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Fossils reveal the complex evolutionary history of the mammalian regionalized spine

  • September 2018
  • Science 361(6408):1249-1252
DOI:10.1126/science.aar3126
Authors:
K. E. Jones
K. E. Jones
K. E. Jones
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K. D. Angielczyk
K. D. Angielczyk
K. D. Angielczyk
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Paul David Polly at Indiana University Bloomington
Paul David Polly
Jason J Head at University of Cambridge
Jason J Head
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Abstract and Figures

A unique characteristic of mammals is a vertebral column with anatomically distinct regions, but when and how this trait evolved remains unknown. We reconstructed vertebral regions and their morphological disparity in the extinct forerunners of mammals, the nonmammalian synapsids, to elucidate the evolution of mammalian axial differentiation. Mapping patterns of regionalization and disparity (heterogeneity) across amniotes reveals that both traits increased during synapsid evolution. However, the onset of regionalization predates increased heterogeneity. On the basis of inferred homology patterns, we propose a “pectoral-first” hypothesis for region acquisition, whereby evolutionary shifts in forelimb function in nonmammalian therapsids drove increasing vertebral modularity prior to differentiation of the vertebral column for specialized functions in mammals.
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MAMMALIAN EVOLUTION
Fossils reveal the complex
evolutionary history of the
mammalian regionalized spine
K. E. Jones
1
*, K. D. Angielczyk
2
, P. D. Polly
3
, J. J. Head
4
, V. Fernandez
5
,
J. K. Lungmus
6
, S. Tulga
7
, S. E. Pierce
1
*
A unique characteristic of mammals is a vertebral column with anatomically distinct regions,
but when and how this trait evolved remains unknown. We reconstructed vertebral regions
and their morphological disparity in the extinct forerunners of mammals, the nonmammalian
synapsids, to elucidate the evolution of mammalian axial differentiation. Mapping patterns
of regionalization and disparity (heterogeneity) across amniotes reveals that both traits
increased during synapsid evolution. However, the onset of regionalization predates increased
heterogeneity. On the basis of inferred homology patterns, we propose a “pectoral-first”
hypothesis for region acquisition, whereby evolutionary shifts in forelimb function in
nonmammalian therapsids drove increasing vertebral modularity prior to differentiation of
the vertebral column for specialized functions in mammals.
The evolution of the mammalian body plan
from the ancestral amniote condition is
one of the most iconic macroevolutionary
transitions in the vertebrate fossil record
(1,2). A unique feature of mammals is their
specialized vertebral column, which displays con-
strained vertebral counts but highly disparate
morphologies (2–4). In therian mammals, the
presacral vertebral column is traditionally divided
into cervical, rib-bearing thoracic, and ribless
lumbar regions (Fig. 1A). In contrast, the pre-
sacral vertebrae of basal amniotes are compar-
atively uniform and show little differentiation
(Fig.1B).Thetransitionfroman“unregionalized”
to a “regionalized”presacral column is an impor-
tant step in mammalian evolution and has been
linked to the origin of specialized gaits and
respiratory function (1,2,5,6).
Recent quantitative work has detected subtle
presacral regionalization in extant snakes and
limbed lizards, superficially unregionalized taxa
(7). It was hypothesized that the ancestral am-
niote condition is “cryptic regionalization,”in
which regions are present but are only subtly
expressed. The global-patterning Homeobox (Hox)
genes were implicated as underlying these con-
served regionalization patterns. Under this model,
thedegreeofregionalization—the number of re-
gions present—has remained constant through
mammalian evolution, whereas the amount of
morphological disparity between regions (here
termed heterogeneity) has increased. But this
evolutionary scenario is based solely on data
from extant species.
The two amniote clades—Synapsida (mammals
and their relatives) and Sauropsida (reptiles,
birds, and their relatives)—diverged more than
320 million years ago and have independently
undergone substantial morphological transforma-
tions. Therefore, to document the evolution of the
mammalian vertebral column, we must examine
mammals’extinct forerunners, the nonmamma-
lian synapsids. Here, we examined the presacral
vertebral columns of 16 exceptionally preserved
nonmammalian synapsids (including “pelycosaurs,”
basal therapsids, and cynodonts), one extinct
amniote outgroup, and a broad range of extant
salamanders, reptiles, and mammals. Using mor-
phometric data, we qua ntified patterns of region-
alization and heterogeneity and compared their
evolution to elucidate when and how synapsid
presacral differentiation occurred.
Using a likelihood-based segmented regression
approach, we calculated a regionalization score
for each taxon [an Akaike information criterion
(AIC)–weighted average of the relative fit of one-
to six-region hypotheses], producing a continu-
ousvariablethatreflectstheestimatednumber
of vertebral regions (fig. S2). Similar to prior
work (7), most reptiles and some extant mam-
mals (e.g., monotremes) have regionalization
scores indicating the presence of four regions
(Fig. 2A), whereas therians (marsupials and pla-
centals) most frequently display five regions.
Therian regionalization scores are also more
variable, probably reflecting high ecomorpho-
logical diversification of their axial system (4).
Thus, data from extant amniotes alone support
the null hypothesis of conserved regionalization.
However, both salamanders and basal synapsids
have lower regionalization scores than extant
amniotes (Fig. 2A, cool colors), which demon-
strates that regionalization increased indepen-
dently in the sauropsid and synapsid lineages.
Accordingly, we reject the hypothesis of con-
served regionalization patterns in amniotes, and
instead propose the hypothesis of increasing re-
gionalization in synapsid evolution.
Heterogeneity, expressed as the logarithm of
themeanvarianceofthemorphologicalmeasures
for each column, also increased during synapsid
evolution (Fig. 2B). Lepidosaurs and salaman-
ders have low heterogeneity, denoting relative
uniformity of the axial column; therians have
much higher values, reflecting their extreme
disparity; and crocodilians have intermediate
levels. Most nonmammalian synapsids also have
intermediate levels of heterogeneity. The out-
group Diadectes and the ophiacodontids display
particularly low values, reinforcing previous as-
sertions of homoplastic increases in mammals
and archosaurs from a homogeneous ancestral
condition (7). The cynodont Kayentatherium
has more heterogeneous morphologies than the
RESEARCH
Jones et al., Science 361, 1249–1252 (2018) 21 September 2018 1of4
1
Museum of Comparative Zoology and Department of
Organismic and Evolutionary Biology, Harvard University,
Cambridge, MA 02138, USA.
