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Evolution of tooth morphological complexity and its association with the position of tooth eruption in the jaw in non-mammalian synapsids

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Heterodonty and complex molar morphology are important characteristics of mammals acquired during the evolution of early mammals from non-mammalian synapsids. Some non-mammalian synapsids had only simple, unicuspid teeth, whereas others had complex, multicuspid teeth. In this study, we reconstructed the ancestral states of tooth morphological complexity across non-mammalian synapsids to show that morphologically complex teeth evolved independently multiple times within Therapsida and that secondary simplification of tooth morphology occurred in some non-mammalian Cynodontia. In some mammals, secondary evolution of simpler teeth from complex molars has been previously reported to correlate with an anterior shift of tooth eruption position in the jaw, as evaluated by the dentition position relative to the ends of component bones used as reference points in the upper jaw. Our phylogenetic comparative analyses showed a significant correlation between an increase in tooth complexity and a posterior shift in the dentition position relative to only one of the three specific ends of component bones that we used as reference points in the upper jaw of non-mammalian synapsids. The ends of component bones depend on the shape and relative area of each bone, which appear to vary considerably among the synapsid taxa. Quantification of the dentition position along the anteroposterior axis in the overall cranium showed suggestive evidence of a correlation between an increase in tooth complexity and a posterior shift in the dentition position among non-mammalian synapsids. This correlation supports the hypothesis that a posterior shift of tooth eruption position relative to the morphogenetic fields that determine tooth form have contributed to the evolution of morphologically complex teeth in non-mammalian synapsids, if the position in the cranium represents a certain point in the morphogenetic fields.
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Evolution of tooth morphological
complexity and its association with the
position of tooth eruption in the jaw in
non-mammalian synapsids
Tomohiro Harano and Masakazu Asahara
Division of Liberal Arts and Sciences, Aichi Gakuin University, Nisshin, Aichi, Japan
ABSTRACT
Heterodonty and complex molar morphology are important characteristics of
mammals acquired during the evolution of early mammals from non-mammalian
synapsids. Some non-mammalian synapsids had only simple, unicuspid teeth,
whereas others had complex, multicuspid teeth. In this study, we reconstructed the
ancestral states of tooth morphological complexity across non-mammalian synapsids
to show that morphologically complex teeth evolved independently multiple times
within Therapsida and that secondary simplication of tooth morphology occurred
in some non-mammalian Cynodontia. In some mammals, secondary evolution of
simpler teeth from complex molars has been previously reported to correlate with an
anterior shift of tooth eruption position in the jaw, as evaluated by the dentition
position relative to the ends of component bones used as reference points in the
upper jaw. Our phylogenetic comparative analyses showed a signicant correlation
between an increase in tooth complexity and a posterior shift in the dentition
position relative to only one of the three specic ends of component bones that we
used as reference points in the upper jaw of non-mammalian synapsids. The ends of
component bones depend on the shape and relative area of each bone, which appear
to vary considerably among the synapsid taxa. Quantication of the dentition
position along the anteroposterior axis in the overall cranium showed suggestive
evidence of a correlation between an increase in tooth complexity and a posterior
shift in the dentition position among non-mammalian synapsids. This correlation
supports the hypothesis that a posterior shift of tooth eruption position relative to the
morphogenetic elds that determine tooth form have contributed to the evolution of
morphologically complex teeth in non-mammalian synapsids, if the position in the
cranium represents a certain point in the morphogenetic elds.
Subjects Evolutionary Studies, Paleontology, Zoology
Keywords Synapsida, Therapsida, Cynodontia, Mammaliamorpha, Mammaliaformes, Dentition,
Field theory, Tritubercular theory
INTRODUCTION
Heterodont dentition and complex molar morphology are evolutionary innovations that
have enabled efcient food processing and adaptive radiations (Romer & Parsons, 1986;
Hunter & Jernvall, 1995;Colbert, Morales & Minkoff, 2001;Kemp, 2005;Luo, 2007;
How to cite this article Harano T, Asahara M. 2024. Evolution of tooth morphological complexity and its association with the position of
tooth eruption in the jaw in non-mammalian synapsids. PeerJ 12:e17784 DOI 10.7717/peerj.17784
Submitted 7 December 2023
Accepted 30 June 2024
Published 12 August 2024
Corresponding author
Masakazu Asahara,
kamono.mana@gmail.com
Academic editor
Nicholas Pyenson
Additional Information and
Declarations can be found on
page 19
DOI 10.7717/peerj.17784
Copyright
2024 Harano and Asahara
Distributed under
Creative Commons CC-BY 4.0
Ungar, 2010) and are fundamental to mammalian diversity (Weller, 1968;Stock et al., 1997;
Feldhamer et al., 2003;Ungar, 2010). These traits have been gradually acquired during the
evolution of early mammals from some of the non-mammalian synapsids (Weller, 1968;
Feldhamer et al., 2003;Kemp, 2005;Ungar, 2010). The acquisition process of complex
molar morphology has been assumed to have progressed in the following sequence: one
cusp, three main cusps, a triangular arrangement of main cusps, and then the addition of
cusps at the lingual side in upper teeth and the buccal side in lower teeth, as indicated by
the tritubercular theory (Osborn, 1888,1897;Gregory, 1934;Crompton & Jenkins, 1968;
Ungar, 2010;Yamanaka, 2022). Therefore, the increase in the number of cusps and the
change in their arrangement are considered major events in the evolution of
mammalian-type molar morphology.
