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Late-surviving stem mammal links the lowermost Cretaceous of North America and Gondwana

Authors:
Adam Huttenlocker at University of Southern California
Adam Huttenlocker
David M Grossnickle at Oregon Institute of Technology
David M Grossnickle
  • Oregon Institute of Technology
James I. Kirkland at Utah Geological Survey
James I. Kirkland
Julia A Schultz at University of Bonn
Julia A Schultz
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Abstract and Figures

Haramiyida was a successful clade of mammaliaforms, spanning the Late Triassic period to at least the Late Jurassic period, but their fossils are scant outside Eurasia and Cretaceous records are controversial1-4. Here we report, to our knowledge, the first cranium of a large haramiyidan from the basal Cretaceous of North America. This cranium possesses an amalgam of stem mammaliaform plesiomorphies and crown mammalian apomorphies. Moreover, it shows dental traits that are diagnostic of isolated teeth of supposed multituberculate affinities from the Cretaceous of Morocco, which have been assigned to the enigmatic 'Hahnodontidae'. Exceptional preservation of this specimen also provides insights into the evolution of the ancestral mammalian brain. We demonstrate the haramiyidan affinities of Gondwanan hahnodontid teeth, removing them from multituberculates, and suggest that hahnodontid mammaliaforms had a much wider, possibly Pangaean distribution during the Jurassic-Cretaceous transition.
| Dentition of Cifelliodon. a, Right posterior molar in buccal (left), occlusal (middle) and lingual (right) views. Arrows denote anterior. b, Reinterpretation of Hahnodon. Roots and posterior molar of Cifelliodon (top) shown for comparison. Note that Hahnodon in b does not match completely divided M 2 roots of multituberculates (c) (Paulchoffatia, GUI MAM 8/73). Images are not to scale. Hahnodon redrawn from previous publications 14, 21. a-b c, anterobuccal cusp; b f, anterobuccal furrow; I, incisor position (homologous positions to earlier haramiyidans); l f, posterolingual furrow; M 2 , second lower molar; p-l c, posterolingual cusp; PC 4 , fourth postcanine (posterior molar).
| Dentition of Cifelliodon. a, Right posterior molar in buccal (left), occlusal (middle) and lingual (right) views. Arrows denote anterior. b, Reinterpretation of Hahnodon. Roots and posterior molar of Cifelliodon (top) shown for comparison. Note that Hahnodon in b does not match completely divided M 2 roots of multituberculates (c) (Paulchoffatia, GUI MAM 8/73). Images are not to scale. Hahnodon redrawn from previous publications 14, 21. a-b c, anterobuccal cusp; b f, anterobuccal furrow; I, incisor position (homologous positions to earlier haramiyidans); l f, posterolingual furrow; M 2 , second lower molar; p-l c, posterolingual cusp; PC 4 , fourth postcanine (posterior molar).
… 
Stratigraphic section through Andrew’s Site and quarry map a, Revised type section of the Yellow Cat Member of the Cedar Mountain Formation showing the stratigraphic position of Andrew’s Site (UMNH 1207). Modified from McDonald et al.¹⁵. b, Quarry map of Andrew’s Site. The position of the mammaliaform skull UMNH VP 16771 is indicated in red.
Stratigraphic section through Andrew’s Site and quarry map a, Revised type section of the Yellow Cat Member of the Cedar Mountain Formation showing the stratigraphic position of Andrew’s Site (UMNH 1207). Modified from McDonald et al.¹⁵. b, Quarry map of Andrew’s Site. The position of the mammaliaform skull UMNH VP 16771 is indicated in red.
… 
Skull and interpretive drawings of C. wahkarmoosuch UMNH VP 16771 a, b, Specimen shown in dorsal (a) and ventral (b) views. Grey areas represent matrix infill, hatched areas represent crushed/desiccated bones, dashed lines represent cracks through the specimen. c, Stereopair of the left side of skull in ventral view to show broad, shallow squamosal glenoid. as, alisphenoid (epipterygoid); bs, basisphenoid; C, upper canine alveolus; e n, external naris; f, frontal; f alt, anterior lateral trough foramen (cavum epiptericum ventral opening); f i, incisive foramen; f l, lacrimal foramen; f m-pal, maxillopalatine foramen; f pl, perilymphatic groove/foramen; f pt-par, pterygoparoccipital foramen; g, squamosal glenoid; I³, second upper incisor alveolus; j, jugal; l, lacrimal; m, maxilla; n, nasal; o, occipital; p, parietal; pal, palatine; PC⁴, in situ posterior upper postcanine (molar); pe, petrosal; pm, premaxilla; pt, pterygoid; sq, squamosal; v, vomer.
Skull and interpretive drawings of C. wahkarmoosuch UMNH VP 16771 a, b, Specimen shown in dorsal (a) and ventral (b) views. Grey areas represent matrix infill, hatched areas represent crushed/desiccated bones, dashed lines represent cracks through the specimen. c, Stereopair of the left side of skull in ventral view to show broad, shallow squamosal glenoid. as, alisphenoid (epipterygoid); bs, basisphenoid; C, upper canine alveolus; e n, external naris; f, frontal; f alt, anterior lateral trough foramen (cavum epiptericum ventral opening); f i, incisive foramen; f l, lacrimal foramen; f m-pal, maxillopalatine foramen; f pl, perilymphatic groove/foramen; f pt-par, pterygoparoccipital foramen; g, squamosal glenoid; I³, second upper incisor alveolus; j, jugal; l, lacrimal; m, maxilla; n, nasal; o, occipital; p, parietal; pal, palatine; PC⁴, in situ posterior upper postcanine (molar); pe, petrosal; pm, premaxilla; pt, pterygoid; sq, squamosal; v, vomer.