2
Integrative Research Center,
Field Museum of Natural History, Chicago, IL 60605, USA.
3
Department of Earth and Atmospheric Sciences, Indiana
University, Bloomington, IN 47405, USA.
4
Department of
Zoology and University Museum of Zoology, University of
Cambridge, Cambridge CB2 3EJ, UK.
5
European Synchrotron
Radiation Facility, 38000 Grenoble, France.
6
Department of
Organismal Biology and Anatomy, University of Chicago,
Chicago, IL 60637, USA.
7
Department of Geophysical
Sciences, University of Chicago, Chicago, IL 60637, USA.
*Corresponding author. Email: katrinajones@fas.harvard.edu
(K.E.J.); spierce@oeb.harvard.edu (S.E.P.)
0
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4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
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3 4 5 6 7 8 910111213141516171819202122232425
Angle of Zygapophyses
Angle of Zygapophyses
Cervical Thoracic Lumbar Cervical Dorsal
AB
Heterogeneity
Regionalization
Fig. 1. Regionalization and heterogeneity. (A) The therian presacral column is highly regionalized
and morphologically differentiated (Mus musculus). (B) Basal synapsids display a homogeneous
dorsal region with little differentiation (Ophiacodon).
on September 20, 2018 http://science.sciencemag.org/Downloaded from
other fossil taxa, reflecting its position close to
the mammal radiation. Given the association
between heterogeneity and functional special-
ization of the axial skeleton in therians, the
more homogeneous morphologies of most non-
mammalian synapsids point toward functional
conservatism.
Although regionalization and heterogeneity
increased during synapsid evolution, they are
not significantly related (fig. S7 and table S6,
P= 0. 73) , meaning that simple linear change is
insufficient to explain these patterns. Instead,
quantitative trait modeling supports evolution
toward shifting adaptive optima (multiple opti-
mum Ornstein-Uhlenbeck models) for these data
(table S7). On the basis of AIC fitting, we recon-
structed two major adaptive shifts in each trait
during synapsid evolution (Fig. 3 and fig. S8). The
adaptive optimum for regionalization increases
from around three regions in “pelycosaurs”to
around four regions at the base of Therapsida, with
a later shift to five regions occurring in Theria. The
adaptive optimum for heterogeneity increases first
at Cynodontia and subsequently within therians.
Taken together, our data reveal that vertebral
regionalization increased before heterogeneity
increased, hence these two measures of axial dif-
ferentiation evolved independently.
To understand how vertebral regionalization
increased in synapsids, we reconstructed region
boundaries recovered in the best-fit segmented
regression models (Fig. 4A). Region boundaries
were then cross-referenced with developmental
data, anatomical landmarks, and variation in
extant species to identify homologies (Fig. 4B).
In extant tetrapods, the cervicothoracic transi-
tion is correlated with Hox6 expression, rib mor-
phology, and the position of the forelimb and
brachial plexus (8). Therefore, the cervicothoracic
boundary was identified by (i) the position of the
posterior branch of the brachial plexus, and
(ii) the location of the anterior sternal articulation
or first long rib. Functional studies in Mus also
show that Hox9 patterns the transition from
sternal to nonarticulating ribs and that Hox10
controls the suppression of ribs altogether in
the lumbar region (Fig. 4B) (9,10). In keeping
with this association, dorsal regions were defined
relative to their proximity to long ribs (anterior
dorsal), short ribs (posterior dorsal), or absent
ribs (lumbar).
Using these criteria, region homology hypothe-
ses were constructed in key taxa for which rib
or neural anatomy are known (Fig. 4B). In sal-
amanders (and the stem amniote Diadectes;see
supplementary text), three regions are recovered.
The anterior break correlates with the posterior
branch of the brachial plexus in Ambystoma,im-
plying homology with the cervical region despite
the lack of a true “neck”(Fig. 4B, red region). Al-
though salamanders have poorly developed ribs,
the position of the posterior break in the mid-
trunk is consistent with the anterior-posterior
dorsal transition in other taxa (Fig. 4, yellow and
pale blue regions). This ancestral three-region
pattern is retained in the most basal synapsids.
In “pelycosaurs,”the first break corresponds
to the inferred cervicothoracic transition based
on rib length and forelimb position (e.g., v5 in
Edaphosaurus,v7inDimetrodon), whereas the
second break corresponds to the gradual tran-
sition from longer to shorter dorsal ribs, signifying
cervical, anterior dorsal, and posterior dorsal
homologies (Edaphosaurus;Fig.4B).
Our data point to the convergent addition of a
fourth region in distinct locations in sauropsids
and synapsids. In sauropsids, a fourth region is
detected anterior to the brachial plexus, suggest-
ing a novel cranial region within the neck (Iguana;
Fig. 4B, purple region). Sauropsids exhibit more
variationincervicalcountthandosynapsids(11),
providing a potential connection between neck
plasticity and cervical modularity in this lineage.
Conversely, in basal therapsids and cynodonts,
afourth region is detected posterior to the cer-
vicothoracic transition (Thrinaxodon; Fig. 4B,
orange region). In Thrinaxodon, the first break
corresponds to the cervicothoracic transition
and first full-length rib (v7–8), the second break
liesinthemiddleofthelongribseries(v12–13),
and the anterior-posterior dorsal boundary falls
at the transition from long to short ribs (v19–20).
These regions conform to the ancestral cervi-
cal region (red), a novel pectoral region (orange),
and the ancestral anterior dorsal (yellow) and
posterior dorsal (pale blue) regions. Therian
mammals display an additional break within the
posterior dorsal region that differentiates the
ribless lumbar region (Mus;Fig.4B,blueregion).