Synapsida includes Therapsida, which in turn includes Cynodontia (see Fig. 1 for the
phylogeny of synapsid taxa considered in this study). Within Cynodontia, all mammals
and their closest extinct relatives such as Morganucodon constitute Mammaliaformes;
furthermore, Mammaliaformes and their closest extinct relatives including
Tritylodontidae constitute Mammaliamorpha (Rowe, 1988). Early synapsids had only
simple, unicuspid teeth, whereas non-mammalian cynodonts had complex, multicuspid
teeth in heterodont dentitions (Weller, 1968;Feldhamer et al., 2003;Kemp, 2005;Ungar,
2010). The evolution of complex tooth morphology has been previously considered
separately for some lower taxa of non-mammalian synapsids, with remarkable examples
including the acquisition of leaf-shaped teeth as an adaptation to herbivorous diet in
Suminia (Rybczynski & Reisz, 2001), the differentiation of a number of cusps on the teeth
in Dvinia (Tatarinov, 1968;Kemp, 1979), and the occurrence of complex molar
morphology in tritylodontids (Kemp, 2005). To our knowledge, no previous study has used
recent phylogenetic hypotheses and comparative methods to reconstruct the evolutionary
history of tooth morphology across non-mammalian synapsids.
Convergent evolution of several types of dental morphology is known to have occurred
in mammals, with the most prominent examples including the independent acquisition of
hypocones in several lineages with herbivorous adaptations (Hunter & Jernvall, 1995) and
the independent evolution of carnassial teeth in several lineages with carnivorous
adaptations (Van Valkenburgh, 2007;Ungar, 2010). In addition, tribosphenic molar
function was independently acquired in both Laurasian and Gondwanan lineages of
mammals during the Mesozoic (i.e., Australosphenida and Boreosphenida), as well as in
Shuotheriidae, and some docodont mammaliaforms (Luo, 2007). Among eutherian
mammals, a simple molar morphology with the linear cusp arrangement or a single cusp
have evolved secondarily in some taxa, such as pinnipeds and toothed whales (Rybczynski,
Dawson & Tedford, 2009;Armeld et al., 2013;Davis, 2019;Harano & Asahara, 2022a). In
squamate reptiles, a phylogenetic comparative study including fossil and extant taxa
showed independent evolution of multicuspid teeth from a unicuspid ancestral
morphology in a large number of lineages and reversals toward reduced tooth complexity
in numerous lineages (Lafuma et al., 2021). Convergent evolution of a complex tooth
morphology and secondary evolution of a simpler tooth morphology may have occurred in
non-mammalian synapsids.
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 2/22
Tooth complexity level
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Mammaliamorpha
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Dinocephalia
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Figure 1 Evolutionary history of tooth complexity on the phylogenetic tree of non-mammalian synapsids. The ancestral states reconstructed
using parsimony methods are indicated by the colors of the branches and the values assigned to the nodes. Schematic diagrams of ventral views of
the cranium of the representative taxa show the approximate outline of the dentition, maxilla, and palatine. These diagrams were drawn based on
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 3/22
The evolutionary and developmental factors underlying tooth morphological
complexity have long been a focus of attention but are relatively poorly understood (Cope,
1883;Osborn, 1888,1897;Tims, 1903;Butler, 1939;Feldhamer et al., 2003;Kemp, 2005;
Ungar, 2010;Yamanaka, 2022). Traditional eld theory (Butler, 1939) postulates that
morphogenetic elds in the jawbone induce different tooth forms, i.e., the incisivization or
caninization eld in the anterior part of the jaw induces simple tooth morphology, whereas
the molarization eld in the posterior part of the jaw induces complex tooth morphology.
Its modern version, the concentration gradients of morphogens, such as bone
morphogenetic protein, BMP4, and broblast growth factor, FGF8, observed along the
anteroposterior axis in the jawbone have been reported to be associated with tooth form. In
the pig (Sus scrofa), BMP4 is expressed in the mesial (rostral) region, in which incisors or
canines with simple morphology erupt, and FGF8 is expressed in the distal (caudal) region,
in which morphologically complex molars erupt (Armeld et al., 2013). In contrast, BMP4
is expressed throughout the region of tooth eruption in the pantropical spotted dolphin
(Stenella attenuata), which possesses only simple teeth (Armeld et al., 2013). In the house
shrew (Suncus murinus), the BMP4 and FGF8 expression regions correspond to the
incisor- and molar-forming regions, respectively, in the jaw (Yamanaka et al., 2015). In the
gray short-tailed opossum (Monodelphis domestica), the regions with differential
expression of homeobox genes, Alx3, Msx1, and BarX1, likely correspond to the regions of
different tooth classes, and the expressions of BMP4 and FGF8 along the mesio-distal axis
in the jaw overlap with those of Msx1 and BarX1, respectively (Wakamatsu et al., 2019).
These morphogens and associated molecules are known to affect the shape and size of
teeth and the size and number of cusps (Asahara et al., 2016;Couzens et al., 2016;Couzens,
Sears & Rücklin, 2019;Zurowski et al., 2018;Selig, Khalid & Silcox, 2021). According to
these ndings, the tooth eruption position relative to the morphogenetic elds along the
anteroposterior axis in the jaw appear to have an important role in determining tooth
morphology.
