Ecomorphological diversity of Mesozoic mammals

Gareth Coleman gc12847
EASC30048 Palaeobiology Analytical Project Literature Review
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The Ecomorphological diversity of Mesozoic mammals
Gareth Andrew Coleman
gc12847@my.bristol.ac.uk
Abstract
There has been much recent progress in understanding the evolution and adaptive
radiations of early mammals and mammaliaformes, showing successive waves of
ecomorphological diversification and adaptive radiations. This is in contrast to many earlier
views on the early evolution and radiation of mammals, which characterised them
exclusively as small, insectivorous and generalised animals, with litter ecomorphological
diversity. Much of the progress has come from new fossil finds and the integration of many
techniques, such as dental microwear analysis, CT-scanning and finite element analysis.
These integrated techniques create a robust set analytical tools, and give us the potential
to increase our understanding of the early history of mammals.
Keywords: ecomorphology, diversity, mammals, Mesozoic
Main text word count: 3500
Total word count: 7635

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Declaration
'I declare that this library project is entirely my own work, and does not contain any
plagiarised material'
Signature:
Name: Gareth Coleman
Date: 17/12/2014

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Introducing the debate: past views on mammalian evolution
Mammals are one the most ubiquitous groups of animals present on Earth today
(Box 1). They exhibit much diversity and occupy a vast array of different ecological niches
on the land, in the oceans and in the air [1] [2]. There has been much research concerning
the diversification of mammals, and their adaptive radiations to fill the many niches they
presently hold, in an attempt to discern the key to their success and the timing of such
diversification. In particular, much of the recent research, coupled with many new fossils
being discovered at various localities, has shed more light and altered our views on
mammalian evolutionary history [3] [4] [5].
In the past, the traditional narrative associated with the early evolution of mammals
described them as small, living in the shadows of the much larger archosaurs which
dominated the ecosystem [6] [7]. They were therefore thought to have only exploited
niches where there was no direct competition with the archosaurs [6]. This limited
exploitable niches, and stopped specialisation, causing them to remain generalised [8].
This was thought to have forced early mammals to become largely insectivorous and
nocturnal. Becoming increasingly insectivorous would have further accelerated the
therapsid trend towards differentiated teeth with precise occlusion, in the need to capture
arthropods and crush their exoskeletons. It would also have restricted the size of the
animals, as they would not have been able to eat enough to sustain themselves [9]. The
decrease in body size, and becoming nocturnal, would have led to the need for insulation
in the form of fur, and thermoregulation [9] [10]. Nocturnal life was also thought to lead to
more acute senses, including acute sense of smell, and therefore a larger brain [11], and
loss of two of the four opsin cones present in amniotes, giving dichromatic vision, which
improved low-light vision [9].

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Much of the evidence from the fossil record supported, and to a certain extent still
does support this model of mammal evolution. Many of the early mammal fossil are small
and insectivorous, such as Morgonucodon, Megazostrodon, Yanoconodon and
Zhangheotherium [3]. However, new techniques are now being used to uncover the real
diversity exhibited by these animals.
Looking at morphology
The most direct source of information on mammalian diet are the contents of its
stomach. However, these are rarely preserved in fossil mammals (with a few remarkable
exceptions), therefore morphology has historically been the best way to assess the diets of
extinct organisms. Ecomorphology is the relation between the morphology of an organism
and its feeding and ecological role. We can look at the morphologies of modern mammals
and how it corresponds with their diets, before applying this to fossils mammals. Many
modern mammal groups have evolved distinct morphologies in order to exploit particular
food sources and ecological niches.
The size of the animal is often important in giving information on their general diet.
Small mammals have high metabolic rates due to high ratio of heat-losing surface area to
heat-generating volume, and therefore need to feed much more often than larger
mammals. Subsequently, most small mammals are insectivorous, as they cannot tolerate
slower rates of food intake or digestion. Larger mammals can generate more heat, and
less of it is lost. They can therefore tolerate slower collection rate of food (if carnivorous) or
slower digestion (if herbivorous). Generally, larger mammals are not insectivorous, as they
would not be able to ingest enough food to sustain themselves, except for a few species
which feed on large insect colonies such as ants and termites. Therefore, the size of the
fossil mammal can potentially indicate its diet [1] [9].