Considering the pattern ofregionacquisition,
we propose a “pectoral-first”hypothesis for the
evolution of mammalian presacral regionaliza-
tion (Fig. 4). Under this hypothesis, “pelycosaurs”
retained the three-region ancestral amniote con-
dition. In basal therapsids, addition of a fourth
“pectoral module”accompanied the reorganiza-
tion of the pectoral girdle and forelimb. Unlike
Jones et al., Science 361, 1249–1252 (2018) 21 September 2018 2of4
Time (Ma)
-5
Time (Ma)
Amniota
Mammalia
'Pelycosaurs'
Therapsida
Cynodontia
AB
-5 1
35
1
Heterogeneity
Regionalization
35
Fig. 2. Evolution of presacral differentiation in amniotes. (A) Regionalization score. (B) Heteroge-
neity [log(mean variance)]. Warmer colors reflect more regions and greater morphological heterogeneity,
respectively. Black circles, mammals; gray circles, fossil taxa; triangles, reptiles; stars, amphibians;
grayed tips in (A), fossil taxa excluded because of <0.75 r
2
of regionalization model. See table S5 for
full taxonomic names. Ma, millions of years.
RESEARCH |REPORT
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“pelycosaurs,”therapsids are characterized by
reduction of the pectoral girdle dermal bones
and increased shoulder mobility (1,12). Medial
extrinsic shoulder muscles (e.g., levator scapulae,
serratus ventralis) originating on the scapula
are thought to have expanded their axial inser-
tions during synapsid evolution (12). As these
vital body-support muscles attach directly onto
the underlying vertebrae and ribs, shifts in pec-
toral morphology and function likely drove di-
vergent neck- and shoulder-selective regimes
in the axial skeleton, providing impetus for in-
creased regionalization (1,12,13). Further, the
vertebrae, medial extrinsic shoulder muscles,
and dorsal border of the scapula all develop
directly from somitic mesoderm (primaxial),
signifying strong developmental ties between
these structures (14).
It has been proposed that the muscular dia-
phragm evolved from an unmuscularized septum
or “proto-diaphragm”via co-option of shoulder
muscle precursor cells that were later canalized
into a distinct cell population by repatterning of
the posterior neck (15). Reorganization of the
anterior column and pectoral girdle in therapsids
may have facilitated this transition by increas-
ing cervicothoracic modularity and remodeling
shoulder musculature. Subsequent fixation of
the cervical count at seven in nonmammalian
cynodontsishypothesizedtorepresenttheap-
pearance of the mammalian-style muscular dia-
phragm (6). Thus, anterior regionalization that
had initially been associated with shoulder evo-
lution in early therapsids was likely later exapted
in cynodonts in response to selection for in-
creased ventilatory efficiency (5,15).
A“lumbar module”evolved later in therian
mammals. Evolution of the lumbar region in
mammals is associated with Hox10,whichfunc-
tions to repress rib formation and patterns lum-
bar identity in Mus (10) (Fig. 4B). Convergent
loss or gain of lumbar ribs in multiple fossil
theriiform clades suggests high plasticity of this
character early in therian evolution (16). Within
therians, lumbar count and morphology vary,
and this is reflected by translocation of the (mor-
phometrically defined) region boundary in our
sample. Because the lumbar region plays a crit-
ical role in mammalian locomotion, it is predicted
that region variability is related to ecological
specialization caused by clade-specific function-
al overprinting.
Regional differentiation is “the major structural
difference between reptilian and mammalian
vertebral columns”(13), yet its evolution has never
been quantitatively examined. Our findings show
that regionalization and heterogeneity—the two
aspects of vertebral differentiation—evolved
independently. Forelimb reorganization in the-
rapsids drove initial increases in regionalizatio n
as a result of developmental and functional
connections between the pectoral girdle and
underlying vertebrae. High heterogeneity and
presumed functional diversity did not appear
until crown mammals. The combination of a
regionalized axial skeleton with heterogeneous
vertebral morphologies ultimately enabled mam-
mals to become specialized for a remarkable di-
versity of ecologies and behaviors.
Jones et al., Science 361, 1249–1252 (2018) 21 September 2018 3of4
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Amniota
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therapsid 'Pelycosaur' Sauropsid
4.38
Synapsida
Therapsida Theria
Ambystoma
Diadectes
Alligator
Sphenodon
Gekko
Varanosaurus
Ophiacodon
Edaphosaurus
Edaphosaurus
Dimetrodon
Sphenacodon
Ctenorachis
Hipposaurus
Eosimops
Lystrosaurus
Dicynodon
Scalaposaurus
Procynosuchus
Thrinaxodon
Massetognathus
Kayentatherium
Zaglossus
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Mus
0100
Fig. 4. Best-fit region models, region homologies, and evolutionary hypothesis. (A) Best-fit
region models for select taxa. Colors represent inferred region homologies; St. Dev., standard
deviation of break locations; PS count, presacral count; R-sq, adjusted r
2
; % complete, total
completeness; shaded region models reflect taxa with <0.75 r
2
fit (excluded from evolutionary
reconstructions). (B)“Pectoral-first”hypothesis for the evolution of synapsid presacral region-
alization. Taxa (left to right): Ambystoma,Iguana,Edaphosaurus [redrawn from (17)], Thrinaxodon
[redrawn from (2)], Mus. Width of gray bars reflects relative rib lengths and/or connection to
sternum; vertical dashed lines denote cervicothoracic transition. For Mus, Hox bands correspond to
vertebrae affected by functional gene manipulation (18).
Region score
Log Variance
Time (Ma)
θ: -3.94
θ: -1.57
θ: -0.48
Therapsida
Theria
Cynodontia
Boreoeutheria
θ: 3.01
θ: 3.89
θ: 4.80
Pz T JKCz
Regionalization
Heterogeneity
A
B
Fig. 3. Adaptive regime shifts in vertebral
evolution. (A) Regionalization. (B) Heterogene-
ity. Theta denotes adaptive optima of each
regime. Pz, Paleozoic; T, Triassic; J, Jurassic;
K, Cretaceous; Cz, Cenozoic.