… 
Skull and interpretive drawings of C. wahkarmoosuch UMNH VP 16771 (continued) Specimen shown in left lateral view. Grey areas represent matrix infill, dashed lines represent broken/reconstructed bones. f in, infraorbital foramen; f v, lateral external vascular foramen; os, orbitosphenoid; t, tabular.
Skull and interpretive drawings of C. wahkarmoosuch UMNH VP 16771 (continued) Specimen shown in left lateral view. Grey areas represent matrix infill, dashed lines represent broken/reconstructed bones. f in, infraorbital foramen; f v, lateral external vascular foramen; os, orbitosphenoid; t, tabular.
… 
Cranial foramina and sinuses in the braincase of C. wahkarmoosuch a, Line drawing of the posterior skull in right oblique (anterolateral) view. b, Computed tomography transparency of the skull in left oblique view, showing the prootic sinus and associated branches of the stapedial artery (light green). d m, diploetica magna; r i, stapedial artery (ramus inferior); r s, stapedial artery (ramus superior); r t, ramus temporalis; V1, orbital vacuity (hypothesized exit for ophthalmic branch of trigeminal nerve); V3, foramen pseudovale (hypothesized exit for mandibular branch of trigeminal nerve).
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Cranial foramina and sinuses in the braincase of C. wahkarmoosuch a, Line drawing of the posterior skull in right oblique (anterolateral) view. b, Computed tomography transparency of the skull in left oblique view, showing the prootic sinus and associated branches of the stapedial artery (light green). d m, diploetica magna; r i, stapedial artery (ramus inferior); r s, stapedial artery (ramus superior); r t, ramus temporalis; V1, orbital vacuity (hypothesized exit for ophthalmic branch of trigeminal nerve); V3, foramen pseudovale (hypothesized exit for mandibular branch of trigeminal nerve).
… 
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LETTER https://doi.org/10.1038/s41586-018-0126-y
Late-surviving stem mammal links the lowermost
Cretaceous of North America and Gondwana
Adam K. Huttenlocker1*, David M. Grossnickle2, James I. Kirkland3,4, Julia A. Schultz5 & Zhe-Xi Luo2,5*
Haramiyida was a successful clade of mammaliaforms, spanning
the Late Triassic period to at least the Late Jurassic period, but
their fossils are scant outside Eurasia and Cretaceous records are
controversial1–4. Here we report, to our knowledge, the first cranium
of a large haramiyidan from the basal Cretaceous of North America.
This cranium possesses an amalgam of stem mammaliaform
plesiomorphies and crown mammalian apomorphies. Moreover, it
shows dental traits that are diagnostic of isolated teeth of supposed
multituberculate affinities from the Cretaceous of Morocco, which
have been assigned to the enigmatic ‘Hahnodontidae’. Exceptional
preservation of this specimen also provides insights into the
evolution of the ancestral mammalian brain. We demonstrate the
haramiyidan affinities of Gondwanan hahnodontid teeth, removing
them from multituberculates, and suggest that hahnodontid
mammaliaforms had a much wider, possibly Pangaean distribution
during the Jurassic–Cretaceous transition.
The ecological expansion of crown Mammalia accelerated in the
wake of extinctions of diverse and disparate archaic mammalia-
morph groups during the mid-Mesozoic
1
. Haramiyidans represent
one such clade of early mammaliamorphs that show preservation of
notable links between nonmammalian and mammalian structure and
physiology2–4. Their fossils, which were dated to the Late Triassic–
Jurassic, were historically limited to isolated teeth and incomplete
gnathal remains4, 5, hindering a more complete understanding of their
radiation. Recent discoveries of articulated skeletal material of eleuth
-
erodont haramiyidans from the Middle–Upper Jurassic of China
have shed new light on their diversification
6, 7
, although these fossils
have also sparked new debate over their phylogenetic position
4, 6–12
.
1Department of Integrative Anatomical Sciences, University of Southern California, Los Angeles, CA, USA. 2Committee on Evolutionary Biology, The University of Chicago, Chicago, IL, USA. 3Utah
Geological Survey, Salt Lake City, UT, USA. 4Natural History Museum of Utah, Salt Lake City, UT, USA. 5Department of Organismal Biology and Anatomy, The University of Chicago, Chicago, IL, USA.
*e-mail: ahuttenlocker@gmail.com; zxluo@uchicago.edu
Fig. 1 | Cranium of C. wahkarmoosuch. a–e, Holotype in dorsal (a), left
lateral (b), frontal (c), ventral (d) and occipital (e) views. as, alisphenoid
(epipterygoid); bs, basisphenoid; C, upper canine alveolus; f, frontal;
f i, incisive foramen; f l, lacrimal foramen; g, squamosal glenoid; I2, first
upper incisor alveolus (homologous to second incisor position in earlier
haramiyidans); I3, second upper incisor alveolus (homologous to third
incisor position); j, jugal; l, lacrimal; m, maxilla; n, nasal; o, occipital;
os, orbitosphenoid; p, parietal; p pr, paroccipital process; pal, palatine; PC4,
in situ posterior upper postcanine (molar); pe, petrosal; pm, premaxilla;
pp, postparietal; pt, pterygoid; sq, squamosal; t, tabular; v, vomer.