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Teeth and jaws are specialised and also convey information on the diet of the
animal. Mammals are heterodont, i.e. they have different kinds of teeth, with different
functions. Many insectivorous animals have very small, reduced teeth or lack dentition
altogether (such as anteaters). Herbivorous mammals generally have large molars for
grinding up vegetation, and some have blade-like incisors for cutting leaves. Specialised
herbivores, such as granivores (seed eaters) have larger, more robust molars for crushing
seeds, while gummivores (gum eaters), have tooth combs made up from the lower incisors
and canines. Carnivorous mammals have sharp teeth with large canines and carnassials
and strong jaws for a big bight force. Filter feeders, such as baleen whales, have baleen
plates for filter feeding. The teeth themselves often exhibit microwear patterns, which can
be used as a powerful tool to assess diet. Recently, analytical and numerical methods to
analyse microwear patterns have developed, as shall be discussed later [1].
There are also many other morphological adaptations to feeding. Long necks in
some mammals could have evolved so that it can take advantage of the leaves higher in
the trees, with trunks or probosces of some species being used for similar purposes, with
modern examples being giraffes and elephants. Many carnivorous mammals which
actively hunt have long legs for running and long tails for balance. These adaptation are
seen in many large cat species. Many insect eating mammals have hypertrophied limbs
built for scratch-digging and fossorial behaviours (e.g. aardvark, pangolin, armadillo and
echidnas). These may also been seen in exaptations for swimming, as in beavers, coupled
with webbed feet and tail. Mammals with these aquatic adaptation could be inferred to be
piscivorous. Scansorial (climbing) mammals often have elongated phalanges and limbs for
climbing, these being exaptations for gliding in volant mammals (e.g. in flying squirrels) [1].

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Modern analytical methods to determine ecomorphology
As well as looking at morphology, a variety of different analytical methods can now
be applied to the remains of fossils mammals to determine their ecological niches and
diets. The most important among these are finite element analysis and microtextural
analysis of dental microwear.
Finite element analysis (FEA) is used to reconstruct stress, strain and deformation
in structures. [12] [13]. It can give insights into the mechanics of various different body
parts of fossil organisms. This can be used to determine function of skeletons and the
ecology of the mammals analysed, and why evolution has shaped the bones in a particular
fashion [14] [15] [16]. Analysis of the effects of forces on structures was hitherto
impossible, as the models formed by differential equations derived from first principles
were impossible to solve, unless they were the simplest geometric shapes with the
simplest boundaries. FEA can overcome these problems by breaking the structures down
into disjoint components of simple geometry, called finite elements, or elements. This
process is called discretisation, as it takes a continuous structure, and represents it as a
series of discrete problems, which are readily solvable by mathematics. The discrete
model is obtained by connecting all of the elements by nodes to form a finite element
mesh.
The first part of the process (Figure 1), the preprocessing stage, involves the
creation of a digital representation of the structure using computer-aided design (CAD).
The structure then undergoes discretisation. The elements in the mesh can then be
assigned specific material properties that represent the elasticity of the real structure.
Virtual loads are then added at the nodes. Constraints are also added, with mobility being
restricted to particular degrees of freedom. The loads and constraints applied at this stage
are collectively called the boundary conditions. When running the analysis, nodal