RESEARCH |REPORT
on September 20, 2018 http://science.sciencemag.org/Downloaded from
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ACKNOW LEDGMEN TS
We thank R. Asher, B. Brainerd, D. Brinkman, T. Capellini,
C. Capobianco, J. Chupasko, J. Cundiff, K. Jakata, T. Kemp,
C. Mehling, A. Millhouse, M. Omura, A. Resetar, J. Rosado,
B. Rubidge, R. Smith, K. Smithson, C. Tabin, R. Tykoski, I. Werneburg,
and B. Zipfel.Funding: Supported by NSF grants EAR-1524523
(S.E.P.) and EAR-1524938 (K.D.A.) and by an AAA Postdoctoral
Fellowship (K.E.J.). Author contributions: Study design, K.E.J.,
K.D.A., and S.E.P.; methods, K.E.J., P.D.P., and S.E.P.; data
collection, K.E.J., K.D.A., S.E.P., J.J.H., V.F., J.K.L., and S.T.; data
analysis, K.E.J.; manuscript preparation, K.E.J., K.D.A., and S.E.P.
Competing interests: The authors have no competing interests. Data
and materials availability: Data are available in table S5 and Dryad
(doi:10.5061/dryad.jm820mg). Code is available via github (https://
github.com/katrinajones/regions).
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/361/6408/1249/suppl/DC1
Materials and Methods
Supplementary Text
Figs. S1 to S8
Tables S1 to S7
References (19–49)
30 October 2017; resubmitted 27 April 2018
Accepted 25 July 2018
10.1126/science.aar3126
Jones et al., Science 361, 1249–1252 (2018) 21 September 2018 4of4
RESEARCH |REPORT
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... Although their cranial osteology has been relatively well documented (e.g., Bardua et al., 2019;Lowie et al., 2021;Sherratt et al., 2014;Wake, 1993;Wilkinson & Nussbaum, 1997), few studies have focused on the vertebral morphology of adult extant caecilians (e.g., Peter, 1894;Renous et al., 1993;Renous & Gasc, 1989;Taylor, 1977;Wake, 1980;Wiedersheim, 1879). In general, vertebrate axial skeletons are not a homogenous series of vertebrae and two types of morphological variation have been documented in previous studies: regionalization and heterogeneity (Jones et al., 2018). Whereas regionalization defines the number of regions along the vertebral column and relies on the expression of Homeobox genes (Head & Polly, 2015), heterogeneity defines the degree of morphological disparity observed among regions (Jones et al., 2018). ...
... In general, vertebrate axial skeletons are not a homogenous series of vertebrae and two types of morphological variation have been documented in previous studies: regionalization and heterogeneity (Jones et al., 2018). Whereas regionalization defines the number of regions along the vertebral column and relies on the expression of Homeobox genes (Head & Polly, 2015), heterogeneity defines the degree of morphological disparity observed among regions (Jones et al., 2018). Although these two types of axial differentiation evolve independently, both increased during synapsid evolution and led to well-defined vertebral regions in mammals (Jones et al., 2018). ...
... Whereas regionalization defines the number of regions along the vertebral column and relies on the expression of Homeobox genes (Head & Polly, 2015), heterogeneity defines the degree of morphological disparity observed among regions (Jones et al., 2018). Although these two types of axial differentiation evolve independently, both increased during synapsid evolution and led to well-defined vertebral regions in mammals (Jones et al., 2018). This combination of morphologically specialized vertebrae and regionalization allowed mammals to become functionally specialized for locomotion (Jones et al., 2020). ...
Regional differences in vertebral shape along the axial skeleton in caecilians (Amphibia: Gymnophiona)
Article
  • Apr 2022
Caecilians are elongate, limbless and annulated amphibians that, as far as is known, all have an at least partly fossorial lifestyle. It has been suggested that elongate limbless vertebrates show little morphological differentiation throughout the postcranial skeleton. However, relatively few studies have explored the axial skeleton in limbless tetrapods. In this study, we used μCT data and three‐dimensional geometric morphometrics to explore regional differences in vertebral shape across a broad range of caecilian species. Our results highlight substantial differences in vertebral shape along the axial skeleton, with anterior vertebrae being short and bulky, whereas posterior vertebrae are more elongated. This study shows that despite being limbless, elongate tetrapods such as caecilians still show regional heterogeneity in the shape of individual vertebrae along the vertebral column. Further studies are needed, however, to understand the possible causes and functional consequences of the observed variation in vertebral shape in caecilians. It has been suggested that elongate limbless vertebrates show little morphological differentiation throughout the postcranial skeleton. However, our results show that, far from morphologically homogeneous, the post‐cranial skeleton of caecilians shows variations in vertebral shape. Whereas the anterior part of the body consists of short, bulky vertebrae, posterior vertebrae is elongated with pronounced basapophyseal processes.
... Analyses so far have been conducted at various phylogenetic scales, including in larger analyses of tetrapod evolution that contain a more limited sampling of early amniotes (e.g., Laurin 2004;Ruta et al. 2006Ruta et al. , 2018Anderson et al. 2013), as well as restricted examinations of early amniote subgroups (Brocklehurst 2016(Brocklehurst , 2017Brocklehurst and Brink 2017;Romano et al. 2017Romano et al. , 2018MacDougall et al. 2019). Studies have also focused on different portions of the anatomy, including limbs (Ruta et al. 2018), jaws and teeth (Anderson and Friedman 2013;, vertebrae (Jones et al. 2018(Jones et al. , 2021, and body size (Laurin 2004). However, thus far there has been no study of macroevolutionary patterns during the origin and early radiation of amniotes including a broad selection of all clades, allowing direct comparison of the evolutionary patterns within the major lineages, and across many anatomical regions. ...
... In contrast, early synapsid postcrania evolved at lower rates for much of the Carboniferous and early Permian, but under significantly relaxed constraints that allowed them to gradually explore a much larger character state space. Our findings are therefore potentially consistent with the limited previous studies of synapsid postcranial variation, which found evidence for the high disparity of humerus shape and heterogeneity between vertebral regions in therapsids (Jones et al. 2018;Lungmus and Angielczyk 2021). ...
... Relaxation of postcranial evolution is shown here among early synapsids (Fig. 4). This is congruent with considerable variation in the postcranial morphology of modern mammals and their therapsid ancestors, including greater variability and distinction between modules in the vertebral column in mammals compared with reptiles (Arnold et al. 2017;Jones et al. 2018;Arnold 2021) and considerable increases in synapsid humeral disparity from the middle Permian onwards (Lungmus and Angielczyk 2021). Our findings, therefore, suggest that an initial release in postcranial evolution occurred at the origin of synapsids, with subsequent increases occurring in therapsids and among mammals (Jones et al. 2018;Lungmus and Angielczyk 2021). ...
Early origins of divergent patterns of morphological evolution on the mammal and reptile stem-lineages
Article
Full-text available
The origin of amniotes 320 million years ago signalled independence from water in vertebrates and was closely followed by divergences within the mammal and reptile stem lineages (Synapsida and Reptilia). Early members of both groups had highly similar morphologies, being superficially 'lizard-like' forms with many plesiomorphies. However, the extent to which they might have exhibited divergent patterns of evolutionary change, with potential to explain the large biological differences between their living members, is unresolved. We use a new, comprehensive phylogenetic dataset to quantify variation in rates and constraints of morphological evolution among Carboniferous-early Permian amniotes. We find evidence for an early burst of evolutionary rates, resulting in the early origins of morphologically distinctive subgroups that mostly persisted through the Cisuralian. Rates declined substantially through time, especially in reptiles. Early reptile evolution was also more constrained compared to early synapsids, exploring a more limited character state space. Postcranial innovation in particular was important in early synapsids, potentially related to their early origins of large body size. In contrast, early reptiles predominantly varied the temporal region, suggesting disparity in skull and jaw kinematics, and foreshadowing the variability of cranial biomechanics seen in reptiles today. Our results demonstrate that synapsids and reptiles underwent an early divergence of macroevolutionary patterns. This laid the foundation for subsequent evolutionary events and may be critical in understanding the substantial differences between mammals and reptiles today. Potential explanations include an early divergence of developmental processes or of ecological factors, warranting cross-disciplinary investigation.
... hox genes j regionalization j chondrichthyan j vertebral column T he axial skeleton (vertebrae and ribs) is a defining feature of the vertebrate body form, and the existence of distinct axial skeletal regions along the anteroposterior (AP) axis of the body is thought to have facilitated evolutionary radiations and ecological specializations across vertebrate phylogeny (1)(2)(3). Tetrapod vertebral columns include at least four axial regions: cervical, trunk (further divided into thoracic and lumbar in most mammals and some reptiles), sacral, and caudal, the lengths of which have been modified in different tetrapod groups to suit various ecologies and lifestyles. In mammals and birds, vertebral regions are patterned by Hox gene expression within the paraxial mesoderm, and experimental manipulations to anterior Hox expression boundaries result in corresponding shifts in vertebral regional boundaries (4)(5)(6)(7)(8). ...
... We quantified vertebral morphology as homologous landmarks represented by three-dimensional (3D) Cartesian grid coordinates ( Fig. 1B and SI Appendix, Table S1) and used principal-component (PC) scores of realigned landmark coordinates as shape variables. To test for region numbers and boundaries, we performed segmented linear regression on PC scores and used maximum-likelihood model selection to determine the best fit number of regions within the quantified axial skeleton, where individual regression slopes indicate regions and slope breaks represent region boundaries (SI Appendix, Fig. S1 and Table S2) (3,38). PC analysis revealed a shape gradient along the AP axis of the vertebral column in the skate ( Fig. 1C and SI Appendix, Fig. S1 A-C), with a four-region model having the best fit to the gradient, and an overall best model of five regions with boundaries at approximately vertebrae 26, 31, 46, and 51 when we included the synarcual as the first region ( Fig. 1 D and E and SI Appendix, Fig. S1 A 0 -C 0 and D and Table S2). ...
... While the tail region of the skate axial column is easily recognizable by the change in morphology from laterally projecting transverse processes to ventrally directed hemal arches, the more rostral vertebral regions vary more subtly in morphology. The morphometric approaches used here have recently resolved cryptic anatomical boundaries in the vertebral skeletons of tetrapod taxa previously thought to have lost axial regionalization (38), and have allowed for finer-scale resolution of regional boundaries in fossil lineages (3). If applied more widely, comparative morphometric approaches can help to detect cryptic regionalization in a much broader array of taxa, providing a more comprehensive picture of the evolutionary history of axial regionalization. ...
hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea
Article
Full-text available
  • Dec 2021
The axial skeleton of tetrapods is organized into distinct anteroposterior regions of the vertebral column (cervical, trunk, sacral, and caudal), and transitions between these regions are determined by colinear anterior expression boundaries of Hox5/6 , -9 , -10 , and -11 paralogy group genes within embryonic paraxial mesoderm. Fishes, conversely, exhibit little in the way of discrete axial regionalization, and this has led to scenarios of an origin of Hox -mediated axial skeletal complexity with the evolutionary transition to land in tetrapods. Here, combining geometric morphometric analysis of vertebral column morphology with cell lineage tracing of hox gene expression boundaries in developing embryos, we recover evidence of at least five distinct regions in the vertebral skeleton of a cartilaginous fish, the little skate ( Leucoraja erinacea ). We find that skate embryos exhibit tetrapod-like anteroposterior nesting of hox gene expression in their paraxial mesoderm, and we show that anterior expression boundaries of hox5/6 , hox9 , hox10 , and hox11 paralogy group genes predict regional transitions in the differentiated skate axial skeleton. Our findings suggest that hox- based axial skeletal regionalization did not originate with tetrapods but rather has a much deeper evolutionary history than was previously appreciated.
... To test whether there were any differences in wholehindlimb muscle architecture among species, we first performed a principal coordinate analysis (PCO) on the entire dataset using the 'regions' package (Jones et al. 2018) in R (R Core Team 2021); PCO is a distance-based ordination that allows for missing data in the distance matrix. We then performed a non-parametric multivariate analysis of variance (MANOVA) on the PCO axes that individually explained at least 3% of the variance (5 axes) in the dataset with species as the grouping factor. ...
Comparison of Hindlimb Muscle Architecture Properties in Small-Bodied, Generalist Mammals Suggests Similarity in Soft Tissue Anatomy
Article
Full-text available
For the first 100+ million years of their evolutionary history, the majority of mammals were very small, and many exhibited relatively generalized locomotor ecologies. Among extant mammals, small-bodied, generalist species share similar hindlimb bone morphology and locomotor mechanics, but details of their musculature have not been investigated. To examine whether hindlimb muscle architecture properties are also similar, we dissected hindlimb muscles of the gray short-tailed opossum (Monodelphis domestica) and aggregated muscle properties from the literature for three other small-bodied mammals (Mus musculus, Rattus norvegicus, Cavia porcellus). We then studied hindlimb musculature from a whole-limb perspective and by separating the limb into nine anatomical regions. The region analysis explained substantially more variance in the data (r²: 0.601 > 0.074) but only detected six statistically significant pairwise species differences in muscle architecture properties. This finding suggests either deep conservation of therian hindlimb muscle properties or, more likely, a biomechanical constraint imposed by small body size. In addition, we find specialization for either large force production (i.e., PCSA) or longer active working ranges (i.e. long muscle fascicles) in proximal limb regions but neither specialization in more distal limb regions. This functional pattern may be key for small mammals to traverse across uneven and shifting substrates, regardless of environment. These findings are particularly relevant for researchers seeking to reconstruct and model soft tissue properties of extinct mammals during the early evolutionary history of the clade.
A Shrewd Inspection of Vertebral Regionalization in Large Shrews (Soricidae: Crocidurinae)
Article
Full-text available
  • Feb 2022
The regionalization of the mammalian spinal column is an important evolutionary, developmental, and functional hallmark of the clade. Vertebral column regions are usually defined using transitions in external bone morphology, such as the presence of transverse foraminae or rib facets, or measurements of vertebral shape. Yet the internal structure of vertebrae, specifically the trabecular (spongy) bone, plays an important role in vertebral function, and is subject to the same variety of selective, functional, and developmental influences as external bone morphology. Here we investigated regionalization of external and trabecular bone morphology in the vertebral column of a group of shrews (family Soricidae). The primary goals of this study were to: 1) determine if vertebral trabecular bone morphology is regionalized in large shrews, and if so, in what configuration relative to external morphology; 2) assess correlations between trabecular bone regionalization and functional or developmental influences; and 3) determine if external and trabecular bone regionalization patterns provide clues about the function of the highly modified spinal column of the hero shrew Scutisorex. Trabecular bone is regionalized along the soricid vertebral column, but the configuration of trabecular bone regions does not match that of the external vertebral morphology, and is less consistent across individuals and species. The cervical region has the most distinct and consistent trabecular bone morphology, with dense trabeculae indicative of the ability to withstand forces in a variety of directions. Scutisorex exhibits an additional external morphology region compared to unmodified shrews, but this region does not correspond to a change in trabecular architecture. Although trabecular bone architecture is regionalized along the soricid vertebral column, and this regionalization is potentially related to bone functional adaptation, there are likely aspects of vertebral functional regionalization that are not detectable using trabecular bone morphology. For example, the external morphology of the Scutisorex lumbar spine shows signs of an extra functional region that is not apparent in trabecular bone analyses. It is possible that body size and locomotor mode affect the degree to which function is manifest in trabecular bone, and broader study across mammalian size and ecology is warranted to understand the relationship between trabecular bone morphology and other measures of vertebral function such as intervertebral range of motion.
On the covariance of phylogenetic quantitative trait evolution models and their matrix condition
Article
  • Feb 2022
Size and shape regional differentiation during the development of the spine in the nine‐banded armadillo (Dasypus novemcinctus)
Article
  • Nov 2021
Xenarthrans (armadillos, anteaters, sloths, and their extinct relatives) are unique among mammals in displaying a distinctive specialization of the posterior trunk vertebrae—supernumerary vertebral xenarthrous articulations. This study seeks to understand how xenarthry develops through ontogeny and if it may be constrained to appear within pre-existing vertebral regions. Using three-dimensional geometric morphometrics on the neural arches of vertebrae, we explore phenotypic, allometric, and disparity patterns of the different axial morphotypes during the ontogeny of nine-banded armadillos. Shape-based regionalization analyses showed that the adult thoracolumbar column is divided into three regions according to the presence or absence of ribs and the presence or absence of xenarthrous articulations. A three-region division was retrieved in almost all specimens through development, although younger stages (e.g., fetuses, neonates) have more region boundary variability. In size-based regionalization analyses, thoracolumbar vertebrae are separated into two regions: a prediaphragmatic, prexenarthrous region, and a postdiaphragmatic xenarthrous region. We show that posterior thoracic vertebrae grow at a slower rate, while anterior thoracics and lumbars grow at a faster rate relatively, with rates decreasing anteroposteriorly in the former and increasing anteroposteriorly in the latter. We propose that different proportions between vertebrae and vertebral regions might result from differences in growth pattern and timing of ossification. Highlights Xenarthrans are unique vertebral xenarthrous articulations. We use three-dimensional geometric morphometrics to explore phenotypic, allometric, and disparity patterns of vertebrae through development, and characterize vertebral regions of the xenarthran spine and how they develop.
Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region
Article
The salamander vertebral column is largely undifferentiated, with a series of more or less uniform rib-bearing presacral vertebrae traditionally designated as the trunk region. We explored regionalisation of the salamander trunk in seven species and two subspecies of the salamander genus Lissotriton by the combination of micro computed tomography scanning and geometric morphometrics. The detailed information on trunk vertebral shape was subjected to a multidimensional cluster analysis and a phenotypic trajectory analysis. With these complementary approaches, we observed a clear morphological regionalization. Clustering analysis showed that the anterior trunk vertebrae (T1 and T2) have distinct morphologies that are shared by all taxa, whereas the subsequent, more posterior vertebrae show significant disparity between species. The phenotypic trajectory analysis revealed that all taxa share a common pattern and amount of shape change along the trunk region. Altogether, our results support the hypothesis of a conserved anterior-posterior developmental patterning which can be associated with different functional demands, reflecting (sub) species’ and possibly, regional ecological divergences within species. Keywords: Geometric morphometrics; Lissotriton; High-dimensional clustering analysis; Micro computed tomography; Phenotypic trajectory analysis; Trunk vertebrae; Regionalization.
Plasticité développementale des voies vestibulo-spinales lors de la métamorphose du xénope (xenopus laevis) : aspects anatomiques et fonctionnels
Thesis
  • Sep 2021
Chez les vertébrés, les voies vestibulo-spinales génèrent des commandes motrices spinales à l’origine des réflexes vestibulo-spinaux responsables de la stabilisation du corps dans l’espace lors des mouvements passifs et actifs de la tête. Cette thèse étudie l’organisation morpho-fonctionnelle des voies vestibulo-spinales impliquées dans le contrôle postural chez le xénope (xenopus laevis), un amphibien anoure exclusivement aquatique possédant un système vestibulaire bien conservé et similaire à celui des vertébrés supérieurs. Ce travail a été mené avec une approche multi-méthodologique, combinant neuroanatomie et électrophysiologie intra- et extracellulaire afin de caractériser les propriétés neuronales et l’organisation des réseaux et des réflexes vestibulo-spinaux. Au cours de la métamorphose, la réorganisation complète du système posturo-locomoteur, passant d’un système axial-ondulatoire chez la larve à un système appendiculaire chez l’adulte, implique l’adaptation anatomo-fonctionnelle de ces voies vestibulo-motrices. Chez le xénope adulte, une partie des muscles dorsaux (dorsalis trunci), innervés par les motoneurones thoraciques, sont uniquement posturaux, contrairement à la grande majorité des vertébrés où les muscles posturaux interviennent aussi dans la propulsion. Par conséquent, ce modèle amphibien permet d’isoler la composante posturale dans le contrôle vestibulaire du comportement posturo-locomoteur. Dans la première partie de ma thèse, j’ai démontré l’existence d’une double commande vestibulaire convergeant sur les motoneurones thoraciques qui innervent les muscles dorsaux posturaux, au repos. Une première voie vestibulaire directe, mettant en jeu des projections descendantes bilatérales en provenance des noyaux vestibulaires centraux (LVST et du noyau tangentiel). Cette première commande vestibulaire semble être responsable d’ajustements posturaux du tronc, en réponse au signal de position de la tête. La seconde voie vestibulo-spinale, indirecte, mettant en jeu un relais ascendant lombo-thoracique, assure la coordination des réseaux moteurs thoraco-lombaires dans le réflexe postural en réponse au signal de vitesse de la tête. Chez la larve, des données préliminaires suggèrent l’existence de connexions vestibulo-spinales fonctionnelles avec les motoneurones axiaux rostraux, dont les motoneurones thoraciques adulte dérivent partiellement, et caudaux qui disparaissent pendant la métamorphose. En parallèle de l’organisation des réseaux, l’enregistrement intracellulaire (patch-clamp) des neurones vestibulo-spinaux et plus particulièrement ceux du LVST sur une préparation de coupe de tronc cérébral a permis de mettre en évidence trois phénotypes électrophysiologiques distincts : phasique, tonique et intermédiaire. Pendant la métamorphose, la proportion entre neurones tonique et phasique s’inverse, allant d’une majorité de neurones toniques chez la larve à une majorité de neurones phasiques chez l’adulte. De plus, l’expression d’une conductance potassique ID, portée par les sous-unités Kv1.1 semble jouer un rôle important dans l’établissement des phénotypes phasiques et intermédiaires. Ces résultats nous permettent d’établir un lien entre l’expression des phénotypes neuronaux spécifiques à la dynamique des réflexes vestibulo-spinaux qu’ils produisent, en relation avec les différents comportements posturo-locomoteurs de nage exprimés entre ces deux stades. Mon travail de thèse a permis d’imaginer les études en cours qui étudient plus en détail la maturation des voies vestibulo-spinales, au cours de la métamorphose, en termes de plasticité cellulaire, de réorganisation des circuits et d’adaptation des réflexes posturaux.
Regionalization, constraints, and the ancestral ossification patterns in the vertebral column of amniotes
Preprint
Full-text available
  • Sep 2021
The development of the vertebral column has been studied extensively in modern amniotes, yet many aspects of its evolutionary history remain enigmatic. Here we expand the existing data on four major vertebral developmental patterns in amniotes based on exceptionally well-preserved specimens of the early Permian mesosaurid reptile Stereosternum: (i) centrum ossification, (ii) neural arch ossification, (iii) neural arch fusion, and (iv) neurocentral fusion. We retrace the evolutionary history of each pattern and reconstruct the ancestral condition in amniotes. Despite 300 million years of evolutionary history, vertebral development patterns show a surprisingly stability in amniotes since their common ancestor. We propose that this conservatism may be linked to constraints posed by underlying developmental processes across amniotes. However, we also point out that mammals and birds differ more strongly from the ancestral condition than other clades, which might be linked to a stronger regionalization of the column in these two clades.
Hox genes and the evolution of vertebrate axial morphology
Article
Full-text available
  • Feb 1995
A common form of evolutionary variation between vertebrate taxa is the different numbers of segments that contribute to various regions of the anterior-posterior axis; cervical vertebrae, thoracic vertebrae, etc. The term ‘transposition’ is used to describe this phenomenon. Genetic experiments with homeotic genes in mice have demonstrated that Hox genes are in part responsible for the specification of segmental identity along the anterior-posterior axis, and it has been proposed that an axial Hox code determines the morphology of individual vertebrae (Kessel, M. and Gruss, P. (1990) Science 249, 347–379). This paper presents a comparative study of the developmental patterns of homeobox gene expression and developmental morphology between animals that have homologous regulatory genes but different morphologies. The axial expression boundaries of 23 Hox genes were examined in the paraxial mesoderm of chick, and 16 in mouse embryos by in situ hybridization and immunolocalization techniques. Hox gene anterior expression boundaries were found to be transposed in concert with morphological boundaries. This data contributes a mechanistic level to the assumed homology of these regions in vertebrates. The recognition of mechanistic homology supports the historical homology of basic patterning mechanisms between all organisms that share these genes.