10 mm
tp
pp
pt
o
p pr
sq
sq
pt
pt
m
sq
j
j
mpm
n
n
l
l
f l f l
p
p
as as
pt
os
pal
pm
pm
pm
m
pal
pt
bs
pe
sq
j
C
g
o
v
f i
I2
I3
PC4
m
j
pe pe
pp
tsq
t
oo
f
f
f
ab
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d
e
108 | NATURE | VOL 558 | 7 JUNE 2018
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
... Well-preserved fossils from the Lagerstätten Yanliao and Jehol biotas represent the best-known specimens in many basal clades and comprise a sizable proportion of ingroup taxa in morphological matrices for mammaliaform phylogeny, e.g., 17% (21/123) in the present dataset (see Supplementary Material, character matrix files), laying the fundamental groundwork for comprehensive reconstruction of mammaliaform phylogeny. However, competing hypotheses on mammaliaform evolution exist with a focus on the affinity and phylogenetic placement of allotherians, a group proposed by some to comprise haramiyidans, multituberculates, and gondwanatherians (Bi et al., 2014;Han et al., 2017;Huttenlocker et al., 2018;Krause et al., 2020Krause et al., , 2014Meng et al., 2017;Wang et al., 2019b;Zheng et al., 2013;Zhou et al., 2013), although the placement of haramiyidans is disputed Luo et al., 2015a;Meng et al., 2017;Huttenlocker et al., 2018). Understanding the timing and composition of crown mammals is fundamental in the evolutionary biology of vertebrates. ...
... Well-preserved fossils from the Lagerstätten Yanliao and Jehol biotas represent the best-known specimens in many basal clades and comprise a sizable proportion of ingroup taxa in morphological matrices for mammaliaform phylogeny, e.g., 17% (21/123) in the present dataset (see Supplementary Material, character matrix files), laying the fundamental groundwork for comprehensive reconstruction of mammaliaform phylogeny. However, competing hypotheses on mammaliaform evolution exist with a focus on the affinity and phylogenetic placement of allotherians, a group proposed by some to comprise haramiyidans, multituberculates, and gondwanatherians (Bi et al., 2014;Han et al., 2017;Huttenlocker et al., 2018;Krause et al., 2020Krause et al., , 2014Meng et al., 2017;Wang et al., 2019b;Zheng et al., 2013;Zhou et al., 2013), although the placement of haramiyidans is disputed Luo et al., 2015a;Meng et al., 2017;Huttenlocker et al., 2018). Understanding the timing and composition of crown mammals is fundamental in the evolutionary biology of vertebrates. ...
... Recently, explorations of deep divergence in mammaliaforms encountered incongruence between phylogeny and stratigraphy, particularly in regard to previously poorly known haramiyidans. Specifically, splitting haramiyidans and multituberculates challenges the monophyly of allotherians but fits well with the stratigraphy (Huttenlocker et al., 2018;Luo et al., 2015aLuo et al., , 2017Meng et al., 2017;Zhou et al., 2013). In this interpretation, substantial similarities in skull, dentition, and ear bones are interpreted as adaptive convergence between the stem clade haramiyidans and the crown clade multituberculates (Huttenlocker et al., 2018;Luo et al., 2015aLuo et al., , 2017Meng et al., 2017;Zhou et al., 2013). ...
View
... This is partly due to the fragmentary material known in the two groups, particularly 'haramiyidans' . For decades, the main evidence that unites 'haramiyidans' and multituberculates as allotherians is the gross similarity of their molar teeth (Butler 2000) and diverse views have been put forward: 'haramiyidans' have been considered either as the earliest multituberculates (Hahn 1973, as a sister-group of the multituberculates MacIntyre 1994, Gambaryan andKielan-Jaworowska 1995), as a paraphyletic group that gave rise to multituberculates (Van Valen 1976, Hahn et al. 1989, Butler 2000, Butler and Hooker 2005, Hahn and Hahn 2006, Han et al. 2017, or as a group that does not share the most recent common ancestor with multituberculates but is placed outside of mammals (Luo et al. 2015, Huttenlocker et al. 2018. Nonetheless, most recent studies have recognized euharamiyidans as a monophyletic group that is clustered with multituberculates and gondwanatherians to form Allotheria within Mammalia , Krause et al. 2020a, Mao et al. 2020. ...
... Mao et al. (2022) demonstrated that haramiyidan teeth previously assigned to the purported haramiyidan 'Eleutherodon' , 'Millsodon' , and 'Kirtlingtonia' and the multituberculate Kermackodon, were actually teeth from different upper or lower dental loci of the same haramiyidan species Kermackodon oxfordensis. This recognition results in significant taxonomical modification of these allotherians and impacts on haramiyidan phylogeny given that some of these taxa have been used in phylogenetic analyses (Huttenlocker et al. 2018, Wang et al. 2021. In this study, we used the haramiyidan species based on the currently recognized species of 'haramiyidans' . ...
... Our analysis reinforces the view that multituberculates, 'haramiyidans' , and gondwanatherians constitute the clade Allotheria within Mammalia, which has long been recognized (Butler 2000, Kielan-Jaworowska et al. 2004, Hahn and Hahn 2006 and has been supported by recent phylogenetic analyses (Luo et al. 2007, Zheng et al. 2013, Krause et al. 2014, 2020a, Han et al. 2017, Hoffmann et al. 2020, Mao et al. 2020, Wang et al. 2021, although competing hypotheses exist (Luo et al. 2015, Huttenlocker et al. 2018. Given the preferred phylogeny and the morphological evidence, it is most probable that the Late Triassic Haramiyavia and Theroteinus represent the primitive morphotypes of allotherians that gave rise to the Jurassic euharamiyidans and multituberculates, a view previously put forward by others (Van Valen 1976, Hahn et al. 1989, Butler 2000, Butler and Hooker 2005, Hahn and Hahn 2006 and supported by several phylogenetic analyses , Krause et al. 2014, Han et al. 2017, Mao et al. 2021, Wang et al. 2021, and that mammals originated in the Late Triassic , Mao et al. 2021). ...
A new euharamiyidan, Mirusodens caii (Mammalia: Euharamiyida), from the Jurassic Yanliao Biota and evolution of allotherian mammals
Article
  • Jul 2023
Allotheria are an extinct group of mammaliaforms that originally comprised multituberculates, to which ‘haramiyidans’ and gondwanatherians were later added. Phylogenetic relationships of allotherians have remained controversial since the first reports of the allotherian fossils in the 1800s. Here we report a new euharamiyidan based on a skeletal specimen from the Jurassic Daohugou phase of the Yanliao Biota, China. The superb specimen preserves impressions of differentiated hairs. The pes with impressions of toe skin and claw sheath represents the first such evidence in Mesozoic mammaliamorphs. The remarkable tooth morphologies surpass in complexity any Mesozoic mammals previously known. Phylogenetic analyses place the new species within euharamiyidans from Eurasia and support euharamiyidans, multituberculates, and gondwanatherians as a tripartite monophyletic Allotheria within mammals. This clade is supported not only by their similar molar pattern, but also by many shared derived features of the dental system recognized from discoveries during the last two decades. Allotherians and therians represent the two most successful groups of mammals that are characterized by distinct dental systems. They originated at the latest in the Late Triassic and became diversified in the Middle Jurassic, representing two directions of ecomorphological adaptation during early evolution of mammals.
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... We used phylogenetic regression models to test Bergmann's rule in Mesozoic dinosaurs and mammaliaforms but focused primarily on the former, given their larger sample size and range in body size. As the foundation for our phylogenetic analyses, we use a comprehensive dinosaur phylogeny from Benson and colleagues 29 , which includes 624 dinosaurian and avemetatarsalian taxa, and a phylogeny of extinct mammaliaforms from Huttenlocker and colleagues 58 . We added Nanuqsaurus hoglundi to the phylogeny of Benson et al. 29 To test Bergmann's rule across taxa, we collected femoral circumferences (log 10 millimetres) and palaeogeographic occurrences for 339 dinosaur species from the datasets of Benson and colleagues 29 and O'Donovan and colleagues 25 . ...
Global latitudinal gradients and the evolution of body size in dinosaurs and mammals
Article
Full-text available
  • Apr 2024
Global climate patterns fundamentally shape the distribution of species and ecosystems. For example, Bergmann’s rule predicts that homeothermic animals, including birds and mammals, inhabiting cooler climates are generally larger than close relatives from warmer climates. The modern world, however, lacks the comparative data needed to evaluate such macroecological rules rigorously. Here, we test for Bergmann’s rule in Mesozoic dinosaurs and mammaliaforms that radiated within relatively temperate global climate regimes. We develop a phylogenetic model that accounts for biases in the fossil record and allows for variable evolutionary dispersal rates. Our analysis also includes new fossil data from the extreme high-latitude Late Cretaceous Arctic Prince Creek Formation. We find no evidence for Bergmann’s rule in Mesozoic dinosaurs or mammaliaforms, the ancestors of extant homeothermic birds and mammals. When our model is applied to thousands of extant dinosaur (bird) and mammal species, we find that body size evolution remains independent of latitude. A modest temperature effect is found in extant, but not in Mesozoic, birds, suggesting that body size evolution in modern birds was influenced by Bergmann’s rule during Cenozoic climatic change. Our study provides a general approach for studying macroecological rules, highlighting the fossil record’s power to address longstanding ecological principles.
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... The appearance of Mammaliaformes is situated ca. 25 Ma after the Permo-Triassic boundary (and mass extinction), during the Carnian, in the Late Triassic (Sues and Fraser 2010). The timing of emergence for the first crown mammals is poorly constrained due to a sparse Late Triassic fossil record, and the equivocal positioning of Haramiyida as either stem or crown mammals, as well as its dubious monophyletic status (Huttenlocker et al. 2018;King and Beck 2020;Williamson et al. 2014). Until now, all of the crown mammals are known from the Early Jurassic onward (King and Beck 2020;Luo 2007), and molecular analyses suggest that Mammalia arose during the Middle (Late) Jurassic, about 166.2 Ma (Bininda-Emonds et al. 2007). ...
Mammals as Paleoenvironmental Proxies
Chapter
  • Apr 2024
Mammals can be defined as the least inclusive clade containing Ornithorhynchus anatinus (Shaw in Nat Miscellany 10(118):7, 1799) and Homo sapiens Linnaeus, 1758. Mexico is the third country with the highest mammalian species richness in the world. Their fossil record in this megadiverse country spans from the Early Jurassic to the Late Pleistocene. Research of fossil mammals have been centered on taxonomy and until recently, some paleoecological and paleoenvironmental reconstructions have been published. In this chapter, some of the techniques of paleoenvironmental reconstruction based on fossil mammals are described (microwear, mesowear, stable isotope analysis, bioclimatic models, ecometric analyses, and mutual ecogeographic range) and some examples of their use with the Mexican record are provided. The extensive fossil record available for some geological epochs makes the Mexican mammals a rich source of paleoenvironmental data that needs to be further explored.
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... For many years, the tabular and postparietal bones have been considered enigmatic by comparative anatomists [50][51][52][53][54][55]. Tritheledontids, probainognathids and Cretaceous Haramiyidan mammaliaforms such as Cifelliodon and Vintana show the clear presence of the tabular [56][57][58][59]. However, a separate tabular is absent in morganucodontid, monotremes, multituberculates, marsupials and placentals [2,5]. ...
Evolution, conservatism and overlooked homologies of the mammalian skull
Article
Full-text available
  • May 2023
In the last decade, studies integrating palaeontology, embryology and experimental developmental biology have markedly altered our homological understanding of the mammalian skull. Indeed, new evidence suggests that we should revisit and restructure the conventional anatomical terminology applied to the components of the mammalian skull. Notably, these are classical problems that have remained unresolved since the ninteenth century. In this review, I offer perspectives on the overlooked problems associated with the homology, development, and conservatism of the mammalian skull, aiming to encourage future studies in these areas. I emphasise that ossification patterns, bone fusion, cranial sutures and taxon-specific neomorphic bones in the skull are virtually unexplored, and further studies would improve our homological understanding of the mammalian skull. Lastly, I highlight that overlooked bones may exist in the skull that are not yet known to science and suggest that further search is needed. This article is part of the theme issue ‘The mammalian skull: development, structure and function’.
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... Therefore, its origin is often hypothesized to be correlated with that of sensory hair [53,96], and in this respect, it is noticeable that the lateral expansion of the cerebral hemispheres occurs in almost the same taxa as those that evolved an IOF, i.e. the prozostrodontian NMC (see above). However, it is important to note that no NMC or NMM display a well-defined rhinal fissure that normally marks the ventral expansion of the isocortex on the sidewalls of the braincase in mammals [83,92,93,97]. In the absence of a clear rhinal fissure, inferring the presence of an isocortex is extremely speculative, and it is possible that an isocortex is limited to Mammalia. ...
Craniodental anatomy in Permian–Jurassic Cynodontia and Mammaliaformes (Synapsida, Therapsida) as a gateway to defining mammalian soft tissue and behavioural traits
Article
Full-text available
  • May 2023
Mammals are diagnosed by more than 30 osteological characters (e.g. squamosal- dentary jaw joint, three inner ear ossicles, etc.) that are readily preserved in the fossil record. However, it is the suite of physiological, soft tissue and behavioural characters (e.g. endothermy, hair, lactation, isocortex and parental care), the evolutionary origins of which have eluded scholars for decades, that most prominently distinguishes living mammals from other amniotes. Here, we review recent works that illustrate how evolutionary changes concentrated in the cranial and dental morphology of mammalian ancestors, the Permian–Jurassic Cynodontia and Mammaliaformes, can potentially be used to document the origin of some of the most crucial defining features of mammals. We discuss how these soft tissue and behavioural traits are highly integrated, and how their evolution is intermingled with that of craniodental traits, thus enabling the tracing of their previously out-of-reach phylogenetic history. Most of these osteological and dental proxies, such as the maxillary canal, bony labyrinth and dental replacement only recently became more easily accessible—thanks, in large part, to the widespread use of X-ray microtomography scanning in palaeontology—because they are linked to internal cranial characters.
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... It was defined as the least inclusive clade containing Prozostrodon brasiliensis, Tritylodon longaevus (Tritylodontidae), Pachygenelus monus ("Trithelodontidae"), and Mus musculus (Mammalia). During the Late Triassic/Early Jurassic, the clade Mammaliaformes emerged and diversified (Hunttenlocker, Grossnicke, Kirkland, Schultz, & Luo, 2018;Liu & Olsen, 2010;Luo, Gates, Jenkins Jr., Amaral, & Shubin, 2015;Rougier, Martinelli, & Forasiepi, 2021;Rowe, 1988). Besides mammaliaforms, "tritheledontids" and tritylodontids were cynodont lineages that survived the Triassic/Early Jurassic boundary, with the former disappearing by the Early Jurassic and the latter in the Early Cretaceous (Matsuoka, Kusuhashi, & Corfe, 2016;Kerber, Martinelli, Müller, & Pretto, 2022 and references cited therein). ...
Endocranial anatomy of the early prozostrodonts (Eucynodontia: Probainognathia) and the neurosensory evolution in mammal forerunners
Article
  • Apr 2023
Prozostrodon brasiliensis and Therioherpeton cargnini are non-mammaliaform cynodonts that lived ~233 million years ago (late Carnian, Late Triassic) in western Gondwana. They represent some of the earliest divergent members of the clade Prozostrodontia, which includes "tritheledontids", tritylodontids, "brasilodontids", and mammaliaforms (including Mammalia as crown group). Here, we studied the endocranial anatomy (cranial endocast, nerves, vessels, ducts, ear region, and nasal cavity) of these two species. Our findings suggest that during the Carnian, early prozostrodonts had a brain with well-developed olfactory bulbs, expanded cerebral hemispheres divided by the interhemispheric sulcus, and absence of an unossified zone and pineal body. The morphology of the maxillary canal represents the necessary condition for the presence of facial vibrissae. A slight decrease in encephalization is observed at the origin of the clade Prozostrodontia. This new anatomical information provides evidence for the evolution of endocranial traits of the first prozotrodonts, a Late Triassic lineage that culminated in the origin of mammals.
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The Decline and Fall of the Mammalian Stem
Article
Full-text available
  • Feb 2024
The mammalian crown originated during the Mesozoic and subsequently radiated into the substantial array of forms now extant. However, for about 100 million years before the crown's origin, a diverse array of stem mammalian lineages dominated terrestrial ecosystems. Several of these stem lineages overlapped temporally and geographically with the crown mammals during the Mesozoic, but by the end of the Cretaceous crown mammals make up the overwhelming majority of the fossil record. The progress of this transition between ecosystems dominated by stem mammals and those dominated by crown mammals is not entirely clear, in part due to a distinct separation of analyses and datasets. Analyses of macroevolutionary patterns tend to focus on either the Mammaliaformes or the non-mammalian cynodonts, with little overlap in the datasets, preventing direct comparison of the diversification trends. Here I analyse species richness and biogeography of Synapsida as a whole during the Mesozoic, allowing comparison of the patterns in the mammalian crown and stem within a single framework. The analysis reveals the decline of the stem mammals occurred in two discrete phases. The first phase occurred between the Triassic and Middle Jurassic, during which the stem mammals were more restricted in their geographic range than the crown mammals, although within localities their species richness remained at levels seen previously. The second phase was a decline in species richness, which occurred during the Lower Cretaceous. The results show the decline of stem mammals, including tritylodontids and several mammaliaform groups, was not tied to a specific event, nor a gradual decline, but was instead a multiphase transition.
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Evolutionary origins of the prolonged extant squamate radiation
Article
Full-text available
  • Nov 2022
Squamata is the most diverse clade of terrestrial vertebrates. Although the origin of pan-squamates lies in the Triassic, the oldest undisputed members of extant clades known from nearly complete, uncrushed material come from the Cretaceous. Here, we describe three-dimensionally preserved partial skulls of two new crown lizards from the Late Jurassic of North America. Both species are placed at the base of the skink, girdled, and night lizard clade Pan-Scincoidea, which consistently occupies a position deep inside the squamate crown in both morphological and molecular phylogenies. The new lizards show that several features uniting pan-scincoids with another major lizard clade, the pan-lacertoids, in trees using morphology were convergently acquired as predicted by molecular analyses. Further, the palate of one new lizard bears a handful of ancestral saurian characteristics lost in nearly all extant squamates, revealing an underappreciated degree of complex morphological evolution in the early squamate crown. We find strong evidence for close relationships between the two new species and Cretaceous taxa from Eurasia. Together, these results suggest that early crown squamates had a wide geographic distribution and experienced complicated morphological evolution even while the Rhynchocephalia, now solely represented by the tuatara, was the dominant clade of lepidosaurs.
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A Jurassic gliding euharamiyidan mammal with an ear of five auditory bones
Article
Full-text available
  • Nov 2017
  • NATURE
Gliding is a distinctive locomotion type that has been identified in only three mammal species from the Mesozoic era. Here we describe another Jurassic glider that belongs to the euharamiyidan mammals and shows hair details on its gliding membrane that are highly similar to those of extant gliding mammals. This species possesses a five-boned auditory apparatus consisting of the stapes, incus, malleus, ectotympanic and surangular, representing, to our knowledge, the earliest known definitive mammalian middle ear. The surangular has not been previously identified in any mammalian middle ear, and the morphology of each auditory bone differs from those of known mammals and their kin. We conclude that gliding locomotion was probably common in euharamiyidans, which lends support to idea that there was a major adaptive radiation of mammals in the mid-Jurassic period. The acquisition of the auditory bones in euharamiyidans was related to the formation of the dentary-squamosal jaw joint, which allows a posterior chewing movement, and must have evolved independently from the middle ear structures of monotremes and therian mammals.
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New gliding mammaliaforms from the Jurassic
Article
Full-text available
  • Aug 2017
Stem mammaliaforms are Mesozoic forerunners to mammals, and they offer critical evidence for the anatomical evolution and ecological diversification during the earliest mammalian history. Two new eleutherodonts from the Late Jurassic period have skin membranes and skeletal features that are adapted for gliding. Characteristics of their digits provide evidence of roosting behaviour, as in dermopterans and bats, and their feet have a calcaneal calcar to support the uropagatium as in bats. The new volant taxa are phylogenetically nested with arboreal eleutherodonts. Together, they show an evolutionary experimentation similar to the iterative evolutions of gliders within arboreal groups of marsupial and placental mammals. However, gliding eleutherodonts possess rigid interclavicle-clavicle structures, convergent to the avian furculum, and they retain shoulder girdle plesiomorphies of mammaliaforms and monotremes. Forelimb mobility required by gliding occurs at the acromion-clavicle and glenohumeral joints, is different from and convergent to the shoulder mobility at the pivotal clavicle-sternal joint in marsupial and placental gliders.
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New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem
Article
Full-text available
  • Aug 2017
Stem mammaliaforms are forerunners to modern mammals, and they achieved considerable ecomorphological diversity in their own right. Recent discoveries suggest that eleutherodontids, a subclade of Haramiyida, were more species-rich during the Jurassic period in Asia than previously recognized. Here we report a new Jurassic eleutherodontid mammaliaform with an unusual mosaic of highly specialized characteristics, and the results of phylogenetic analyses that support the hypothesis that haramiyidans are stem mammaliaforms. The new fossil shows fossilized skin membranes that are interpreted to be for gliding and a mandibular middle ear with a unique character combination previously unknown in mammaliaforms. Incisor replacement is prolonged until well after molars are fully erupted, a timing pattern unique to most other mammaliaforms. In situ molar occlusion and a functional analysis reveal a new mode of dental occlusion: dual mortar-pestle occlusion of opposing upper and lower molars, probably for dual crushing and grinding. This suggests that eleutherodontids are herbivorous, and probably specialized for granivory or feeding on soft plant tissues. The inferred dietary adaptation of eleutherodontid gliders represents a remarkable evolutionary convergence with herbivorous gliders in Theria. These Jurassic fossils represent volant, herbivorous stem mammaliaforms associated with pre-angiosperm plants that appear long before the later, iterative associations between angiosperm plants and volant herbivores in various therian clades.
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First haramiyid (Mammalia, Allotheria) from the Mesozoic of Gondwana
Article
Full-text available
  • Jan 1999
A haramiyid tooth is described from the Upper Jurassic of Tendaguru in southwestern Tanzania, East Africa. The specimen, identified tentatively as a lower posterior premolar, is made the holotype of a new taxon, Staffia aenigmatica gen. et sp. nov. which is placed in the Haramiyida. Staffia gen. nov. shares several features with Thomasia from the Late Triassic to Early Jurassic of Europe, notably the arrangement of cusps in two parallel longitudinal rows bordering a central basin, cusp height which progressively decreases in both rows posteriorly, the different height of the rows, the U-shaped posterior rim, and the smooth enamel surface. The main difference between these taxa is the presence of well-developed synclines with rounded floors in Staffia gen. nov., especially that of the principal syncline LS1. Resemblances in the basic tooth crown pattern indicate that occlusion and chewing might have been similar in both genera, but the synclines in Staffia gen. nov. suggest some subtle differences in food processing. Staffia aenigmatica gen. et sp. nov. is the first record of a haramiyid from Gondwana, and also the youngest stratigraphic occurrence for this allotherian group so far. Ein unterer Backenzahn aus den oberjurassischen Tendaguru-Schichten von Tansania in Ostafrika wird als Staffia aenigmatica gen. et sp. nov. beschrieben und zu den Haramiyida gestellt. Bei dem Fund handelt es sich wahrscheinlich um einen hinteren unteren Prämolaren. Staffia gen. nov. weist zahlreiche Merkmale auf, die bei der spät-triassischen bis früh-jurassischen Gattung Thomasia auftreten. Dazu zählen z. B. die Anordnung der Höcker in zwei unterschiedlich hohen Längsreihen, die in beiden Reihen von vorn nach hinten abnehmende Höckerhöhe, der U-förmige Hinterrand und die glatte Schmelzoberfläche. Die Synklinalen zwischen den Zahnhöckern von Staffia gen. nov. stellen ein neuerworbenes Merkmal dar. Die weitgehenden Übereinstimmungen im Grundaufbau der Zahnkronen beider Gattungen lassen darauf schließen, daß die Kieferbewegung und der Kauvorgang ähnlich waren, doch deuten die Synclinalen bei Staffia gen. nov. auf eine differenziertere Aufbereitung der Nahrung hin. Staffia aenigmatica gen. et sp. nov. ist der erste Nachweis eines Haramiyiden auf dem Gondwana-Kontinent und zugleich der bisher erdgeschichtlich jüngste Beleg für diese Säugetiergruppe. doi:10.1002/mmng.1999.4860020112
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Allometric Scaling in the Dentition of Primates and Insectivores
Chapter
Full-text available
  • Jan 1985
Size is probably the single most important determinant of body architecture, physiology, ecology, life history, and social organization in mammals. Morphological characteristics associated with each of these broadly defined aspects of structure and function can profitably be studied in relation to size, and none can be fully understood without considering size. Here we outline the relationship of tooth size to body size in frugivorous and folivorous primates. For comparison we shall also consider the relationship of tooth size to body size in insectivorous mammals.
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Ear ossicle morphology of the Jurassic euharamiyidan Arboroharamiya and evolution of mammalian middle ear
Article
  • May 2016
  • J MORPHOL
The middle ear bones of Mesozoic mammals are rarely preserved as fossils and the morphology of these ossicles in the earliest mammals remains poorly known. Here, we report the stapes and incus of the euharamiyidan Arboroharamiya from the lower Upper Jurassic (∼160 Ma) of northern China, which represent the earliest known mammalian middle ear ossicles. Both bones are miniscule in relation to those in non-mammalian cynodonts. The skull length/stapedial footplate diameter ratio is estimated as 51.74 and the stapes length as the percentage of the skull length is 4%; both numbers fall into the stapes size ranges of mammals. The stapes is "rod-like" and has a large stapedial foramen. It is unique among mammaliaforms in having a distinct posterior process that is interpreted as for insertion of the stapedius muscle and homologized to the ossified proximal (stapedial) end of the interhyal, on which the stapedius muscle attached. The incus differs from the quadrate of non-mammalian cynodonts such as morganucodontids in having small size and a slim short process. Along with lack of the postdentary trough and Meckelian groove on the medial surface of the dentary, the ossicles suggest development of the definitive mammalian middle ear (DMME) in Arboroharamiya. Among various higher-level phylogenetic hypotheses of mammals, the one we preferred places "haramiyidans" within Mammalia. Given this phylogeny, development of the DMME took place once in the allotherian clade containing euharamiyidans and multituberculates, probably independent to those of monotremes and therians. Thus, the DMME has evolved at least three times independently in mammals. Alternative hypothesis that placed "haramiyidans" outside of Mammalia would require independent acquisition of the DMME in multituberculates and euharamiyidans as well as parallel evolution of numerous derived similarities in the dentition, occlusion pattern, mandibles, cranium, and postcranium between the two groups and between "haramiyidans" and other mammals. J. Morphol., 2016. © 2016 Wiley Periodicals, Inc.
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Late Mesozoic North Atlantic land bridges
Article
  • May 2016
  • EARTH-SCI REV
Current palaeogeographical reconstructions suggest that since the onset of the Late Jurassic and during the whole Cretaceous Period, the landmasses of North America and West Eurasia have been separated by seaway(s) exposed on the North Atlantic rift system. Such a palaeogeographical setting should have limited the possibility of direct overland dispersals between the biotas of the two continents. Strong faunal affinities between the two sides of the North proto-Atlantic Ocean presuppose faunal exchanges between the landmasses, however, suggesting the existence of ephemeral land bridges around the Jurassic/Cretaceous boundary and the mid-Early Cretaceous. This study reviews the current faunal evidence and discusses palaeogeographical evidence that might better elucidate the existence of the postulated land bridges. Evaluation of the evidence leads to the conclusion that two land bridges were exposed: 1) between East North America and Iberia during the Late Kimmeridgian (~ 154 Ma) and 2) between North America and Fennoscandia, via the Barents Shelf, around the Hauterivian-Barremian boundary (~ 131 Ma). The former land bridge was terminated in the earliest Tithonian (~ 151 Ma), and the latter was terminated in the late Early Barremian (~ 129 Ma). Furthermore, the latter land bridge was contemporaneous with regressive stages in both the Mid-Polish Trough and the sea strait crossing the Russian Platform, allowing broad, direct terrestrial communication among North America, Europe, and Asia in the earliest Barremian.
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Dinosaur biogeographic structure and Mesozoic continental fragmentation: a network-based approach
Article
  • Mar 2016
  • J BIOGEOGR
Aim To reconstruct dinosaur macro‐biogeographical patterns through the Mesozoic Era using a network‐based approach. We test how continental fragmentation affected dinosaur macro‐biogeographical structure and evolutionary rates. Location A global occurrence database of dinosaur families from the Late Triassic to the end‐Cretaceous was used for this study. Methods Biogeographical and geographical network models were constructed. Continental landmasses were linked by direct continental contact and sea level (SL)‐conditioned connections in geographical networks, and by shared dinosaur families in biogeographical networks. Biogeographical networks were run with raw, novel and first‐step connections for all dinosaur, ornithischian, theropod, and sauropodomorph taxa. Results Geographical connectedness declines through time, from peak aggregation in the Triassic–Jurassic to complete separation in the latest Cretaceous. Biogeographical connectedness shows no common trend in the raw and novel connection network models, but decreases through time while showing some correlation with continental fragmentation in most of the first‐step network models. Despite continental isolation and high SLs, intercontinental faunal exchange continued right up to the end of the Cretaceous. Continental fragmentation and dinosaurian macro‐biogeographical structure do not share a common pattern with dinosaurian evolutionary rates, although there is evidence that increased continental isolation resulted in increased origination rates in some dinosaurian lineages. Spatiotemporal sampling biases and early Mesozoic establishment of family‐level distribution patterns are important drivers of apparent dinosaur macro‐biogeographical structure. Main conclusions There is some evidence to suggest that dinosaur macro‐biogeographical structure was influenced by continental fragmentation, although intercontinental exchange of dinosaur faunas appears to have continued up to the end of the Cretaceous. Macro‐biogeographical patterns are obscured by uneven geographical sampling through time and a residual earlier Mesozoic distribution which is sustained up to the end of the Cretaceous.
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