Recently, Harano & Asahara (2022a) evaluated the morphological complexity of teeth
and the anteroposterior position of dentition relative to the component bones in the upper
jaws of numerous species of eutherian mammalian, including the carnivorans, cetaceans,
and even-toed ungulates, and found a phylogenetically adjusted correlation between tooth
simplication and an anterior shift (anteriorization) of the dentition position in the
carnivoran clade (Carnivora) and the cetacean and even-toed ungulate clade (Artiodactyla,
sometimes called Cetartiodactyla). Taken together, this nding, the eld theory
Figure 1 (continued)
illustrations taken from the literature: Euromycter rutenus (non-therapsid synapsids) from Sigogneau-Russell & Russell (1974);Dimetrodon limbatus
(non-therapsid synapsids) from Amson & Laurin (2011);Ulemosaurus svijagensis (Dinocephalia) from Kemp (2005);Suminia getmanovi
(Anomodontia) from Kemp (2005);Leontosaurus vanderhorsti (Gorgonopsia) from Kammerer (2016);Moschorhinus kitchingi (Therocephalia) from
Durand (1991);Dvinia prima (Cynodontia) from Tatarinov (1968);Probainognathus jenseni (Cynodontia) from Hopson & Kitching (2001);
Kayentatherium (Mammaliamorpha) from Kemp (2005); and Haldanodon exspectatus (Mammaliaformes) from Kielan-Jaworowska, Cifelli & Luo
(2004). Additional details on the trees and the values of the ancestral states at each node are presented in Fig. S1.
Full-size
DOI: 10.7717/peerj.17784/g-1
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(Butler, 1939), and the experimental evidence for morphogen concentration gradients
associated with different tooth types (Armeld et al., 2013;Yamanaka et al., 2015;
Wakamatsu et al., 2019) suggest that an anterior shift of the tooth eruption position
relative to the morphogenetic elds, which are assumed to be present at specic locations
associated with the component bones in the jaw, is a factor in the evolutionary
simplication in tooth morphology in some carnivorans (e.g., pinnipeds) and cetaceans (i.
e., toothed whales) (Harano & Asahara, 2022a).
The evolutionary simplication in tooth morphology in some eutherian mammals
appears to have reversed the acquisition process of complex teeth that occurred during the
evolution of early mammals from some of the non-mammalian synapsids (Harano &
Asahara, 2022a). The evolution of complex teeth, as well as of simplied teeth, may be
attributable to the shifting of the dentition position relative to the morphogenetic elds.
Therefore, we hypothesized that a posterior shift of the dentition position relative to the
morphogenetic elds in the jaw has contributed to the evolution of complex tooth
morphology in non-mammalian synapsids. According to this hypothesis, tooth complexity
can be expected to be correlated with the anteroposterior position of the dentition in
synapsid jaws. To test this expectation, a comprehensive phylogeny of synapsids (Jones,
Angielczyk & Pierce, 2019) was used in this study, along with phylogenetic comparative
analyses that were conducted across a number of non-mammalian synapsids.
In this study, we rated tooth morphological complexity in non-mammalian synapsids
and quantied the anteroposterior position of their dentition relative to the ends of
component bones as reference points in the upper jaw, following a previous study (Harano
& Asahara, 2022a). This approach assumed that the ends of component bones are a proxy
for the positions of the morphogenetic elds. However, this assumption may not be valid
for non-mammalian synapsids because the ends of component bones depend on the shape
and relative area of each component bone in the upper jaw, and these appear to vary more
remarkably among the synapsids (schematic diagrams of the cranium of the representative
taxa are presented in Fig. 1) than among the carnivoran clade or the cetacean and
even-toed ungulate clade in eutherian mammals. Therefore, the position of the dentition
along the anteroposterior axis in the overall cranium was also quantied in
non-mammalian synapsids. These measurements were used to reconstruct the
evolutionary history of tooth morphological complexity and to test the correlation between
tooth complexity and the anteroposterior position of the dentition in the upper jaw or the
cranium.
MATERIALS AND METHODS
Measurements of dentition position
To measure the positioning of the dentition in the upper jaw or cranium, illustrations of
ventral views of crania that were taken from the literature listed in Dataset S1 were used.
These illustrations came from 60 taxa of non-mammalian synapsids, 55 of which belong to
Therapsida. The Therapsida taxa included Biarmosuchia, Dinocephalia, Anomodontia,
Gorgonopsia, Therocephalia, and Cynodontia. Of the 24 taxa of Cynodontia, 11 belong to
Mammaliamorpha, and three belong to Mammaliaformes.
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 5/22
The posterior end of the dentition was used as a point to measure the dentition position
(Fig. 2). In the upper jaw of mammals, the morphologically complex molars are rooted in
the maxilla (Yamanaka et al., 2015). The regions of maxilla and the palatine adjacent to the
maxilla were examined to determine reference points in the upper jaw of non-mammalian
synapsids. The anterior end of palatine, posterior end of palatine, and posterior end of
maxilla were identiable in illustrations of crania of various non-mammalian synapsids
and were used as the reference points (Fig. 2). Accordingly, the dentition position was
evaluated relative to each of the three reference points. Moreover, the dentition position
within the overall cranium was evaluated.
Measurements were conducted as previously described in Harano & Asahara (2022a).
Specically, landmarks were digitized onto the illustrations using tpsDig software version
2.31 (Rohlf, 2017), with the conguration displayed in Fig. 2. A perpendicular line was
drawn from each landmark to the midline of the cranium (the line connecting landmarks
1 and 2; Fig. 2), and the point of intersection was used to determine the position of the
landmark along the anteroposterior axis. The length from the anterior end of the
premaxilla to each of the posterior end of the dentition (length to post-dentition), the
anterior end of palatine (length to ante-palatine), posterior end of palatine (length to post-
palatine), and posterior end of maxilla (length to post-maxilla) were all calculated from the
anteroposterior positions of landmarks on the left and right sides and then averaged for
each specimen. Data on the length to post-maxilla were not available for two taxa
(Yunnanodon and Pseudotherium argentinus) because the position of the posterior
end of maxilla could not be identied in available illustrations. The length from the
Length to ante-palatine
1
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Length to post-dentition
Cranial length
Length to post-palatine
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10
Length to post-maxilla
Figure 2 Positions of landmarks used in this study. The landmarks were dened as follows: (1) anterior
end of the premaxilla; (2) basion; (3) and (4) posterior end of the dentition; (5) and (6) anterior end of the
palatine; (7) and (8) posterior end of the palatine; (9) and (10) posterior end of the maxilla. The inter-
section of the midline of the cranium (the line connecting landmark 1 to 2) with the perpendicular line
(denoted by the dotted lines) from each landmark (3 to 10) to the midline was taken to determine the
anteroposterior position of each landmark. The distances between the anteroposterior positions were
calculated as the lengths from the anterior end of the premaxilla to the posterior end of the dentition
(length to post-dentition), the anterior end of palatine (length to ante-palatine), posterior end of palatine
(length to post-palatine), posterior end of maxilla (length to post-maxilla), and posterior end of the
cranium (cranial length). The diagram of the cranium used in this representation was drawn from an
illustration of Aelurognathus tigriceps in Kammerer (2016).Full-size
DOI: 10.7717/peerj.17784/g-2
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anterior end of the premaxilla to the posterior end of the cranium (cranial length)
were calculated for each specimen. If the scale was not provided with the illustration,
available data on skull length of the taxon were used as a proxy for scale to allow the
conversion of the distance seen in the illustration into an actual measurement usable for
analyses. The measurements for all taxa included in the present study are shown in,
Dataset S2. All data on length were converted to natural logarithms prior to subsequent
analyses.
Tooth complexity
Illustrations or images of teeth of the synapsid taxa included in this study were obtained
from the literature listed in Dataset S1. The number and arrangement of cusps on the teeth
shown in the illustration or image were visually examined to assess the tooth
morphological complexity. Cusp number and arrangement have been used to classify
tooth morphology in mammals (Jernvall et al., 1996;Harano & Asahara, 2022a) and
mammaliaforms (Couzens, Sears & Rücklin, 2021), and cusp number has been used as a
measure of tooth complexity in squamate reptiles (Lafuma et al., 2021). The criteria for
classifying the tooth complexity level established in a previous study (Harano & Asahara,
2022a) were derived primarily from the stages originally proposed by the tritubercular
theory (Osborn, 1888,1897;Gregory, 1934). We used these criteria with a few changes to
accommodate any cusp arrangement observed in non-mammalian synapsids. Our criteria
were as follows (Fig. 3):
1
2
3
4
5
Tooth complexity level
Figure 3 Classication of tooth complexity used in this study. Tooth complexity was categorized into
ve levels based on cusp number and arrangement. The schematic drawings represent occlusal views of
the cusp arrangement on the tooth at each level of complexity.
Full-size
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Level 1: Only one cusp.
Level 2: Two or three cusps arranged in a row along the mesio-distal axis.
Level 3: More than three cusps arranged in a row along the mesio-distal axis or
continuously in a row along the cingulum.
Level 4: Three cusps arranged in triangle form by shifting the cusps to the lingual or
buccal side. If a tooth has more than two cusps, one of which was deviated from the row of
cusps beyond the cusp width, then the tooth was classied in this level.
Level 5: Development of an additional cusp at the lingual side. If a tooth has the rows of
cusps on both lingual and buccal side, then the tooth was classied in this level.
If the illustration or image showed only a lateral view of teeth, we considered that the
cusps were arranged in a line along the mesio-distal axis and classied the teeth into either
level 1, 2, or 3. Each taxon received a score of one of these ve levels based on the highest
level found in their teeth.
Phylogenetic comparative analyses
The phylogeny of synapsids used in this study was derived from the supertree
reconstructed by Jones, Angielczyk & Pierce (2019), who described 60 time-scaled
phylogenetic trees. A majority-rule consensus tree was computed with branch lengths
from these 60 trees using the consensus edges function in the phytools package (Revell,
2012) of R version 4.2.2 (R Development Core Team, 2022). Taxa that were not included in
our analyses were pruned from the tree. P. argentinus was inserted into the relevant
positions in the tree according to Wallace, Martínez & Rowe (2019). Among the taxa
included in this study, Hadrocodium wui is the most closely related to mammals.
The ancestral states of tooth complexity level and the positioning of the dentition in the
upper jaw or cranium were reconstructed using parsimony methods in Mesquite version
3.61 (Maddison & Maddison, 2019), as previously described in Harano & Asahara (2022a).
The tooth complexity level was treated as an ordered character. For an ordered character,
parsimony methods determine the ancestral states that minimize the number of steps of
character change, assuming that the number of steps from state i to state j is |i-j| (Maddison
& Maddison, 2019). Thus, the underlying assumption for this approach is that all tooth
complexity levels are placed at equal intervals. The positioning of the dentition was treated
as a continuous character in the ancestral state reconstructions. To obtain univariate trait
values of the positioning of the dentition, the length to post-dentition was regressed on
each of the following: length to ante-palatine, length to post-palatine, length to post-
maxilla, and cranial length (see Fig. 2 for length measurements); after which a residual
value was calculated for each taxon. The residual values were used to quantify the dentition
position relative to the anterior end of palatine (model formula: length to post-dentition
(log) ~ length to ante-palatine (log)), relative to the posterior end of palatine (model
formula: length to post-dentition (log) ~ length to post-palatine (log)), relative to the
posterior end of maxilla (model formula: length to post-dentition (log) ~ length to
post-maxilla (log)), and in the cranium (model formula: length to post-dentition
(log) ~ cranial length (log)) because a larger residual value represents a more posterior
positioning of the dentition. These regressions were conducted using phylogenetic
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 8/22
generalized least squares (PGLS) to control for the effect of phylogenetic relatedness
between taxa. Pagels lambda (λ), a measure of the phylogenetic signal, was estimated to
scale the phylogenetic correlation structure in the PGLS models. In general, λranges from
0 to 1, where 0 indicates no phylogenetic correlation and 1 indicates that the phylogenetic
correlation structure is in agreement with a Brownian motion model of evolution. All
PGLS analyses were performed using the phylolm function in the phylolm package (Ho &
Ané, 2014) in R version 4.2.2 (R Development Core Team, 2022).
A correlation between tooth complexity and the positioning of the dentition in the
upper jaw or cranium was tested following the methods previously described in Harano &
Asahara (2022a). Specically, separate PGLS models were used to analyze the dentition
position relative to the anterior end of palatine, relative to the posterior end of palatine,
relative to the posterior end of maxilla, and in the cranium. The length to post-dentition
was included as the response variable, and the level of tooth complexity and either the
length to ante-palatine, length to post-palatine, length to post-maxilla, or cranial
length were included as explanatory variables in the PGLS models (model formula: length
to post-dentition (log) ~ tooth complexity level + length to ante-palatine (log), length
to post-dentition (log) ~ tooth complexity level + length to post-palatine (log),
length to post-dentition (log) ~ tooth complexity level + length to post-maxilla (log), and
length to post-dentition (log) ~ tooth complexity level + cranial length (log); see Fig. 2 for
denitions of positions and length measurements). These models enable the examination
of the relationship between tooth complexity level and length to post-dentition while
controlling for either the length to ante-palatine, length to post-palatine, length to post-
maxilla, or cranial length as a predictor and phylogeny. To control for the effect of a
predictor, including the predictor as one of the explanatory variables in a multiple
regression model is more appropriate than taking the residual from the regression against
the predictor and using the residual as data during further regression analysis (García-
Berthou, 2001;Freckleton, 2009). The tooth complexity level was treated as a single
quantitative variable in the PGLS models. This assumed that all tooth complexity levels are
placed at equal intervals, similar to the ancestral state reconstructions using parsimony
method described above.
RESULTS
Ancestral state reconstructions
To visualize the evolutionary history of tooth complexity, the reconstructed ancestral states
were mapped onto the phylogenetic tree (Fig. 1; further details on the tree can be found in
Fig. S1). All non-therapsid synapsids included in this analysis had the simplest, unicuspid
teeth. The reconstruction showed that the most recent common ancestor of all therapsids
inherited the simplest teeth from its ancestor. Within Therapsida, teeth with a second cusp
(tooth complexity level 2) were independently acquired three times. Teeth with more than
three cusps arranged in a line (tooth complexity level 3) evolved independently twice, one
instance of which occurred at the base of Cynodontia. Within Cynodontia, the highest
level of tooth complexity (tooth complexity level 5) evolved independently four times, two
instances of which occurred in lineages that did not lead to Mammaliamorpha. The
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 9/22
Cynodontia
Therocephalia
Gorgonopsia
Anomodontia
Dinocephalia
Biarmosuchia
Mammaliamorpha
Mammaliaformes
Non-therapsid synapsids
Therapsida
Dentition position relative to the anterior end of palatine
Anterior
Posterior
Unambiguous increase
Possible increase
Change in tooth complexity level
Unambiguous reduction
Possible reduction
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Figure 4 Evolutionary history of the dentition position relative to the anterior end of palatine on the phylogenetic tree of non-mammalian
synapsids. This position was calculated as residuals from the PGLS regression of the length to post-dentition on the length to ante-palatine.
The denitions of positions and length measurements are presented in Fig. 2. The statistics of the regression are presented in Table S1a. The ancestral
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 10/22
remaining two occurrences of independent evolution of the highest level of tooth
complexity were found within Mammaliamorpha, one of which was found within
Mammaliaformes. Within Mammaliamorpha, two possible patterns for the evolutionary
history of teeth with triangular cusp arrangement (tooth complexity level 4) were equally
supported. In one pattern, these teeth were independently acquired twice, while in the
other, they were acquired at the base of Mammaliamorph and subsequently lost (evolution
from tooth complexity level 4 to 3) at the base of the subclade including Mammaliaformes.
Furthermore, reductions in tooth complexity occurred independently twice, with one
instance (evolution from tooth complexity level 3 to 2) observed within
Mammaliamorpha, and the other (evolution from tooth complexity level 5 to 4) occurring
in another cynodont lineage.
The reconstructed ancestral states of the dentition position relative to the anterior end
of palatine (Fig. 4; further details on the trees can be found in Fig. S2), relative to the
posterior end of palatine (Fig. 5; further details on the trees can be found in Fig. S3),
relative to the posterior end of maxilla (Fig. 6; further details on the trees can be found in
Fig. S4), and in the cranium (Fig. 7; further details on the trees can be found in Fig. S5)
were mapped onto the phylogenetic tree. The evolutionary history of these dentition
positions appears to demonstrate considerable differences. The dentition position relative
to the posterior end of maxilla (Fig. 6) and in the cranium (Fig. 7) showed a tendency to be
more anterior in non-cynodont therapsids compared with the earlier, non-therapsid
synapsids. These positions appear to have shifted posteriorly during the evolution of
cynodonts from non-cynodont therapsids (Figs. 6 and 7). The dentition position in the
cranium seems to have shifted further posteriorly in Mammaliamorpha (Fig. 7). Such
shifts were not apparent in the evolutionary history of the dentition position relative to the
anterior end of palatine (Fig. 4) and the posterior end of palatine (Fig. 5). An additional
description of the reconstructed ancestral state of these positions is provided in
Supplemental Text.
Correlation between tooth complexity and the positioning of the
dentition
No signicant relationship was found between tooth complexity level and the length to
post-dentition when controlled for the length to ante-palatine (Table 1A;Fig. S6A) and
controlled for the length to post-palatine (Table 1B;Fig. S6B) across non-mammalian
synapsids. A signicant positive relationship between tooth complexity level and the length
to post-dentition was found when controlled for the length to post-maxilla (Table 1C;
Fig. S6C). A signicant positive relationship was also observed between tooth complexity
Figure 4 (continued)
states reconstructed using parsimony methods are indicated by the colors of the branches with numerical labels corresponding to each color.
The open circles represent nodes of unambiguous increased tooth complexity, the open triangles represent nodes with increased tooth complexity in
one of the most likely patterns for the evolutionary history of tooth complexity, the closed circle represents a node of unambiguous reduction in
tooth complexity, and the closed triangle represents a node where reduction in tooth complexity was observed in one of the most likely patterns for
the evolutionary history of tooth complexity. Additional details on the tree are presented in Fig. S2. The values of the ancestral states at each node can
be found in Table S2.Full-size
DOI: 10.7717/peerj.17784/g-4
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 11/22
Cynodontia
Therocephalia
Gorgonopsia
Anomodontia
Dinocephalia
Biarmosuchia
Mammaliamorpha
Mammaliaformes
Non-therapsid synapsids
Therapsida
Dentition position relative to the posterior end of palatine
Anterior
Posterior
Unambiguous increase
Possible increase
Change in tooth complexity level
Unambiguous reduction
Possible reduction
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Figure 5 Evolutionary history of the dentition position relative to the posterior end of palatine on the phylogenetic tree of non-mammalian
synapsids. This position was calculated as residuals from the PGLS regression of the length to post-dentition on the length to post-palatine.
The denitions of positions and length measurements are presented in Fig. 2. The statistics of the regression are given in Table S1b. The ancestral
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 12/22
level and the length to post-dentition when controlled for the cranial length (Table 1D;
Fig. S6D). Therefore, an increase in tooth complexity level was signicantly correlated with
a posterior shift of the dentition position relative to post-maxilla, as well as with a posterior
shift of the dentition position along the anteroposterior axis in the cranium across
non-mammalian synapsids.
DISCUSSION
This study reconstructed the evolutionary history of tooth morphological complexity on
the phylogeny of non-mammalian synapsids to reveal that the common ancestor of all
therapsids had the simplest, unicuspid teeth (tooth complexity of level 1), and complex
teeth, characterized by the development of additional cusps and a triangular arrangement
(tooth complexity of level 5), evolved independently in four lineages (Fig. 1). Furthermore,
secondary simplication was estimated to have occurred independently in at least two
lineages of non-mammalian cynodonts (Fig. 1). These results were obtained through the
analyses performed in this study, which included a limited number of taxa. If a larger
number of taxa are included in the analyses, it is possible that complex and secondarily
simplied teeth could be estimated to have evolved more frequently in non-mammalian
synapsids.
Tooth morphology is a relatively stable trait and is widely used in the phylogenetic
estimation and classication of mammals (Kangas et al., 2004;Ungar, 2010;Harjunmaa
et al., 2014). However, the number of cusps on the postcanine teeth varies among
individuals in the ringed seal (Phoca hispida)(Jernvall, 2000). The outcomes of the present
study indicate that the evolutionary changes in tooth morphological complexity have
occurred independently multiple times in non-mammalian synapsids, in a similar manner
as was inferred in mammals (e.g., Hunter & Jernvall, 1995;Couzens, Sears & Rücklin, 2021;
Harano & Asahara, 2022a) and squamate reptiles (Lafuma et al., 2021). These ndings
suggest that cusp differentiation may be inuenced by changes in a small number of
parameters involved in the developmental process of tooth morphogenesis (Salazar-
Ciudad & Jernvall, 2010;Asahara et al., 2016;Zurowski et al., 2018;Couzens et al., 2016;
Couzens, Sears & Rücklin, 2019;Selig, Khalid & Silcox, 2021).
Simple tooth variants appear more readily than complex tooth variants, which generates
a bias against increase in tooth complexity (Harjunmaa et al., 2012). Nevertheless, an
evolutionary increase rather than a decrease in tooth complexity was predominant in
mammals (Hunter & Jernvall, 1995;Ungar, 2010;Couzens et al., 2016;Couzens, Sears &
Rücklin, 2021). A similar pattern was observed in non-mammalian synapsids. This pattern
is not solely due to evolution beginning from the lowest tooth complexity (tooth
complexity of level 1), where only increases in tooth complexity can occur. Our study
showed that in teeth of intermediate complexity (tooth complexity of level 2, 3, or 4),
Figure 5 (continued)
states reconstructed using parsimony methods are indicated by the colors of the branches with numerical labels corresponding to each color.
The open circles, open triangles, closed circle, and closed triangle are as in Fig. 4. Additional details on the tree can be found in Fig. S3. The values of
the ancestral states at each node can be found in Table S3.Full-size
DOI: 10.7717/peerj.17784/g-5
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 13/22
Cynodontia
Therocephalia
Gorgonopsia
Anomodontia
Dinocephalia
Biarmosuchia
Mammaliamorpha
Mammaliaformes
Non-therapsid synapsids
Therapsida
Unambiguous increase
Possible increase
Change in tooth complexity level
Unambiguous reduction
Possible reduction
1
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10 10
10 10
10 9
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666
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5
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6
6
5
5
44
6
6
8
7
8
8
8
9
Dentition position relative to the posterior end of maxilla
Anterior
Posterior
10
Figure 6 Evolutionary history of the dentition position relative to the posterior end of maxilla on the phylogenetic tree of non-mammalian
synapsids. This position was calculated as residuals from the PGLS regression of the length to post-dentition on the length to post-maxilla.
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 14/22
where both increases and decreases in tooth complexity are possible, an increase in tooth
complexity occurred at least six times, while a decrease occurred once or twice (Fig. 1). The
morphologically complex molars of mammals have shearing, crushing or grinding
function that facilitates food processing through mastication (Ungar, 2010;Williams,
2019). Selection for improved ability to process foods appears to overcome the bias in the
production of variation in tooth morphology, thereby resulting in more frequent evolution
toward complex teeth across synapsids including mammals.
In eutherian mammals, the simplication of molar morphology is correlated with the
anteriorization of the dentition position relative to component bones in the upper jaw in
the carnivoran clade and the cetacean and even-toed ungulate clade (Harano & Asahara,
2022a). This implies that shifting the dentition position relative to the morphogenetic
elds along the anteroposterior axis in the jaw, which are assumed to be present at specic
locations associated with the component bones in the jaw, has contributed to the evolution
of tooth complexity (Harano & Asahara, 2022a). Our phylogenetic comparative analyses
failed to detect a signicant correlation between tooth complexity and the dentition
position relative to two of the three specic ends of component bones used as reference
points in the upper jaw of non-mammalian synapsids (Tables 1A,1B). This study included
a limited number of taxa of non-mammalian synapsids, as data on the dentition position
relative to the ends of component bones in the upper jaw were only available for these taxa.
This limitation might have hindered the detection of a signicant correlation between
tooth complexity and the dentition position. Nevertheless, our analyses showed a
signicant correlation between more complex tooth morphology and a more posterior
dentition position relative to the remaining one of the three specic ends of component
bones in the upper jaw of non-mammalian synapsids (Table 1C). The reconstructed
evolutionary history of the dentition positioning in the upper jaw varied considerably
according to the reference point (Figs. 46). These results are attributable to the fact that
the positional relationships between the ends of component bones vary among the taxa
(Fig. S7).
The ends of component bones depend on the shape and relative area of each component
bone in the upper jaw (see Fig. 1), whereas the position of the dentition along the
anteroposterior axis in the overall cranium does not. A more complex tooth morphology
was signicantly correlated with a more posterior dentition position along the
anteroposterior axis in the cranium across non-mammalian synapsids (Table 1D). The
morphogenetic elds may be associated with the specic location along the anteroposterior
axis in the cranium rather than specic bone locations in non-mammalian synapsids. If
this is the case, our results are consistent with the expectation from the hypothesis that a
Figure 6 (continued)
The denitions of positions and length measurements are presented in Fig. 2. The statistics of the regression are given in Table S1c. The ancestral
states reconstructed using parsimony methods are indicated by the colors of the branches with numerical labels corresponding to each color.
The open circles, open triangles, closed circle, and closed triangle are as in Fig. 4. Additional details on the tree can be found in Fig. S4. The values of
the ancestral states at each node can be found in Table S4.Full-size
DOI: 10.7717/peerj.17784/g-6
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 15/22
Cynodontia
Therocephalia
Gorgonopsia
Anomodontia
Dinocephalia
Biarmosuchia
Mammaliamorpha
Mammaliaformes
Non-therapsid synapsids
Therapsida
Unambiguous increase
Possible increase
Change in tooth complexity level
Unambiguous reduction
Possible reduction
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Dentition position in the cranium
Anterior
Posterior
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Figure 7 Evolutionary history of the dentition position in the cranium on the phylogenetic tree of non-mammalian synapsids. This position
was calculated as residuals from the PGLS regression of the length to post-dentition on the cranial length. The denitions of positions and length
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 16/22
posterior shift of the dentition position relative to the morphogenetic elds is a factor in
the evolution of morphologically complex teeth.
The dentition position along the anteroposterior axis in the cranium can be affected not
only by its position within the upper jaw but also by braincase size, and because the
posterior expansion of braincase may move the dentition relatively forward in the
cranium. The morphogenetic elds that were supposed originally in the eld theory
(Butler, 1939) could be interpreted to represent the concentration gradients of
morphogens, such as BMP4 and FGF8 (Armeld et al., 2013). If future studies identify a
metric that corresponds to the morphogen concentration gradient of the jaw, then it would
be possible to more rigorously test a correlation between the tooth complexity and the
dentition position relative to the morphogenetic elds in non-mammalian synapsids.
In the reconstructed evolutionary history, the dentition position showed a tendency to
be more posterior relative to the posterior end of maxilla (Fig. 6) and in the cranium
(Fig. 7) in non-therapsid synapsids compared with non-cynodont therapsids and early
Figure 7 (continued)
measurements are presented in Fig. 2. The statistics of the regression are given in Table S1d. The ancestral states reconstructed using parsimony
methods are indicated by the colors of the branches with numerical labels corresponding to each color. The open circles, open triangles, closed circle,
and closed triangle are as in Fig. 4. Additional details on the tree can be found in Fig. S5. The values of the ancestral states at each node can be found
in Table S5.Full-size
DOI: 10.7717/peerj.17784/g-7
Table 1 Estimates of phylogenetic generalized least squares (PGLS) models investigating the
relationship between tooth complexity and length to post-dentition when controlled for either the
length to ante-palatine, length to post-palatine, length to post-maxilla, or cranial length across
non-mammalian synapsids.
Explanatory variable Estimate SE t P
(a) Intercept 1.097 0.251 4.371 <0.001
Length to ante-palatine 0.902 0.057 15.819 <0.001
Tooth complexity 0.001 0.044 0.020 0.984
(b) Intercept 0.053 0.210 0.252 0.802
Length to post-palatine 0.988 0.037 26.938 <0.001
Tooth complexity 0.043 0.031 1.370 0.176
(c) Intercept 0.146 0.169 0.865 0.391
Length to post-maxilla 0.990 0.031 31.572 <0.001
Tooth complexity 0.068 0.025 2.699 0.009
(d) Intercept 0.941 0.217 4.328 <0.001
Cranial length 1.043 0.037 28.400 <0.001
Tooth complexity 0.069 0.029 2.372 0.021
Note:
(a) The length to post-dentition (log) was included as the response variable, while the tooth complexity level and the
length to ante-palatine (log) were included as explanatory variables (see Fig. 2 for denitions of positions and length
measurements). An estimated λof 0.527 was used in the PGLS model. (b) The length to post-dentition (log) was
included as response variable, while the tooth complexity level and the length to post-palatine (log) were included
as explanatory variables. An estimated λof 0.919 was used in the PGLS model. (c) The length to post-dentition
(log) was included as response variable, while the tooth complexity level and the length to post-maxilla (log) were
included as explanatory variables. An estimated λof 0.777 was used in the PGLS model. (d) The length to
post-dentition (log) was included as the response variable, while the tooth complexity level and the cranial length
(log) were included as explanatory variables. An estimated λof 0.839 was used in the PGLS model.
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 17/22
cynodonts. In contrast, the ancestral simplest tooth morphology was retained throughout
non-therapsid synapsids (Fig. 1). Therefore, the shifting of dentition position did not affect
tooth morphology in non-therapsid synapsids. Among the synapsid taxa included in this
study, teeth with multiple cusps (tooth complexity of level 2 or higher) were acquired
within the therapsid clade and evolution toward more complex teeth (tooth complexity of
level 3 or higher) occurred within the therocephalian and cynodont clades (Fig. 3). The
dentition position in the cranium appears to have shifted posteriorly during the evolution
from non-cynodont therapsids to Mammaliamorpha (Fig. 7). Changes in developmental
mechanisms that allow the morphogen concentration gradient to affect tooth morphology
may have occurred in early therapsids.
A posterior shift of the dentition position in the cranium brings the teeth closer to the
jaw joint, which increases the mechanical advantage by converting the force of the
masticatory muscle to a higher bite force (Greaves, 1978;Thomason, 1991). The dietary
habit of consuming mechanically resistant foods has been suggested to favor the evolution
of the molars closer to the jaw joint in carnivoran mammals (Harano & Asahara, 2022b).
Selection for improved ability to process foods may have caused the evolution of complex
teeth in correlation with a more posterior dentition position in non-mammalian synapsids.
Furthermore, this selection may have facilitated the evolution of the novel jaw joint
between the dentary and squamosal bones, which enables the precise occlusion between
the upper and lower teeth and thereby efcient mastication (Kemp, 2006;Tucker, 2017;
Navarro-Díaz, Esteve-Altava & Rasskin-Gutman, 2019).
CONCLUSIONS
The present study revealed that morphologically complex teeth evolved independently
multiple times and that the reversible evolution occurred in non-mammalian synapsids, as
is also found in mammals (Couzens, Sears & Rücklin, 2021;Harano & Asahara, 2022a).
Our analyses indicated suggestive evidence of a correlation between a more complex tooth
morphology and a more posterior dentition position relative to one of the three specic
bone locations used as reference points in the upper jaw across non-mammalian synapsids.
Furthermore, quantication of the dentition position in the cranium revealed similar
suggestive evidence. This nding provides conditional support for the hypothesis that a
posterior shift of the dentition position relative to the morphogenetic elds in the jaw has
contributed to the evolution of morphologically complex teeth in non-mammalian
synapsids. Future studies will need to more closely examine the developmental
mechanisms linking a posterior shift of the dentition and changes in tooth complexity
during evolution.
ACKNOWLEDGEMENTS
We thank Christian Kammerer and the anonymous reviewer for their valuable comments
on the manuscript.
Harano and Asahara (2024), PeerJ, DOI 10.7717/peerj.17784 18/22
ADDITIONAL INFORMATION AND DECLARATIONS
Funding
This work was supported by JSPS KAKENHI Grant Number JP 19H03290 to Masakazu
Asahara. The funders had no role in study design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Grant Disclosures
The following grant information was disclosed by the authors:
JSPS KAKENHI: JP 19H03290.
Competing Interests
The authors declare that they have no competing interests.
Author Contributions
.Tomohiro Harano conceived and designed the experiments, performed the experiments,
analyzed the data, prepared gures and/or tables, authored or reviewed drafts of the
article, and approved the nal draft.
.Masakazu Asahara conceived and designed the experiments, authored or reviewed drafts
of the article, and approved the nal draft.
Data Availability
The following information was supplied regarding data availability:
The measurement data is available in the Supplemental File.
Supplemental Information
Supplemental information for this article can be found online at http://dx.doi.org/10.7717/
peerj.17784#supplemental-information.
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