A cautionary note on the use of Ornstein Uhlenbeck models in macroevolutionary studies
Article
Full-text available
Phylogenetic comparative methods are increasingly used to give new insights into the dynamics of trait evolution in deep time. For continuous traits the core of these methods is a suite of models that attempt to capture evolutionary patterns by extending the Brownian constant variance model. However, the properties of these models are often poorly understood, which can lead to the misinterpretation of results. Here we focus on one of these models - the Ornstein Uhlenbeck (OU) model. We show that the OU model is frequently incorrectly favoured over simpler models when using Likelihood ratio tests, and that many studies fitting this model use datasets that are small and prone to this problem. We also show that very small amounts of error in datasets can have profound effects on the inferences derived from OU models. Our results suggest that simulating fitted models and comparing with empirical results is critical when fitting OU and other extensions of the Brownian model. We conclude by making recommendations for best practice in fitting OU models in phylogenetic comparative analyses, and for interpreting the parameters of the OU model.
Evolution of the snake body form reveals homoplasy in amniote Hox gene function
Article
Full-text available
Hox genes regulate regionalization of the axial skeleton in vertebrates, and changes in their expression have been proposed to be a fundamental mechanism driving the evolution of new body forms. The origin of the snake-like body form, with its deregionalized pre-cloacal axial skeleton, has been explained as either homogenization of Hox gene expression domains, or retention of standard vertebrate Hox domains with alteration of downstream expression that suppresses development of distinct regions. Both models assume a highly regionalized ancestor, but the extent of deregionalization of the primaxial domain (vertebrae, dorsal ribs) of the skeleton in snake-like body forms has never been analysed. Here we combine geometric morphometrics and maximum-likelihood analysis to show that the pre-cloacal primaxial domain of elongate, limb-reduced lizards and snakes is not deregionalized compared with limbed taxa, and that the phylogenetic structure of primaxial morphology in reptiles does not support a loss of regionalization in the evolution of snakes. We demonstrate that morphometric regional boundaries correspond to mapped gene expression domains in snakes, suggesting that their primaxial domain is patterned by a normally functional Hox code. Comparison of primaxial osteology in fossil and modern amniotes with Hox gene distributions within Amniota indicates that a functional, sequentially expressed Hox code patterned a subtle morphological gradient along the anterior-posterior axis in stem members of amniote clades and extant lizards, including snakes. The highly regionalized skeletons of extant archosaurs and mammals result from independent evolution in the Hox code and do not represent ancestral conditions for clades with snake-like body forms. The developmental origin of snakes is best explained by decoupling of the primaxial and abaxial domains and by increases in somite number, not by changes in the function of primaxial Hox genes.
A Novel Bayesian Method for Inferring and Interpreting the Dynamics of Adaptive Landscapes from Phylogenetic Comparative Data
Article
Full-text available
  • Jul 2014
Our understanding of macroevolutionary patterns of adaptive evolution has greatly increased with the advent of large-scale phylogenetic comparative methods. Widely used Ornstein–Uhlenbeck (OU) models can describe an adaptive process of divergence and selection. However, inference of the dynamics of adaptive landscapes from comparative data is complicated by interpretational difficulties, lack of identifiability among parameter values and the common requirement that adaptive hypotheses must be assigned a priori. Here, we develop a reversible-jump Bayesian method of fitting multi-optima OU models to phylogenetic comparative data that estimates the placement and magnitude of adaptive shifts directly from the data. We show how biologically informed hypotheses can be tested against this inferred posterior of shift locations using Bayes Factors to establish whether our a priori models adequately describe the dynamics of adaptive peak shifts. Furthermore, we show how the inclusion of informative priors can be used to restrict models to biologically realistic parameter space and test particular biological interpretations of evolutionary models. We argue that Bayesian model fitting of OU models to comparative data provides a framework for integrating of multiple sources of biological data—such as microevolutionary estimates of selection parameters and paleontological timeseries—allowing inference of adaptive landscape dynamics with explicit, process-based biological interpretations.
Bethesda: National Institutes of Health
Article
  • Jan 1998
Multivariate comparative analysis using OUCH
Conference Paper
  • Feb 2009
The Chañares (Argentina) Triassic reptile fauna. VII. The postcranial skeleton of the traversodontid Massetognathus pascuali (Therapsida, Cynodontia)
Article
The Origin and Evolution of Mammals
Book
  • Jan 2005
Mammals are the dominant large animals of today, occurring in virtually every environment. This book is an account of the remarkable fossil records that document their origin since the extinction of the dinosaurs. Tracing their evolution over the last 35 million years. For the first time presented in one single volume Kemp unveils the exciting DNA sequence evidence which coupled with fossil evidence challenges current thinking on the relationships amongst mammal and their inferred history.
The Nlme Package: Linear and Nonlinear Mixed Effects Models, R Version 3
Book
  • Jan 2012
Cynodont Postcranial Anatomy and the "Prototherian" Level of Mammalian Organization
Article
  • Mar 1970
Study of the reptile-mammal evolutionary transition requires both a functional interpretation of fossil material and a comparative approach to the biology of primitive living mammals. The biological level of organization of mammalian ancestors in Late Triassic time is evaluated here by (1) reviewing the functional implications of the postcranial skeleton of cynodonts (an advanced group of Permo-Triassic mammal-like reptiles from which all mammals were probably derived) and (2) comparing salient physiological and anatomical features of monotremes with those of therians. Cynodonts possessed a number of postcranial skeletal characters which were incipiently mammalian in function. Therefore, there is evidence that a "mammalian level of organization," defined by features generally retained by living mammals, had very early beginnings. Monotremes share with therians so many basic physiological and anatomical features that it appears unlikely that all of these could have been developed in parallel. Rather, monotremes and therians must have inherited from their common (and probably Late Triassic) ancestor a fundamentally mammalian biological system.