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displacements are calculated in response to boundary conditions, taking the structure’s
predefined geometry and elasticity into account. These can be used to calculate structural
strain, stress and deformation, building up a picture of the mechanical behavior of a
structure under the predefined conditions. After the analysis, the final, postprocessing step
involves the representation and interpretation of the results, usually as a digital image. The
images usually have scaled colour plots and can be animated to represent structural
deformities. Results may be used to assess the accuracy of the mesh and boundary
conditions, and convergency tests can be run to assess how well the discrete model
represents the original structure. The analysis can rerun with successively smaller
elements to get more accurate results [17] [18].
While FEA is a powerful tool, it has limitations and problems, mostly the concern
that there are too many problems and assumptions associated with modelling biological
systems, particularly a fossil organism where less data is available. The main areas to
which this applies are the model creation and the application of boundary conditions. One
of the most fundamental issues faced is the level of detail which should be used, and how
this effects the accuracy of the analysis. Ultimately, this has to be a trade-off between how
accurate the model will be compared to the amount of time and computer power needed to
complete the analysis. The answer to this is complex and depends on the areas of the
skeleton that are being considered. It may be possible for certain areas of the skeleton to
be simplified more than others, while some parts have to be done in more detail to be
accurate. This also relates to whether one wishes to use 2-D or 3-D models, which will
depend on what questions are being asked. When creating the mesh, users must choose
between 2-D triangular or quadrilateral, or 3-D tetrahedral or cuboidal elements, and
whether linear of quadratic elements are required. Generally, the most accurate analyses
would be generated with cuboidal, quadratic elements, but these analyses require much

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time and computing power, maybe more than is practical [19]. Material properties also
have to be added to the elements, which can be problematic when dealing with fossil
organism, where data on material properties is not necessarily available. The applications
of boundary conditions also present problems. Knowing which loads would have been
applied to the skull of the organism in life is impossible to know, and modern analogues
(using extant phylogenetic bracketing) are essential in predicting the behavior and
possible usages of the particular anatomy in question. Further, while constraints must be
applied for the analysis to work, applying too many can prevent the model from deforming
naturally and give inaccurate results [20].
The way we can validate the FEA, and therefore combat many of these problems, is
by doing FEA analyses on living animals and seeing what levels of detail and how
accurate material properties and boundaries need to be in order for the analysis to work.
So far, it seems that these have been done exclusively on vertebrates, with the macaque
monkey being the most used animal. FEA studies on the eating mechanics of the
macaque skull have shown that accurate models can be produced if the loads applied to
the muscles are accurate, and that muscle activation patterns are not an important
consideration. This means that palaeontologists only have to worry about reconstructing
the musculature of the animal. Biological materials are very complex and may necessitate
a number of simplifications. Further studies on macaque skulls have shown that, although
more accurate modelling of material properties improved the accuracy of the analysis, the
same broad patterns were repeated in more simplified models. Generally, it seems
possible to predict the nature of deformation, even when detailed information about the
material properties are not known. Material distribution may also be have an important
effect, especially in the different types of bone with different densities, which are not
readily identifiable from fossil remains. Some studies in macaques have shown that the

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bone of the lower jaw can be represented by a solid mass of low Young’s modulus [20],
and fine anatomic detail is not necessary. However, this has not been widely applied to
other animals, with may have different arrangements of bones type in their jaws. Where
these have been done, the results vary considerably from the macaque and from each
other. Also, the problem of how teeth are set in the jaw (i.e. set directly or via ligaments)
and how this affects the models, continues to be debated [20].
FEA has had only limited use in palaeontology thus far [20]. However, important
papers, such as those on the feeding mechanics of theropod dinosaurs by Emily Rayfield
[21] [22], particularly a landmark paper in 2001 where FEA was applied to the skull of
Allosaurus [23], and in early mammaliaforms in Gill et al. 2014 [24], as well as several
important papers on various fossil mammals, have shown the potential impact that the use
of FEA can have on palaeontology [25] [26] [27] [28].
Microtextural analysis of dental microwear is another powerfull technique which can
be used to assess mammalian diet. Dental microwear are the many pits and scratches
found on the enamel of teeth, which vary with diet. Many studies have been done on fossil
mammals, particularly early hominids and other primates [29] [30] [31] [32] [33].
Conventional method of microwear analysis have been limited to two-dimensional imaging
studies using scanning electron microscopes to identify features on the teeth. This was
time-consuming, and could be very subjective and prone to error. New three-dimensional
microtextural analysis has given us a way to reliably quantify and analyse dental
microwear patterns, saving time, minimising the error and making the analysis more
objective. These measurements are taken using white-light confocal microscopy and
scale-sensitive fractal analysis, and charactierise microwear surface textures as 3-D
images [34]. The data can then undergo statistical analysis, where samples can be
compared with each other and with modern analogues. This data can be used in a

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principle component analysis (PCA), using International Organization for Standardization
(ISO) roughness parameters from animals that are being analysed [35]. The data is plotted
onto a set of axes, where different the results for different animals can be compared.
Current views on ecomorphological diversity in Mesozoic mammals
All of the evidence currently being uncovered, from new fossil finds to more
powerful analytical techniques, has brought about a drastic change in the way we think of
mammals in the Mesozoic. Certainly, while many of Mesozoic mammalian clades are still
seen to contain mainly relatively small, generalised insectivors (with these making up
much of the mammalian fauna in ecosystems such as the Jehol Biota [36]), many lineages
and clades exhibit much higher levels diversity and specialisation. We also see is
successive radiations of mammals throughout the Mesozoic, coupled with much more
ecomorpological diversity than was previously thought [3] [24].
The discovery of many of these new fossils of basal mammaliaforms (Boxes 2 and
3), especially from China [36], have greatly increased our knowledge of the earliest part of
mammal evolution and shown us that these early mammals were more diverse than
expected [3] [37]. However, while much research has been done on the diversity of
mammaliaforms from the Mid Jurassic to the Cretaceous, until recently, little had been
done on the very earliest mammaliaforms of the Late Triassic and Early Jurassic. Now,
studies are showing diversity in these earliest mammaliaforms. Using a suite of
techniques, including finite element analysis and microtextural analysis of dental
microwear, Gill et al. (2014) found that early mammaliaforms Morganucodon and
Kuehneotherium had different feeding ecologies, with Morganucodon specialising in eating
insects with hard cuticles, such as beetles, and Kuehneotherium appearing to specialise in
eating soft bodied insects, such as moths [24]. This early specialisation shows “previously

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hidden trophic diversity and niche partitioning at the base of the mammalian radiation,
supporting a hypothesis of coupled lineage splitting and ecomorphological adaptation of
the skull and jaws, even during the earliest stages of mammalian evolution” [24]. This
paper was important in its use of finite element analysis combined with microtextural
analysis of microwear, classical mechanics and imaging techniques to verify their findings
from independent lines of evidence which could be integrated together to form a more
complete picture.
Most other evidence for mammalian diet come mainly from morphological data.
Many mammaliaform lineages show many adaptations to various behaviors and ecological
specialisations. Adaptations for fossorial (digging) behavior are seen in the hypertrophied
burrowing limbs in Hadanodon, a doconodont (Box 3) from the Upper Jurassic of Portugal,
which shows many convergent characteristics with desmans and moles. These
adaptations also represent exaptations for swimming in Castorocauda, another
doconodont, from the Middle Jurassic. Castrocauda is larger than most mammaliaforms of
the period and showed further adaptations to swimming, such as a flattened tail and
possibly webbed feet, among other features showing convergence with modern
platypuses, otters and beavers. It was possibly piscivorous. It is further important in
demonstrating the earliest evidence of fur [38]. Adaptions for fossorial behavior were
originally known only from pre-mammaliaform cynodonts [39], but have now also been
demonstrated to be widespread in mammaliaform lineages.
The multituberculates (Box 4) were a very diverse group. They occupied a variety of
different niches, ranging from fossorial to scansorial and arboreal lifestyles [40]. The
ptilodonts of the Upper Cretaceous of North America, show convergences with modern
squirrels, with legs and longs tails which suggest a scansorial or aboreal lifestyle. The
ptilodonts also had enlarged and elongated last lower premolars, which may have been

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used to crush seeds, suggesting granivory [41]. A European family of multituberculates,
the kogaionids, also developed these large, blade-like lower premolars, suggesting similar
diet had convergently evolved. Another family, the taeniolabids, were larger, similar in size
to beavers, and heavily built, suggesting that they were fully terrestrial. Some
multituberculates have adaptations for eating wood, particularly shown in the enlarged
front teeth [41] [42]. The euharamiyids are a group thought to be closely related to the
multuberculates and seem to have included some of the first herbivorous mammals. Some
species showed elongated limbs and tails, similar to modern squirrels, suggesting a
scansorial lifestyle [43].
The eutriconodonts were another diverse groups. Fossorial and scansorial
behaviors seem to have been common in the eutriconodonts, as demonstrated by long
legs and tails and the ability to abduct and adduct their big toes [44]. Scansorial traits may
have become exaptations for gliding in the eutriconodont Volaticotherium, which shows
convergence with modern sugar gliders and flying squirrels [45]. Scansorial adaptations
are also widespread in other linneages, including early therians Henkelotherium and
Eomaia, and the early metatherian Sinidelphis [3] [41] [42] [44] [46].
An interesting mammal from the Late Jurassic of North America of uncertain
affinities is Fruitafossor. It seem have adaptation for feeding on ant and termites
(myrmecophagy) and has many convergent characteristics with anteaters and aardvarks
[3] [47]. Basal mammaliamorph tritylodontids have balde like teeth with suggested that
they ate leaves [48] [49].
Predation and scavenging are also represented in Castorocauda [38], and basal
mammaliamorph Sinoconodon, shown in their large canines and strong jaws [50]. Another
very interesting find is a relatively large gobiconodont, Repenomamus, which was found
with a juivinile Psittacosaurus preserved in its stomach, showing that some Mesozoic

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mammals were carnivorous and prayed on small vertebrates, such as young dinosaurs
[51] [52] [53].
What this ecomorphological diversity tells us about the patterns of evolution and
adaptive radiation in early mammals is of particular importance. Mammal evolution seems
best characterized not by long branches with little ecomorphological diversity stretching
deep into the Mesozoic, but lots of short lived branches coupled with ecological
specialisation, representing many successive episodes or waves of diversification and
adaptive radiation throughout the Mesozoic (Figure 2a) [3]. These short lived, dead-end
lineages iteratively evolved developmental homoplasies and convergent ecological
specialisations, parallel to those in modern mammal groups (Figure 2b) [3]. This means we
can see successive lineages adapting into similar niches and evolving similar
morphologies at different times during the Mesozoic, long before the analogous modern
mammals [3] [24]. It seems that “correlation of ecomorphological specialisations with
phylogenetic splitting is a basic feature of Mesozoic mammal evolution” [3].
Concluding remarks
While there is still some truth in the stereotype of Mesozoic mammals being small,
generalised insectivores, there is much more ecomorphological diversity and niche
specialization in these mammals than was previously known. A range of different diets,
feeding ecologies and adaptations for various niches are exhibited, including
insectivorous, herbivorous, myrmecophagous, carnivorous, fossorial and scansorial
lifestyles, and even adaptations for swimming and gliding. We also see lots of short-lived
lineages representing burst of iterative evolution through-out the Mesozoic, rather than
long branches with little ecomorphological diversity. There are now a range of techniques

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which can be integrated to continue to shed light on this area of evolutionary history, as
well as many others.
Future research should concentrate on using these techniques and applying them
to a wider range of fossils to try and build a more complete picture of the ecomoprhological
diversity of Mesozoic mammals. Most research up to now has largely been looking at
comparative morphology, with many of these analytical techniques having been used only
in limited contexts. In particular, the use of FEA in vertebrate biomechanics, especially
applied to extinct organisms, in still in its infancy, and has yet to be applied to a wide range
of living animals, let alone fossil organisms. Further research would be needed to further
validate the approach. Also, few studies have combined this with other techniques (with
the notable execption of Gill et al. 2014), and it would therefore be important to use this
integrated approach on many different fossil samples in the future.
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Box 1. