheres coincides with the ventral sutural crest
between the posterior parietal and the supraoccipital
(Figure 4e). Similar to the condition in Thamnophis
and Epicrates, the posterior dorso-median extent of the
cerebral hemispheres in Xerotyphlops shows no corre-
spondences with the surrounding bones; however, the
limit in Xerotyphlops sits in the same coronal plane as the
anterior-most extent of the anterior semicircular canal
(Figure 6a) but not in Thamnophis (Figure 6b) and Epicrates
(Figure 6c). In contrast to the configuration in snakes, the
posterior dorsal extent of the cerebral hemispheres in
“lizards” (including amphisbaenians) does not correlate
with specific osseous elements (Figures 4a,b and 5).
Although similar relationships between the anterior semi-
circular canal and the posterior dorso-median (Blanus,
Figure 6d) or the postero-lateral (Melanoseps, Figure 6f;
Tropidurus, Figure 6h; Sphaerodactylus, Figure 6i) extent
of the cerebral hemispheres can be established, such corre-
lations are not consistent (Leposternon [Figure 6e], Pseudo-
pus [Figure 6g], and Lepidothyris [Figure 6j] in which the
anterior semicircular canal is notably posterior to the cere-
bral hemispheres). Squamate endocasts provide variable
information to delimit the posterior extent of the cast of
the cerebral hemispheres. Both the posterior dorso-median

F I G U R E 2 Virtual reconstructions of the brain (left) and endocast (right) in dorsal (a, b, e, f, i, and j) and lateral (c, d, g, h, k, and l)
views of Blanus cinereus (a–d), Thamnophis sirtalis (e–h), and Pseudopus apodus (i–l). Scale bars equal 2 mm. cb, cerebellum; cer, cerebral
hemispheres; dienc., ventral diencephalon; hyp, hypothalamus; inter.f, interhemispheric fissure; lab, impressions left by the endosseous
labyrinth on the endocast; olf, olfactory bulbs and peduncles; op, optic lobes; pa.eye, parietal eye; pi, pineal complex; pit, pituitary; mf,
mesencephalic flexure; mo, medulla oblongata; tg, tegmentum; ts, torus semicircularis; 1. Transversal groove marking the transition between
the dorsomedial cortex and the dorsal cortex; CN III, oculomotor cranial nerve; CN IV, trochlear cranial nerve
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ALLEMAND ET AL. 9

F I G U R E 3 Virtual reconstructions of the brain (in red) and endocast (in blue) in dorsal (left) and lateral (right) views. Scale bars equal
2 mm. Leposternon scutigerum (a, b), Xerotyphlops vermicularis (b, d), Epicrates cenchria (e, f), Melanoseps loveridgei (g, h), Lepidothyris
fernandi (i, j), Sphaerodactylus caicosensis (k, l), and Tropidurus torquatus (m, n)
 19328494, 0, Downloaded from https://anatomypubs.onlinelibrary.wiley.com/doi/10.1002/ar.25142 by Daniel Fernandes - CAPES , Wiley Online Library on [31/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
10 ALLEMAND ET AL.

F I G U R E 4 Three-dimensional renderings showing the spatial relationships between the brain and skull bones in amphisbaenians and
snakes. Scale bars equal 2 mm. Blanus cinereus (a), Leposternon scutigerum (b), Thamnophis sirtalis (c), Epicrates cenchria (d), and
Xerotyphlops vermicularis (e) in dorsal and lateral views. bo, basioccipital; fr, frontal; os, orbitosphenoid/tabulosphenoid; oto.c, otooccipital
complex; pa, parietal; pbs, para-basisphenoid; so, supraoccipital

and lateral limits of the cast of the cerebral hemispheres
can be delineated directly from the endocast in Thamno-
phis (Figure 2f), Epicrates (Figure 3e), and Tropidurus
(Figure 3m). This differs from Xerotyphlops (Figure 3c), in
which only the postero-lateral extent of the cast of the
cerebral hemispheres can be delimited from the endocast,
as well as from other squamates in which the endocast
provides no clear features to posteriorly delimit the struc-
ture (e.g., Pseudopus, Figure 2j).
The extent to which the cast of the cerebral hemi-
spheres in squamates reflects the morphology of the cor-
responding brain structure differs markedly across
species (Figures 2 and 3). The interhemispheric fissure,
running between the paired cerebral hemispheres on the
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ALLEMAND ET AL. 11

F I G U R E 5 Three-dimensional renderings showing the spatial relationships between the brain and skull bones in non-amphisbaenian
“lizards.” Scale bars equal 2 mm. Lepidothyris fernandi (a), Melanoseps loveridgei (b), Pseudopus apodus (c), Sphaerodactylus caicosensis (d),
and Tropidurus torquatus (e) in dorsal and lateral views. bo, basioccipital; cp, cultriform process; fr, frontal; os, orbitosphenoid; oto.c,
otooccipital complex; pa, parietal; pacc, pila accessoria; pa.f, parietal foramen; pbs, para-basisphenoid; ps, planum supraseptale; so,
supraoccipital; tc, trabecula communis; tm, taenia medialis; tma, taenia marginalis; ts, tectum synoticum

brain (“inter.f” in Figure 2), may be located based on
a groove on the dorsal surface of the endocast in most
species (e.g., Thamnophis, Figure 2f). In Pseudopus
(Figure 2j) and Melanoseps (Figure 3g) such a groove is
poorly defined, and the dorsal surface of the cast of the
cerebral hemispheres is flat. The cast of the cerebral
hemispheres in both Thamnophis (Figure 2f,h) and
Epicrates (Figure 3e,f), similar to the brain, consists of a
wide and bulbous structure projecting both laterally and
dorso-ventrally, being nearly round in lateral view, and
well-delimited from the rest of the endocast. However,
comparisons between the cerebral hemispheres and the

12
F I G U R E 6 Three-dimensional renderings showing the spatial relationships between the brain (in red) and endosseous labyrinth
(in yellow) of Xerotyphlops vermicularis (a), Thamnophis sirtalis (b), Epicrates cenchria (c), Blanus cinereus (d), Leposternon scutigerum (e),
Melanoseps loveridgei (f), Pseudopus apodus (g), Tropidurus torquatus (h), Sphaerodactylus caicosensis (i), and Lepidothyris fernandi (g) in
dorsal view. Scale bars equal 2 mm
corresponding cast in Thamnophis show that the most
lateral point of the cast is more anteriorly located than it
is actually found to be on the brain (Figure 7d). In Blanus
(Figure 2a–d), as well as Leposternon, Xerotyphlops, and
Melanoseps (Figure 3a–d,g,h), the cast of the cerebral
hemispheres also reflects the morphology of the corre-
sponding brain structure. It exhibits an ovoid and tubular
form, distinct from the rest of the endocast, and projected
only along the horizontal axis. The cast of the cerebral
hemispheres in Pseudopus (Figure 2i–l), Lepidothyris,
Sphaerodactylus, and Tropidurus (Figure 3i–n) is poorly
differentiated from the neighboring regions. In only Tro-
pidurus, the ventral margin of the cerebral hemisphere
cast is indicated in lateral view by slight depressions on
the lateral surface of the endocast (Figure 3n). In this spe-
cies, the cast exhibits, similar to the brain structure, a
nearly pyriform to oval shape in lateral view, the poste-
rior part of the structure being more developed dorsoven-
trally than the anterior one. In Lepidothyris, Pseudopus,
and Sphaerodactylus such indications about the ventral
margin of the structure are absent, challenging an accu-
rate delimitation of the cerebral hemispheres from the
endocast only.
3.2 | Diencephalon
The squamate diencephalon consists of the epithalamus
(including the pineal complex [i.e., pineal and parapineal
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ALLEMAND ET AL.
organs] and the habenula, Smith et al., 2018), thalamus,
hypothalamus, and the posterior lobe of the pituitary
gland (i.e., neurohypophysis, ten Donkelaar, 1998). Nei-
ther the habenula nor the thalamus are visible from the
external morphology of squamate brains.
Postero-medial to the cerebral hemispheres, the pineal
complex was reconstructed in only Pseudopus (“pi” in
Figure 2i), Sphaerodactylus and Tropidurus (Figure 3k,m).
The brain structure is located ventral to the parietal, leav-
ing no imprints on the surface of the bone, and posterior
to the median aperture of the parietal (i.e., parietal or
pineal foramen, Smith et al., 2018). Such a parietal fora-
men (“pa.f” in Figure 5c) is occupied by the parietal eye, a
structure considered as homologous with the parapineal
organ in lepidosaurs (Smith et al., 2018). Squamate
endocasts generally offer no indications about the pineal
and parapineal organs (sensu Smith et al., 2018). In both
Pseudopus (Figure 2j) and Lepidothyris (Figure 3i), the
dorsal surface of the endocast bears a small bulge that
coincides with the median aperture of the parietal
(i.e., parietal or pineal foramen) and, thus, represents the
cast of the parietal eye (“pa.eye” in Figure 2j; sensu Smith
et al., 2018). It is worth noting that, despite the presence of
a parietal foramen, the cast of the parietal eye is not
discernable from the dorsal surface of the endocast in
Melanoseps (Figure 3g) and Tropidurus (Figure 3m).
Postero-ventral to the hypothalamus (“hyp” in
Figure 2g), the whole pituitary gland (including the ante-
rior lobe, i.e., adenohypophysis, ten Donkelaar, 1998) is
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13

blue) for each squamate of the study. ch, optic chiasm; en.s, endolymphatic sacs; occ.s, occipital sinus; ts + tp, tectum synoticum and tectum
F I G U R E 7 Three-dimensional renderings showing the spatial relationships between the brain (in red) and the endocast (transparent

posterius. Scale bars equal 2 mm

ALLEMAND ET AL.

14
distinct from the rest of the diencephalon in only Tham-
nophis (“pit” in Figure 2g), Lepidothyris and Tropidurus
(Figure 3j,n). Despite such exceptions, the two structures
remain generally difficult to delineate from the external
morphology of the squamate brain, and the whole region
is here reported as the ventral diencephalon in most spec-
imens (“dienc” in Figure 2c,k). According to ten Donke-
laar (1998), the ventral diencephalic brain in squamates
extends postero-ventral to the cerebral hemispheres and
the basal telencephalon, posterior to the optic chiasm,
and ends at the level of the mesencephalic flexure, just
anterior to the exit for the oculomotor (III) cranial nerve.
The diencephalon in snakes, amphisbaenians and Mela-
noseps is bordered ventrally by the parabasisphenoid
(Figures 4 and 5b), and is located within the concavity
made by the sella turcica, as well as in the pituitary fossa.
In contrast, the diencephalon in Tropidurus, Pseudopus,
Lepidothyris, and Sphaerodactylus lies dorsal to the cultri-
form process of the parabasisphenoid (“cp” in Figure 5a)
and only the postero-ventral part of the brain region is
situated within the sella turcica and pituitary fossa. In
these taxa, the lateral margin of the ventral diencephalic
brain is only delimited by the dural envelope supported
by the trabecula communis of the orbitotemporal chon-
drocranium (e.g., Pseudpus, “tc” in Figure 5c).
The cast that contains the ventral diencephalon in squa-
mates also comprises non-diencephalic structures such as
the optic tracts and the optic chiasm (e.g., Tropidurus, “ch”
in Figure 7h), which therefore could not be differentiated
in the endocast. The cast of the ventral diencephalon in
Blanus (Figure 2d), Leposternon, Xerotyphlops, and Melano-
seps (Figure 3b,d,h), forms only a small bulge on the ventral
surface of the endocast in lateral view, and as such is a poor
reflection of the morphology of the corresponding brain
structure. In other species, the whole structure exhibits,
similar to the brain, various ventral projections depending
on the taxon observed (e.g., Sphaerodactylus, Figure 3l;
Tropidurus, Figure 3n); however, the diencephalic cast
offers no basis upon which to delineate the diencephalon
from the pituitary gland.
3.3 | Mesencephalon
The external morphology of the mesencephalic brain con-
sists, from dorsal to ventral, of the optic tectum, the torus
semicircularis and the tegmentum (ten Donkelaar, 1998).
The optic tectum constitutes the largest part of the mes-
encephalon, whereas the torus semicircularis remains
here undiscernible from the external morphology of
the brain. Its anterior margin may be situated between
the postero-dorsal part of the cerebral hemispheres
(e.g., Blanus, “op” in Figure 2a) or be completely
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ALLEMAND ET AL.
posterior to it (e.g., Thamnophis, Figure 2e). In both
Lepidothyris and Tropidurus (Figure 3j,n), the optic
tectum is postero-ventral to the cerebral hemispheres and
the whole mesencephalic brain is tilted antero-ventrally/
postero-dorsally. In contrast, the optic tectum in other taxa
is on the same axis as the cerebral hemispheres and shows
a more vertical orientation (e.g., Pseudopus, Figure 2k).
Ventral to the optic tectum, the tegmentum reaches
the mesencephalic flexure (e.g., Thamnophis, “tg” in
Figure 2g), just posterior to the diencephalon, at the level
of the exit for the oculomotor (CN III) cranial nerve. In all
species, the limit between the tegmentum and the optic
tectum is not distinguishable from the external surface of
the brain. According to ten Donkelaar (1998), the bound-
aries of the ventral mesencephalon with both the dien-
cephalon and the rhombencephalon can be approximately
delineated by two lines running, respectively, from the
antero-ventral corner of the optic tectum to the anterior
mesencephalic flexure, and from the antero-ventral corner
of the cerebellum, at the level of the exit for the trochlear
(IV) nerve, to the posterior mesencephalic flexure.
The mesencephalic brain in snakes and non-
amphisbaenian “lizards” lies ventral to the posterior
parietal (Figures 4 and 5), whereas in amphisbaenians
the posterior part of the brain region is also covered by
the otic-occipital complex (e.g., Leposternon, Figure 4b),
formed by the fusion of the prootic, supraoccipital, otooc-
cipitals, basioccipital, and parabasisphenoid (Maisano
et al., 2006). The mesencephalon in snakes is surrounded
anteriorly by the posterior parietal downgrowths, and pos-
teriorly by the prootic (Thamnophis and Epicrates), with a
contribution from the supraoccipital lateral process on its
posterior end (Xerotyphlops, Figure 4e). In contrast to the
morphology observed in snakes, the parietal does not
delimit the lateral margin of the amphisbaenian mesen-
cephalon (Figure 4a,b). In both Blanus and Leposternon,
the brain region is delineated laterally by only the otic-
occipital complex (Figure 4a,b). In non-amphisbaenian
“lizards,” the lateral margin of the mesencephalon is not
fully ossified and consists of a variable mix between
the dural membrane supported by the taenia marginalis of
the orbitotemporal chondrocranium (e.g., Pseudopus,
Figure 5c), and both the dorsal and ventral anterior pro-
cesses of the prootic at the level of the incisura prootica.
The optic tectum in squamates forms a distinct struc-
ture on the dorsal surface of the brain (“op” in Figure 2).
Although this brain region shows no correspondences
with the surrounding bones in all species, its anterior limit
is aligned with the anterior-most extent of the anterior
semicircular canal in Xerotyphlops, Blanus, Melanoseps,
and Sphaerodactylus (Figure 6a,d,f,i). In contrast, the ante-
rior limit of the optic tectum in other squamates shows no
specific spatial relationships with the endosseous labyrinth

ALLEMAND ET AL.
and the anterior semicircular canal is far posterior of this
point (Thamnophis, Epicrates, Leposternon, Pseudopus,
Tropidurus, Lepidothyris, Figure 6b,c,e,g,h,j). The posterior
limit of the optic tectum in squamates displays no
consistent spatial relationships. The limit may variably
align with the postero-median end of the parietal
(e.g., Xerotyphlops, Figure 4e; Lepidothyris, Melanoseps,
Pseudopus, and Tropidurus, Figure 5a,b,c,e), the anterior-
most extent of the lateral downgrowths of the supraoccipi-
tal (e.g., Thamnophis, Figure 4c, Epicrates, Figure 4d), or
with the common crus of the endosseous labyrinth in
amphisbaenians (Figure 6d,e). Although the trochlear
nerve was only reconstructed here for Thamnophis
(Figure 2g), the boundaries of the ventral mesencephalon
with both the diencephalon and the rhombencephalon
can be approximately delineated in all taxa and show no
specific spatial relationships with the surrounding bones
or other cranial structures. Finally, the mesencephalic
flexure in Thamnophis coincides with the dorsum
sellae on the parabasisphenoid; however, such a corre-
lation was not observed in other species and the
flexure may occur more anteriorly (e.g., Epicrates) or
posteriorly (e.g., Sphaerodactylus) than the dorsum sellae.
Similar to the brain, squamate endocasts provide no
indication about the torus semicircularis and the limit
between the optic tectum and the tegmentum. Thus,
endocasts generally offer only an indication of the loca-
tion of the optic tectum and variable degrees of resolu-
tions regarding its morphology. The dorsal surface of the
optic tectum cast in Thamnophis forms, similar to the
corresponding brain structure, a pair of domes separated
by a median sulcus (Figure 2e–h). Anteriorly, the dorsal
surface of the structure is delimited by a slight groove just
posterior to the cast of the cerebral hemispheres. Posteri-
orly, the dorsal margin of the optic tectum cast follows
the sutural crest on the ventral surface of the parietal. In
contrast to Thamnophis, the cast of the optic tectum in
Blanus (Figure 2a–d), Leposternon, and Xerotyphlops
(Figure 3a–d), is not distinguishable and cannot be
delimited from the rest of the endocast. In Pseudopus
(Figure 2i–l), Epicrates, Melanoseps, Lepidothyris, Sphaer-
odactylus, and Tropidurus (Figure 3e–n), the cast of the
optic tectum exhibits only a smooth and flattened dorsal
surface that weakly reflects the corresponding brain
structure. In both Epicrates (Figure 3e) and Tropidurus
(Figure 3m), the anterior-most extent of the optic tectum
cast is weakly marked on the dorsal surface of the endo-
cast, whereas the posterior end is not visible. The cast of
the optic tectum in Pseudopus (Figure 2j,l), Melanoseps,
Lepidothyris, and Sphaerodactylus (Figure 3g–l), forms a
bulge on the lateral margin of the endocast, and can
mainly be located by a marked change in width, relative
to the cerebral hemispheres. It is worth noting that the
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15
optic tectum cast in Melanoseps offers a poor reflect of
both the dorso-ventral position and the lateral extent of
the cerebral optic tectum (Figure 7m,n). The well differ-
entiated casts of both the optic tectum and the mesence-
phalic flexure in Thamnophis (Figure 2h) may help to
delimit approximately the cast of the ventral mesenceph-
alon. In contrast, although the mesencephalic flexure is
also distinguishable in Pseudopus (Figure 2l), Epicrates,
Melanoseps, Lepidothyris, Sphaerodactylus, and Tropi-
durus (Figure 3f,h,j,l,n), the accurate delineation of the
ventral mesencephalic cast in these species is not possi-
ble, as the exact delineation of the cast of the optic tec-
tum remains indistinguishable. Similarly, the cast of the
mesencephalic flexure in Blanus (Figure 2d), Leposternon
and Xerotyphlops (Figure 3b,d) forms only a slight con-
cavity on the ventral surface of the endocast, challenging
the identification of the ventral mesencephalic cast.
3.4 | Rhombencephalon
Posterior to the mesencephalon, the rhombencephalon
forms the posterior-most region of the squamate brain
and includes the cerebellum, the isthmus and the
medulla oblongata (ten Donkelaar, 1998). The cerebel-
lum (“cb” in Figure 2) corresponds to the antero-dorsal
part of the rhombencephalic brain. In squamates, this
brain region lies in the depression formed by the mesen-
cephalon anteriorly, and the swelling of the medulla
oblongata posteriorly. Ventral to the cerebellum, the limit
between the isthmus and medulla oblongata (“mo” in
Figure 2) cannot be distinguished from the external
surface of squamate brains. Similarly, the limit between
the medulla oblongata and the spinal cord cannot be
delimited as the transition between the two structures is
gradual and not differentiated on brain external morphol-
ogies (ten Donkelaar, 1998).
Cerebellum. The cerebellum morphology in squa-
mates varies extensively among species and this structure
is differently oriented between snakes and “lizards”
(e.g., Macrì et al., 2019). In snakes and amphisbaenians,
the cerebellum is posteriorly tilted. It forms in Blanus
(Figure 2c), Leposternon and Xerotyphlops (Figure 3b,d) a
small sheet-shaped structure, hidden ventral to the poste-
rior part of the optic tectum. In both Thamnophis
(Figure 2e,g) and Epicrates (Figure 3e,f), the brain region
is better developed posteriorly and extends over the
fourth ventricle. The cerebellum consists of a simple
lamella in Thamnophis (Figure 2g), whereas in Epicrates
it shows a more triangular shape in lateral view
(Figure 3f), the anterior margin being projected postero-
dorsally and then bending postero-ventrally toward its
posterior end. In contrast, the cerebellum in non-

16
amphisbaenian “lizards” displays an everted morphology
and is tilted anteriorly (e.g., Pseudopus, Figure 2i,k). In both
Melanoseps (Figure 3g,h) and Tropidurus (Figure 3m,n), the
structure forms a plate standing nearly vertically from
the antero-posterior axis, both the anterior and posterior
margins extending dorsally. While the whole cerebellum
remains posterior to the optic tectum in Melanoseps
(Figure 3h), it extends anteriorly over the optic tecta
in Tropidurus (Figure 3n). In Pseudopus (Figure 2k),
Lepidothyris and Sphaerodactylus (Figure 3j,l), the
everted cerebellum forms a concavo-convex plate, in
which the anterior margin projects dorsally whereas the
posterior margin extends postero-dorsally and then
bends anteriorly toward the optic tectum.
The relative position of the squamate cerebellum
within the braincase appears fairly consistent across spe-
cies. In Thamnophis (Figure 4c), Lepidothyris (Figure 5a)
and Melanoseps (Figure 5b), the cerebellum is roofed by
the supraoccipital along its entire anterior–posterior
length. Similarly, although the bones surrounding the
amphisbaenian cerebellum are fused to form the otic-
occipital complex, the structure extends ventral to the
processus ascendens, which corresponds to the anterior
extent of the supraoccipital (Figure 4a,b; Maisano
et al., 2006). In other species, only the posterior part of
the cerebellum is roofed by the supraoccipital and its
anterior part is either ventral to the posterior parietal
(e.g., Epicrates, Figure 4d) or to the ascending process of
the tectum synoticum (e.g., Pseudopus, “ts” in Figure 5c),
the latter being a part of the otic chondrocranium that
may form a broad cartilaginous bridge or a reduced
medial rod between the otic capsules. The only exception
to such organization is observed in Sphaerodactylus in
which the cerebellum is ventral to only the parietal
(Figure 5d), without any participation from the supraoc-
cipital. In all species, the lateral cerebellar margins are
mostly delineated by the ventral flanges of the supraocci-
pital (e.g., Thamnophis, Figure 4c; Pseudopus, Figure 5c),
as well as the internal surface of the prootic on the
antero-ventral corner of the structure.
According to Nieuwenhuys (1967), the anterior end of
the squamate cerebellum is located just posterior to the
exit for the trochlear nerve (CN IV), and its ventral limit
with the isthmus/medulla oblongata, is usually indicated
by the auricle (ten Donkelaar & Bangma, 1992). In the
current study the limits could not be accurately posi-
tioned from the external morphology of the squamate
brain and no consistent spatial relationships were deter-
mined with the surrounding bones. Posteriorly, the con-
striction that lies between the medial-most points of the
labyrinth may serve as a proxy to delimit the cerebellum
extent in most squamates (Figure 6). In dorsal view, the
posterior-most extent of the cerebellum may occur in the
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ALLEMAND ET AL.
same coronal plane as the middle of the crus commune
(e.g., Epicrates, Figure 6c), at the level where the medial
constriction reaches its maximum. Although the postero-
most extent of the cerebellum is somewhat aligned with
the crus commune in other species, the limit can be just
anterior (e.g., Tropidurus, Figure 6h) or posterior to that
structure (e.g., Pseudopus, Figure 6g). In only Melanoseps
(Figure 6f) and Sphaerodactylus (Figure 6i), the posterior
aspect of the cerebellum does not reach the common
crus. Dorsally, although the dorsal-most point of the
squamate cerebellum does not exceed the endosseous
labyrinth in most species, with the exception of Tropi-
durus, no particular spatial relationships were found with
the surrounding bones.
The cast of the cerebellum is only discernable in
Tropidurus and the dorsal-most part of the everted cere-
bellum forms a peak on the dorsal surface of the endo-
cast, postero-dorsal to the cast of the optic tectum
(Figure 3n). Despite such a useful landmark to locate the
cerebellum in Tropidurus, the accurate delineation of the
brain region remains difficult from the endocast. In other
squamates, the endocast provides no information about
the position and morphology of the cerebellum, and that
brain region is hidden between the two large and round
impressions made by the endosseous labyrinth on the
lateral surface of the rhombencephalic cast (“lab” in
Figure 2). Such a lack of evidence is related to the dorso-
ventral extent of the cerebellum itself. Indeed, despite
showing variable morphologies, the cerebellum in taxa
studied here (except Tropidurus) displays a limited dorso-
ventral extent, compared to the optic tectum, and does
not reach the endocranial surface. This contrasts with
Tropidurus, in which the cerebellum is extended dorso-
ventrally and covers the postero-dorsal surface of the
optic tectum (Figure 3n). Additionally, the distance
between the squamate cerebellum and the endocranial
surface is lengthened by the inclusion of non-neural com-
ponents within the reconstructed endocast (Figure 7). As
these components could not be reconstructed accurately
and in all species here, their identification remains chal-
lenging. In Epicrates, two different structures were par-
tially reconstructed and interpreted as the occipital sinus
(“occ.s” in Figure 7a; Witmer et al., 2008) and the
remains of the endolymphatic sacs (“en.s” in Figure 7b;
Al Mohammadi et al., 2020). In both Blanus (Figure 7l)
and Lepidothyris (Figure 7s,t), the reconstructed compo-
nent here may correspond to the occipital sinus, as the
structure show no connection with the endolymphatic
foramen. The presence/absence of endolymphatic sacs in
these taxa is unknown. Finally, in Sphaerodactylus, the
cartilaginous bridge spanning between the dorsal por-
tions of the otic capsules consists potentially of both the
tectum synoticum and tectum posterius (“ts + tp” in

ALLEMAND ET AL.
Figure 7r; Khannoon & Evans, 2020). It is worth noting
that the presence/absence of both the occipital sinus and
endolymphatic sacs in this taxon remains unclear.
Medulla oblongata. The medulla oblongata forms a ven-
trally convex, wide arc and exhibits a pronounced pontine
flexure as it extends dorsally to connect with the spinal
cord at the level of the foramen magnum (Figures 2 and 3).
The relative position of this brain region within the poste-
rior braincase is somewhat consistent across squamates
(Figures 4 and 5). In all species, the structure is bordered
ventrally by the posterior part of the parabasisphenoid, pos-
terior to the dorsum sellae, and the basioccipital. In snakes,
its postero-ventral end is also bounded by the otooccipital
forming the lateral component of the occipital condyle. In
all squamates, both the medial surface of the prootic and
the otooccipital outline the lateral margin of the medulla
oblongata, and the posterior part of the supraoccipital roofs
its posterior extent. Additionally, the otooccipital in snakes
delimits the postero-dorsal part of the medulla oblongata,
whereas in non-amphisbaenian “lizards,” this portion is
only limited by the dural membrane.
The cast of the medulla oblongata in squamates is, simi-
lar to the corresponding brain structure, narrower than the
cast of the cerebral hemispheres (Figures 2 and 3). Due to
the round impressions left by the endosseous labyrinth on
the lateral surface of the endocast, both its anterior and
dorsal margins cannot be accurately delimited. The ventral
projection of the medulla oblongata in some species may
show a weak correspondence between the endocast and
the brain. In Blanus (Figure 2c,d) and Sphaerodactylus
(Figure 3l), the cast of the ventral rhombencephalon corre-
sponds to the most ventral surface of the endocast in
lateral view, whereas the corresponding brain structure is
less projected ventrally and remains dorsal to the most
ventral extent of the diencephalon.
4 | DISCUSSION
4.1 | Brain-Skull spatial relationships
in Squamata
Our results show that the spatial relationships between
the brain, each of its regions, and the squamate skull,
reveal some similarities in the relative position of these
structures. Correspondences between the skull roof and
the dorsal surface of the brain show that the frontal is
mainly associated with the olfactory bulbs and peduncles,
whereas the parietal generally coincides with the cerebral
hemispheres and the optic lobes. The fronto-parietal
suture in snakes is aligned with the artificial anterior
limit of the cerebral hemispheres but not in “lizards.”
Additional correlations can be observed between bones
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17
composing the squamate braincase and both the ventral
and posterior parts of the brain. The parabasisphenoid in
snakes, amphisbaenians and the “lizard” Melanoseps is
associated with the ventral diencephalic brain, whereas
in other “lizards,” the bone is located more posteriorly
than the brain region. Posteriorly, the supraoccipital in
squamates is generally aligned with the cerebellum,
whereas the prootic, otoocipital and basioccipital relate
to the isthmus/medulla oblongata. Finally, the squamate
endosseous labyrinth may provide additional clues about
the limit between the cerebral hemispheres and the optic
lobes, and the extent of the cerebellum. It is worth noting
that exceptions to this global pattern exist, which
prevents any generalization for the whole clade.
As squamate endocasts display variable degrees of neu-
roanatomical resolution, the location and delimitation of
at least some of the different brain regions can be chal-
lenging. The spatial relationships reported here between
the brain regions, the cranial bones, and the endosseous
labyrinth, may help to position the cerebral components
on squamate endocasts. However, as one-to-one corre-
spondences between a bone and a specific brain region
appear limited and highly variable across squamates, such
spatial relationships remain insufficient to delineate accu-
rately weakly-delimited endocast components such as the
diencephalon, mesencephalon and rhombencephalon. In
order to better understand interactions between the brain
and the skull in squamates, future studies should test
how these spatial relationships may change as a function
of taxonomic or ecologic (e.g., habitat) factors, and if
any pattern can be detected across this variability.
In addition, brain-to-bone relationships should be
considered under an ontogenetic perspective in order to
highlight the dynamic networks responsible for such
correspondences. Fabbri et al. (2017) reported a close
alignment of the prosencephalon (i.e., telencephalon
and diencephalon)–mesencephalon boundary and the
fronto-parietal suture in the developmental series of
the lizard Chalcides chalcides. Such a pattern is not
universally found among the different adult specimens
studied here, the fronto-parietal suture occurring anterior
to the limit between the prosencephalon and the mesen-
cephalon. Although this suggests a shift in the correspon-
dence between the divisions of the brain and the skull
during squamate ontogeny, that remains to be tested.
4.2 | Neuroanatomical resolutions
of squamate endocasts
Qualitative comparisons performed here show that the
neuroanatomical resolution of squamate endocasts, and
the accuracy to which they may reflect the corresponding

18
brain, differs across species and does not follow clear
phylogenetic trends. Indeed, weakly-delimited endocast
components variably occur in “lizards” and snakes,
whereas well-regionalized endocasts can be found in both
groups. It is worth noting that levels of resolution in
squamate endocasts do not depend only on the degree to
which the brain fills the endocranial cavity. Thus, squa-
mates in which the brain occupies a large part of the
endocranial cavity can show a weakly-resolved endocast
(e.g., Leposternon). In contrast, endocast components
can be easier to distinguish in taxa exhibiting a weaker
correspondence between the brain and the endocast
(e.g., Sphaerodactylus).
Our results indicate that the neuroanatomical resolu-
tion of squamate endocasts also differs according to brain
regions. Without considering their accurate delineation,
the olfactory bulbs and peduncles, cerebral hemispheres
and medulla oblongata represent generally the most eas-
ily discernable brain regions from squamate endocasts
and are visible in all species. In contrast, endocranial res-
olution of the optic tectum, ventral diencephalon and
pituitary appear more variable across squamates. Endo-
casts in the amphisbaenians Blanus and Leposternon, as
well as the scolecophidian snake Xerotyphlops, differ from
other squamates as they provide little indication about
these brain regions. Similar levels of resolution were
reported in other amphisbaenians (Amphisbaena gonaven-
sis, A. kingii, A. vanzolinii, Allemand, 2017), scolecophi-
dian snakes (Typhlophis squamosus, Rhinotyphlops
schlegelii, Allemand et al., 2017; Typhlops jamaicensis,
Scanferla, 2022), and alethinophidian snakes (Uropeltis
woodmasoni, Olori, 2010; U. pulneyensis, Allemand
et al., 2017; Teretrurus sanguineus, Scanferla, 2022). All
these taxa being fully fossorial (e.g., Herrel et al., 2021;
Kearney, 2003; Navas et al., 2004; Olori & Bell, 2012), this
suggests that weak endocranial resolutions for the optic
tectum, pituitary and ventral diencephalon are common in
burrowing squamates that spend prolonged periods of
time underground and are capable of penetrating sub-
strates of higher resistance (Scanferla, 2016). In contrast,
these brain regions are distinguishable from the endocast
reconstructed here for the cryptozoic lizard Melanoseps,
defined as such as it mostly uses the softer top compart-
ment of the soil for burrowing (Malonza & Bwong, 2011;
Scanferla, 2016), and similar levels of endocranial reso-
lution were observed in two cryptozoic alethinophidian
snakes, Anilius scytale and Atractaspis irregularis
(Allemand et al., 2017; Scanferla, 2022). This degree of
variability between fully burrower and cryptzoic taxa
suggests that the endocranial resolution reflects the vari-
able degrees of fossoriality found within the clade. This
finding is consistent with the identification of a specific
underground cerebrotype in fossorial snakes (Scanferla,
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ALLEMAND ET AL.
2022) and the observation of skeletal adaptations observed
within fossorial squamates (e.g., Ebel et al., 2020;
Roscito & Rodrigues, 2010). Despite such a straightforward
trend here, endocranial studies have so far mostly focused
on snakes and represent currently only a small part of the
diversity that evolved independently a fossorial lifestyle
(e.g., Ebel et al., 2020). By reconstructing endocasts in
other fossorial squamates, more particularly among line-
ages of non-amphisbaenian “lizards” such as dibamids,
gymnophthalmids, scincids and anniellids, future endocra-
nial studies will offer a broader context to discuss the rela-
tionships between endocast resolution and degree of
fossoriality.
Squamate endocasts reconstructed here provide gen-
erally no indication of the cerebellum, consistent with
the observations made from snake endocasts by Alle-
mand et al. (2017) and Scanferla (2022). Such a lack of
evidence results from both the morphology of the brain
region itself, as well as the presence of non-neural com-
ponents in this area. The only exception to such a trend
is observed here in Tropidurus, in which the large dorso-
ventral extent of the cerebellum enables the location of it
on the endocast. Our results support the inference that
the cerebellum in snakes and amphisbaenians cannot be
assessed from the endocast. In contrast, the picture is
more nuanced in non-amphisbaenian “lizards” as the
dorso-ventral extension of the cerebellum in these taxa is
more variable (e.g., Macrì et al., 2019). Future studies
are needed in non-amphisbaenian “lizards” showing an
extended cerebellum (e.g., Draco volans, Bradypodion
pumilum, Macrì et al., 2019) in order to determine whether
their endocasts offer similar level of resolution as Tropi-
durus in allowing the location of that brain region.
Additionally, the occipital sinus, endolymphatic sacs and
cartilaginous elements surrounding the cerebellum may
occupy variable portions of the area and, therefore, affect
the resolution of the endocast. As the position, shape and
size of these structures appear highly variable in squamates
(e.g., Bruner, 1907; Ineich et al., 2018; Lamb et al., 2017;
Mangione & Montero, 2001; Porter & Witmer, 2015), it is
likely that the impact of these non-neural components on
the endocast resolution is different, according to species,
and further studies are needed to test it.
4.3 | Squamate endocast as proxy for the
brain morphology
The validity of endocranial studies rests on the reliability
of endocasts as a proxy for brain morphology (Watanabe,
Gignac, et al., 2019). Qualitative comparisons performed
here indicate that certain aspects of brain morphologies
in squamates can be extrapolated from the endocast

ALLEMAND ET AL.
morphology. Nevertheless, such information differs
notably according to species and brain regions. It
would be interesting to investigate quantitatively the
degree to which squamate endocasts reflect true brain
morphologies in term of both size and shape. Endo-
casts naturally overestimate brain sizes due to the
intermediary space between the brain and the internal
surface of the skull that contains different non-neural
components. Volumetric measurements of brains and
endocasts have already shown that size differences
between them are highly variable in squamates,
depending on species (e.g., Kim & Evans, 2014; Perez-
Martinez & Leal, 2021). However, such measurements
remain limited to few species of squamates and addi-
tional volumetric analyses are needed to investigate
how brain–endocast correspondences in size vary
through the entire clade. Although testing brain–
endocast relationships in term of volume ratio were
beyond the objective of this study, our results indicate
that the brain in most squamates here, except Sphaero-
dactylus, fills a large portion of the endocranial space.
In these taxa, areas with greater physical distances
between the brain and endocranial surface are gener-
ally located in the region of the cerebellum. Despite
such a trend, spatial relationships between the brain
and the endocranial wall appear not to be uniform but
may vary between the different neuroanatomical
regions and according to species. By controlling the
degree of brain shrinkage induced by the preparation
of specimens, future studies are needed in order to
investigate quantitatively how brain regions may vari-
ably fill the endocranial space in squamates. In addi-
tion, although endocasts may be a good proxy for brain
volume in certain squamates, our results suggest that
shape divergences may also occur between the endo-
cast and corresponding brain. In Thamnophis, for instance,
the lateral-most extent of the cast of the cerebral
hemispheres is located more anteriorly than the true
lateral-most point of the brain region. This indicates that
areas with a close correspondence between the brain and
endocranial surface can potentially exhibit deviations in
shape; however, the typical degree and pattern of such
divergences remain to be tested. By employing landmark-
based geometric morphometric methods (e.g., Allemand
et al., in press; Watanabe, Gignac, et al., 2019), future
quantitative assessments of brain–endocast correspon-
dence in shape will help us to understand which brain
regions are accurately or poorly approximated by the cor-
responding areas on squamate endocasts. Such analyses
will have important implications for accurate and pre-
cise inferences of brain morphology from squamate
endocasts.
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19
5 | CONCLUSION
This study aimed to investigate the extent to which a
squamate endocast is reflecting the brain morphology.
By qualitatively comparing brains and endocasts of
different squamates, our results indicate that certain
aspect of brain morphology and its regions can be
extrapolated from endocasts. Squamate endocasts dis-
play variable neuroanatomical resolution according to
both species and brain regions. Thus, the olfactory
bulbs and peduncles, cerebral hemispheres and ventral
rhombencephalon are discernible from the endocast in
all squamates. In contrast, the optic tectum, ventral
diencephalon and pituitary exhibit variable levels of
resolution depending on species, these brain regions
being more difficult to observe in fossorial squamates.
Finally, due both to its morphology and to the inclu-
sion of non-neural components in the relevant area,
squamate endocasts provide poor indications about the
cerebellum. Future studies should evaluate if this
pattern of resolution holds for the whole clade of
Squamata. The spatial relationships reported in this
study between brain regions, cranial bones, and the
endosseous labyrinth, may help to position the brain
components on squamate endocasts. Although the
absence of one-to-one correspondences between a
bone and a specific brain region prevents consistent
accurate delineations, we hope our results will offer
guidelines to interpret the apparently feature-less
nature of certain squamate endocasts. Quantifying the
degree of reliability of endocranial regions to reflect
brain morphology in squamates will be critical for
accurate and precise inferences of brain morphology in
future (paleo) neuro-anatomical studies.
AUTHOR CONTRIBUTIONS
Rémi Allemand: Conceptualization; formal analysis;
investigation; methodology; writing – original draft.
Jade Abdul-Sater: Investigation; writing – review and
editing. Simone Macrì: Resources; writing – review
and editing. Nicolas Di-Poi: Resources; writing – review
and editing. Gheylen Daghfous: Resources; writing –
review and editing. Mary T. Silcox: Conceptualization;
funding acquisition; investigation; methodology; supervi-
sion; writing – review and editing.
ACKNOWLEDGMENTS
Thanks to David Blackburn on MorphoSource for grant-
ing access to the micro-diceCT scans of Sphaerodactylus
caicosensis. We would also like to thank two anonymous
reviewers for helpful comments and suggestions that
improved the paper.

20
ORCID
Rémi Allemand https://orcid.org/0000-0002-7912-7607
R EF E RE N C E S
Afsar, M., Çiçek, K., Tayhan, Y., & Tok, C. V. (2016). New records
of Eurasian blind Snake, Xerotyphlops vermicularis (Merrem,
1820) from the Black Sea region of Turkey and its updated dis-
tribution. Biharean Biologist, 10(2), 98–103.
Akani, G. C., Capizzi, D., & Luiselli, L. (2002). Community ecology
of scincid lizards in a swamp rainforest of South-Eastern
Nigeria. Russian Journal of Herpetology, 9, 125–134.
Al Mohammadi, A. G., Khannoon, E. R., & Evans, S. E. (2020). The
development of the osteocranium in the snake Psammophis
sibilans (Serpentes: Lamprophiidae). Journal of Anatomy,
236(1), 117–131.
Allemand, R. (2017). Etude microtomographique de l'endocrâne de
reptiles marins (Plesiosauria et Mosasauroidea) du Turonien
(Crétacé supérieur) du Maroc: Implications paléobiologiques
et comportementales [PhD dissertation, Muséum National d'His-
toire Naturelle, Paris, France], p. 285.
Allemand, R., Boistel, R., Daghfous, G., Blanchet, Z., Cornette, R.,
Bardet, N., Vincent, P., & Houssaye, A. (2017). Comparative
morphology of snake (Squamata) endocasts: Evidence of
phylogenetic and ecological signals. Journal of Anatomy,
231(6), 849–868. https://doi.org/10.1111/joa.12692
Allemand, R., L opez-Aguirre, C., Abdul-Sater, J., Khalid, W.,
Lang, M. M., Macrì, S., Di-Poï, N., Daghfous, G., & Silcox, M. T.
(in press). A landmarking protocol for geometric morphometric
analysis of squamate endocasts. The Anatomical Record.
Andrade-Junior, A., França, M. S., Sudré, V., & Passos, P. (2020). Are
there threatened snakes at the end of the rainbow? Notes on the
distribution and morphology of Epicrates cenchria, Rainbow
Boa, in the Brazilian Atlantic Forest. Cuadernos de Herpetología,
34(2), 299–304. https://doi.org/10.31017/CdH.2020.(2019-030)
Aristide, L., Strauss, A., Halenar-Price, L. B., Gilissen, E.,
Cruz, F. W., Cartelle, C., Rosenberger, A. L., Lopes, R. T., dos
Reis, S. F., & Perez, S. I. (2019). Cranial and endocranial diver-
sity in extant and fossil atelids (Platyrrhini: Atelidae): A geo-
metric morphometric study. American Journal of Physical
Anthropology, 169(2), 322–331. https://doi.org/10.1002/ajpa.
23837
Armstrong, J. A., Gamble, H. J., & Goldby, F. (1953). Observations
on the olfactory apparatus and the telencephalon of Anolis, a
microsmatic lizard. Journal of Anatomy, 87, 288–307.
Balanoff, A. M., & Bever, G. S. (2017). The role of endocasts in the
study of brain evolution. In J. H. Kaas & G. Striedter (Eds.),
Evolution of nervous systems (pp. 223–241). Academic Press.
Balanoff, A. M., Bever, G. S., Colbert, M. W., Clarke, J. A.,
Field, D. J., Gignac, P. M., Ksepka, D. T., Ridgely, R. C.,
Smith, N. A., Torres, C. R., Walsh, S., & Witmer, L. M. (2016).
Best practices for digitally constructing endocranial casts:
Examples from birds and their dinosaurian relatives. Journal of
Anatomy, 229(2), 173–190. https://doi.org/10.1111/joa.12378
Balanoff, A. M., Bever, G. S., Rowe, T. B., & Norell, M. A. (2013).
Evolutionary origins of the avian brain. Nature, 501, 93–96.
https://doi.org/10.1038/nature12424
Barros, F. C., Herrel, A., & Kohlsdorf, T. (2011). Head shape
evolution in Gymnophthalmidae: Does habitat use constrain
the evolution of cranial design in fossorial lizards? Journal of
19328494, 0, Downloaded from https://anatomypubs.onlinelibrary.wiley.com/doi/10.1002/ar.25142 by Daniel Fernandes - CAPES , Wiley Online Library on [31/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ALLEMAND ET AL.
Evolutionary Biology, 24(11), 2423–2433. https://doi.org/10.
1111/j.1420-9101.2011.02372.x
Bellairs, A. A., & Kamal, A. M. (1981). The chondrocranium and
the development of the skull in recent reptiles. In C. Gans &
T. S. Parsons (Eds.), Biology of the Reptilia. Vol. 11: Morphology
(pp. 1–263). Academic Press.
Benoit, J., Fernandez, V., Manger, P. R., & Rubidge, B. S. (2017).
Endocranial casts of pre-mammalian therapsids reveal an unex-
pected neurological diversity at the deep evolutionary root of
mammals. Brain, Behavior and Evolution, 90(4), 311–333.
https://doi.org/10.1159/000481525
Beyrand, V., Voeten, D. F., Bureš, S., Fernandez, V., Janaček, J.,
Jirak, D., Rauhut, O., & Tafforeau, P. (2019). Multiphase proge-
netic development shaped the brain of flying archosaurs. Scientific
Reports, 9(10807), 10807. https://doi.org/10.1038/s41598-019-
46959-2
Bjerring, H. C. (1991). Two intracranial ligaments supporting the
brain of the brachiopterygian fish Polypterus senegalus. Acta
Zoologica, 72(1), 41–47. https://doi.org/10.1111/j.1463-6395.
1991.tb00314.x
Boyer, D. M., Gunnell, G. F., Kaufman, S., & McGeary, T. M.
(2016). Morphosource: Archiving and sharing 3-D digital speci-
men data. The Paleontological Society Papers, 22, 157–181.
https://doi.org/10.1017/scs.2017.13
Bruner, H. (1907). On the cephalic veins and sinuses of reptiles,
with a description of a mechanism for raising the venous
blood-pressure in the head. American Journal of Anatomy, 7,
1–117.
Burger, J., Jeitner, C., Jensen, H., Fitzgerald, M., Carlucci, S.,
Shukla, S., Burke, S., Ramos, R., & Gochfeld, M. (2004). Habitat
use in basking northern water (Nerodia sipedon) and eastern
garter (Thamnophis sirtalis) snakes in urban New Jersey.
Urban Ecosystem, 7(1), 17–27.
Butler, A. B., & Hodos, W. (2005). Comparative vertebrate anatomy:
Evolution and adaptation (p. 744). John Wiley & Sons.
Buytaert, J., Goyens, J., De Greef, D., Aerts, P., & Dirckx, J. (2014).
Volume shrinkage of bone, brain and muscle tissue in sample
preparation for micro-CT and light sheet fluorescence micros-
copy (LSFM). Microscopy and Microanalysis, 20(4), 1208–1217.
https://doi.org/10.1017/S1431927614001329
Clement, A. M., Mensforth, C. L., Challands, T. J., Collin, S. P., &
Long, J. A. (2021). Brain reconstruction across the fish-tetrapod
transition; insights from modern amphibians. Frontiers in Ecology
and Evolution, 9, 160. https://doi.org/10.3389/fevo.2021.640345
Da Silva, F. O., Fabre, A. C., Savriama, Y., Ollonen, J., Mahlow, K.,
Herrel, A., Müller, J., & Di-Poï, N. (2018). The ecological ori-
gins of snakes as revealed by skull evolution. Nature Communi-
cations, 9(1), 1–11. https://doi.org/10.1038/s41467-017-02788-3
De Miguel, C., & Henneberg, M. (1998). Encephalization of the
koala, Phascolarctos cinereus. Australian Mammalogy, 20(3),
315–320. https://doi.org/10.1071/AM98315
Dozo, M. T., Paulina-Carabajal, A., Macrini, T. E., & Walsh, S.
(2022). Paleoneurology and brain evolution: New directions in
the study of fossil endocasts in reptiles, birds and mammals.
Springer.
Dumoncel, J., Subsol, G., Durrleman, S., Bertrand, A., de Jager, E.,
Oettlé, A. C., Lockhat, Z., Suleman, F. E., & Beaudet, A. (2020).
Are endocasts reliable proxies for brains? A 3D quantitative
comparison of the extant human brain and endocast. Journal of
Anatomy, 238(2), 480–488. https://doi.org/10.1111/joa.13318

ALLEMAND ET AL.
Early, C. M., Iwaniuk, A. N., Ridgely, R. C., & Witmer, L. M.
(2020). Endocast structures are reliable proxies for the sizes of
corresponding regions of the brain in extant birds. Journal of
Anatomy, 237(6), 1162–1176. https://doi.org/10.1111/joa.13285
Early, C. M., Ridgely, R. C., & Witmer, L. M. (2020). Beyond endo-
casts: Using predicted brain-structure volumes of extinct birds
to assess neuroanatomical and behavioral inferences. Diversity,
12(1), 34. https://doi.org/10.3390/d12010034
Ebel, R., Müller, J., Ramm, T., Hipsley, C., & Amson, E. (2020).
First evidence of convergent lifestyle signal in reptile skull roof
microanatomy. BMC Biology, 18, 185. https://doi.org/10.1186/
s12915-020-00908-y
Edinger, T. (1951). The brains of the Odontognathae. Evolution,
5(1), 6–24.
Evans, S. E. (2008). The skull of lizards and tuatara. In C. Gans,
A. S. Gaunt, & K. Adler (Eds.), Biology of the Reptilia, Vol. 20:
Morphology H, the skull of Lepidosauria (pp. 1–347). Society for
the Study of Amphibians and Reptiles.
Fabbri, M., Koch, N. M., Pritchard, A. C., Hanson, M., Hoffman, E.,
Bever, G. S., Amy, M., Balanoff, A. M., Morris, Z. S.,
Field, D. J., Camacho, J., Rowe, T. B., Norell, M. A.,
Smith, R. M., Abzhanov, A., & Bhullar, B.-A. S. (2017). The
skull roof tracks the brain during the evolution and develop-
ment of reptiles including birds. Nature Ecology & Evolution,
1(10), 1543–1550. https://doi.org/10.1038/s41559-017-0288-2
Falk, D. (2014). Interpreting sulci on hominin endocasts: Old
hypotheses and new findings. Frontiers in Human Neuroscience,
8, 134. https://doi.org/10.3389/fnhum.2014.00134
Gil, M. J., Guerrero, F., & Pérez-Mellado, V. (1993). Observations
on morphometrics and ecology in Blanus cinereus (Reptilia:
Amphisbaenia). Journal of Herpetology, 27(2), 205–209.
Giles, S., & Friedman, M. (2014). Virtual reconstruction of endocast
anatomy in early ray-finned fishes (Osteichthyes, Actinopterygii).
Journal of Paleontology, 88, 636–651. https://doi.org/10.1666/
13-094
Haight, J. R., & Nelson, J. E. (1987). A brain that doesn't fit its skull:
A comparative study of the brain and endocranium of the
koala, Phascolarctos cinereus (Marsupialia: Phascolarctidae). In
M. Archer (Ed.), Possums and Opossums (pp. 331–352). Royal
Zoological Society of New South Wales.
Halpern, M. (1980). The telencephalon of snakes. In S. O. E.
Ebbesson (Ed.), Comparative neurology of the telencephalon
(pp. 257–295). Springer.
Hedrick, B. P., Yohe, L., Vander Linden, A., Davalos, L. M., Sears, K.,
Sadier, A., Rossiter, S. J., Davies, K. T. J., & Dumont, E. (2018).
Assessing soft-tissue shrinkage estimates in museum specimens
imaged with diffusible iodine-based contrast-enhanced computed
tomography (diceCT). Microscopy and Microanalysis, 24(3), 284–
291. https://doi.org/10.1017/S1431927618000399
Herrel, A., Lowie, A., Miralles, A., Gaucher, P., Kley, N. J.,
Measey, J., & Tolley, K. A. (2021). Burrowing in blindsnakes: A
preliminary analysis of burrowing forces and consequences for
the evolution of morphology. The Anatomical Record, 304(10),
2292–2302.
Holloway, R. L. (1978). The relevance of endocasts for studying pri-
mate brain evolution. In C. R. Noback (Ed.), Sensory systems of
primates (pp. 181–200). Springer.
Holloway, R. L., Sherwood, C. C., Hof, P. R., & Rilling, J. K. (2009).
Evolution of the brain in humans–paleoneurology. In M. D.
19328494, 0, Downloaded from https://anatomypubs.onlinelibrary.wiley.com/doi/10.1002/ar.25142 by Daniel Fernandes - CAPES , Wiley Online Library on [31/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
21
Binder, N. Hirokawa, & U. Windhorst (Eds.), Encyclopedia of
neuroscience (pp. 1326–1334). Springer-Verlag.
Hopson, J. A. (1979). Paleoneurology. In C. Gans, R. G. Northcutt, &
P. Ulinski (Eds.), Biology of the Reptilia, Vol. 9: Neurology A
(pp. 39–146). Academic Press.
Ineich, I., Bissessur, P., Girard, F., & Probst, J. M. (2018). Les sacs
endolymphatiques hypertrophiés chez Phelsuma ornata Gray,
1825 à l'île Maurice (Mascareignes) et leurs liens avec l'insular-
ité. Bulletin de la Société Herpétologique de France, 168, 1–14.
Iwaniuk, A. N., Keirnan, A. R., Janetzki, H., Mardon, K.,
Murphy, S., Leseberg, N. P., & Weisbecker, V. (2020). The endo-
cast of the night parrot (Pezoporus occidentalis) reveals insights
into its sensory ecology and the evolution of nocturnality in
birds. Scientific Reports, 10, 9258. https://doi.org/10.1038/
s41598-020-65156-0
Iwaniuk, A. N., & Nelson, J. E. (2002). Can endocranial volume be
used as an estimate of brain size in birds? Canadian Journal of
Zoology, 80(1), 16–23. https://doi.org/10.1139/z01-204
Jerison, H. J. (1969). Brain evolution and dinosaur brains. The
American Naturalist, 103(934), 575–588.
Jerison, H. J. (1973). Evolution of the brain and intelligence (p. 496).
Academic Press.
Kearney, M. (2003). Systematics of the Amphisbaenia (Lepidosauria:
Squamata) based on morphological evidence from recent and
fossil forms. Herpetological Monographs, 17(1), 1–74. https://doi.
org/10.1655/0733-1347(2003)017[0001:SOTALB]2.0.CO;2
Khannoon, E. R., & Evans, S. E. (2020). Embryonic skull develop-
ment in the gecko, Tarentola annularis (Squamata: Gekkota:
Phyllodactylidae). Journal of Anatomy, 237(3), 504–519.
Kim, R., & Evans, D. (2014). Relationships among brain, endocra-
nial cavity, and body sizes in reptiles. Society of Vertebrate Pale-
ontology 74th annual meeting, Berlin, Germany, p. 159.
Lamb, A. D., Watkins-Colwell, G. J., Moore, J. A., Warren, D. L.,
Iglesias, T. L., Brandley, M. C., & Dornburg, A. (2017).
Endolymphatic sac use and reproductive activity in the Lesser
Antilles endemic gecko Gonatodes antillensis (Gekkota:
Sphaerodactylidae). Bulletin of the Peabody Museum of Natural
History, 58(1), 17–29. https://doi.org/10.3374/014.058.0103
Lautenschlager, S., Ferreira, G. S., & Werneburg, I. (2018). Sensory
evolution and ecology of early turtles revealed by digital endo-
cranial reconstructions. Frontiers in Ecology and Evolution, 6, 7.
https://doi.org/10.3389/fevo.2018.00007
Leonard, K. C., Worden, N., Boettcher, M. L., Dickinson, E., &
Hartstone-Rose, A. (2021). Effects of long-term ethanol storage
on muscle architecture. The Anatomical Record, 305, 184–198.
https://doi.org/10.1002/ar.24638
Lynch, L. M., & Allen, K. L. (2022). Relative brain volume of carni-
vorans has evolved in correlation with environmental and die-
tary variables differentially among clades. Brain, Behavior and
Evolution, 97, 284–297. https://doi.org/10.1159/000523787
Macrì, S., Savriama, Y., Khan, I., & Di-Poï, N. (2019). Comparative
analysis of squamate brains unveils multi-level variation in
cerebellar architecture associated with locomotor specializa-
tion. Nature Communications, 10(1), 1–16. https://doi.org/10.
1038/s41467-019-13405-w
Macrini, T. E., Rowe, T., & VandeBerg, J. L. (2007). Cranial endocasts
from a growth series of Monodelphis domestica (Didelphidae,
Marsupialia): A study of individual and ontogenetic variation.
Journal of Morphology, 268(10), 844–865.

22
Maisano, J. A., Kearney, M., & Rowe, T. (2006). Cranial anatomy of
the spade-headed amphisbaenian Diplometopon zarudnyi
(Squamata, Amphisbaenia) based on high-resolution X-ray
computed tomography. Journal of Morphology, 267(1), 70–102.
https://doi.org/10.1002/jmor.10388
Malonza, P. K., & Bwong, B. A. (2011). Life history notes on
loveridge's limbless skink Melanoseps loveridgei Brygoo &
Roux-Esteve, 1981 (Sauria: Scincidae: Feylininae). Herpetotropi-
cos, 5, 115–117.
Mangione, S., & Montero, R. (2001). The endolymphatic sacs in
embryos of Amphisbaena darwini. Journal of Herpetology,
35(3), 524–529.
McKeown, M., Brusatte, S. L., Williamson, T. E., Schwab, J. A.,
Carr, T. D., Butler, I. B., Muir, A., Schroeder, K., Espy, M. A.,
Hunter, J. F., Losko, A. S., Nelson, R. O., Gautier, D. C., &
Vogel, S. C. (2020). Neurosensory and sinus evolution as tyran-
nosauroid dinosaurs developed giant size: Insight from the
endocranial anatomy of Bistahieversor sealeyi. The Anatomical
Record, 303(4), 1043–1059. https://doi.org/10.1002/ar.24374
Morhardt, A. C. (2016). Gross anatomical brain region approxima-
tion (GABRA): Assessing brain size, structure, and evolution in
extinct archosaurs. [PhD Dissertation, Ohio University, Athens,
GA], p. 276.
Navas, C. A., Antoniazzi, M. M., Carvalho, J. E., Chaui-Berlink, J. G.,
James, R. S., Jared, C., Kohlsdorf, T., Dal Pai-Silva, M., &
Wilson, R. S. (2004). Morphological and physiological speciali-
zation for digging in amphisbaenians, an ancient lineage of
fossorial vertebrates. Journal of Experimental Biology, 207(14),
2433–2441.
Neubauer, S. (2014). Endocasts: Possibilities and limitations for the
interpretation of human brain evolution. Brain, Behavior and
Evolution, 84(2), 117–134. https://doi.org/10.1159/000365276
Nieuwenhuys, R. (1967). Comparative anatomy of the cerebellum.
Progress in Brain Research, 25, 1–93. https://doi.org/10.1016/
S0079-6123(08)60962-0
Northcutt, R. G. (2002). Understanding vertebrate brain evolution.
Integrative and Comparative Biology, 42, 743–756.
Olori, J. C. (2010). Digital endocasts of the cranial cavity and osse-
ous labyrinth of the burrowing snake Uropeltis woodmasoni
(Alethinophidia: Uropeltidae). Copeia, 2010(1), 14–26. https://
doi.org/10.1643/CH-09-082
Olori, J. C., & Bell, C. J. (2012). Comparative skull morphology of
uropeltid snakes (Alethinophidia: Uropeltidae) with special ref-
erence to disarticulated elements and variation. PLoS One, 7(3),
e32450. https://doi.org/10.1371/journal.pone.0032450
Perez-Martinez, C. A., & Leal, M. (2021). Lizards as models to
explore the ecological and neuroanatomical correlates of minia-
turization. Behaviour, 158(12–13), 1121–1168. https://doi.org/
10.1163/1568539X-bja10104
Porter, W. R., & Witmer, L. M. (2015). Vascular patterns in iguanas
and other squamates: Blood vessels and sites of thermal
exchange. PLoS One, 10, e0139215. https://doi.org/10.1371/
journal.pone.0139215
Puelles, L. (2009). Forebrain development: prosomere model. In L. R.
Squire (Ed.), Encyclopedia of Neuroscience, Vol. 4 (pp. 315–319).
Academic Press.
Pyron, R. A., Burbrink, F. T., & Wiens, J. J. (2013). A phylogeny
and revised classification of Squamata, including 4161 species
of lizards and snakes. BMC Evolutionary Biology, 13(1), 1–54.
https://doi.org/10.1186/1471-2148-13-93
19328494, 0, Downloaded from https://anatomypubs.onlinelibrary.wiley.com/doi/10.1002/ar.25142 by Daniel Fernandes - CAPES , Wiley Online Library on [31/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ALLEMAND ET AL.
Racicot, R. (2021). Evolution of whale sensory ecology: Frontiers in
nondestructive anatomical investigations. The Anatomical
Record, 305(3), 736–752. https://doi.org/10.1002/ar.24761
Reynolds, R. G. (2011). Status, conservation, and introduction of
amphibians and reptiles in The Turks and Caicos Islands, Brit-
ish West Indies. In A. Hailey, B. S. Wilson, & J. A. Horrocks
(Eds.), Conservation of Caribbean Island herpetofaunas, Vol. 2:
Regional accounts of the West Indies (pp. 377–406). BRILL.
Roscito, J. G., & Rodrigues, M. T. (2010). Comparative cranial oste-
ology of fossorial lizards from the tribe Gymnophthalmini
(Squamata, Gymnophthalmidae). Journal of Morphology, 271,
1352–1365. https://doi.org/10.1002/jmor.10878
Scanferla, A. (2016). Postnatal ontogeny and the evolution of
macrostomy in snakes. Royal Society Open Science, 3(11),
160612. https://doi.org/10.1098/rsos.160612
Scanferla, A. (2022). A glimpse into the evolution of the ophidian
brain. In D. Gower & H. Zaher (Eds.), The origin and Early evo-
lutionary history of snakes (pp. 294–315). Cambridge University
Press. https://doi.org/10.1017/9781108938891.019
Schade, M., Stumpf, S., Kriwet, J., Kettler, C., & Pfaff, C. (2022).
Neuroanatomy of the nodosaurid Struthiosaurus austriacus
(Dinosauria: Thyreophora) supports potential ecological differ-
entiations within Ankylosauria. Scientific Reports, 12(144), 144.
https://doi.org/10.1038/s41598-021-03599-9
Schwenk, K. (1993). The evolution of chemoreception in squamate
reptiles: A phylogenetic approach. Brain, Behavior and Evolu-
tion, 41(3–5), 124–137.
Segall, M., Cornette, R., Rasmussen, A. R., & Raxworthy, C. J.
(2021). Inside the head of snakes: Influence of size, phylogeny,
and sensory ecology on endocranium morphology. Brain Struc-
ture and Function, 226(7), 2401–2415. https://doi.org/10.1007/
s00429-021-02340-6
Singhal, S., Colston, T. J., Grundler, M. R., Smith, S. A.,
Costa, G. C., Colli, G. R., Moritz, C., Pyron, R. A., &
Rabosky, D. L. (2021). Congruence and conflict in the higher-
level phylogenetics of squamate reptiles: An expanded phyloge-
nomic perspective. Systematic Biology, 70(3), 542–557. https://
doi.org/10.1093/sysbio/syaa054
Siqueira, C. C., Kiefer, M. C., Sluys, M. V., & Rocha, C. F. D. (2013).
Variation in the diet of the lizard Tropidurus torquatus along its
coastal range in Brazil. Biota Neotropica, 13, 93–101.
Smeets, W. J., Hoogland, P. V., & Lohman, A. H. (1986). A fore-
brain atlas of the lizard Gekko gecko. Journal of Comparative
Neurology, 254(1), 1–19. https://doi.org/10.1002/cne.902540102
Smith, K. T., Bhullar, B. A. S., Köhler, G., & Habersetzer, J. (2018).
The only known jawed vertebrate with four eyes and the bau-
plan of the pineal complex. Current Biology, 28(7), 1101–1107.
https://doi.org/10.1016/j.cub.2018.02.021
Starck, D. (1979). Cranio-cerebral relations in recent reptiles. In C.
Gans, R. G. Northcutt, & P. Ulinski (Eds.), Biology of the Repti-
lia, Vol. 9: Neurology a (pp. 1–38). Academic Press.
Telenchev, I., Simeonovska-Nikolova, D., & Tzonev, R. (2017). Hab-
itat use and activity of European glass lizard, Pseudopus apodus
(Pallas, 1775), in southeastern Bulgaria. Turkish Journal of
Zoology, 41(2), 286–293. https://doi.org/10.3906/zoo-1601-3
ten Donkelaar, H. J. (1998). Reptiles. In R. Nieuwenhuys, H. J. ten
Donkelaar, & C. Nicholson (Eds.), The central nervous system of
vertebrates (pp. 1315–1499). Springer-Verlag.
ten Donkelaar, H. J., & Bangma, G. C. (1992). The cerebellum. In
C. Gans & P. S. Ulinski (Eds.), Biology of the Reptilia. Vol. 17:

ALLEMAND ET AL.
Neurology C. sensorimotor integration (pp. 496–586). The
University of Chicago Press.
Triviño, L. N., Albino, A. M., Dozo, M. T., & Williams, J. D. (2018).
First natural endocranial cast of a fossil snake (cretaceous of
Patagonia, Argentina). The Anatomical Record, 301(1), 9–20.
https://doi.org/10.1002/ar.23686
Vickerton, P., Jarvis, J., & Jeffery, N. (2013). Concentration-dependent
specimen shrinkage in iodine-enhanced microCT. Journal of
Anatomy, 223, 185–193. https://doi.org/10.1111/joa.12068
Watanabe, A., Fabre, A. C., Felice, R. N., Maisano, J. A., Müller, J.,
Herrel, A., & Goswami, A. (2019). Ecomorphological diversifi-
cation in squamates from conserved pattern of cranial integra-
tion. Proceedings of the National Academy of Sciences, 116(29),
14688–14697. https://doi.org/10.1073/pnas.1820967116
Watanabe, A., Gignac, P. M., Balanoff, A. M., Green, T. L.,
Kley, N. J., & Norell, M. A. (2019). Are endocasts good proxies
for brain size and shape in archosaurs throughout ontogeny?
Journal of Anatomy, 234(3), 291–305. https://doi.org/10.1111/
joa.12918
Weisbecker, V., Rowe, T., Wroe, S., Macrini, T. E., Garland, K. L.,
Travouillon, K. J., Black, K., Archer, M., Hand, S. J.,
Berlin, J. C., Beck, R. M. D., Ladevèze, S., Sharp, A. C.,
Mardon, K., & Sherratt, E. (2021). Global elongation and high
shape flexibility as an evolutionary hypothesis of accommodat-
ing mammalian brains into skulls. Evolution, 75(3), 625–640.
https://doi.org/10.1111/evo.14163
Werneburg, I., Evers, S. W., & Ferreira, G. (2021). On the “cartilagi-
nous rider” in the endocasts of turtle brain cavities. Vertebrate
Zoology, 71, 403–418. https://doi.org/10.3897/vz.71.e66756
Witmer, L. M., Ridgely, R. C., Dufeau, D. L., & Semones, M. C.
(2008). Using CT to peer into the past: 3D visualization of the
brain and ear regions of birds, crocodiles, and non-avian
19328494, 0, Downloaded from https://anatomypubs.onlinelibrary.wiley.com/doi/10.1002/ar.25142 by Daniel Fernandes - CAPES , Wiley Online Library on [31/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
23
dinosaurs. In H. Endo & R. Frey (Eds.), Anatomical Imaging
(pp. 67–87). Springer.
Yaryhin, O., Klembara, J., Pichugin, Y., Kaucka, M., &
Werneburg, I. (2021). Limb reduction in squamate reptiles cor-
relates with the reduction of the chondrocranium: A case study
on serpentiform anguids. Developmental Dynamics, 250, 1300–
1317. https://doi.org/10.1002/dvdy.307
Zaher, H., & Scanferla, C. A. (2012). The skull of the upper creta-
ceous snake Dinilysia patagonica Smith-Woodward, 1901, and
its phylogenetic position revisited. Zoological Journal of the Lin-
nean Society, 164(1), 194–238.
Zhu, Y. A., Giles, S., Young, G., Hu, Y., Bazzi, M., Ahlberg, P. E.,
Min, Z., & Lu, J. (2020). Endocast and bony labyrinth of a stem
gnathostome shed light on the earliest diversification of jawed
vertebrates. Current Biology, 31(5), 1112–1118. https://doi.org/
10.1016/j.cub.2020.12.046
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Correspondences and spatial relationships in
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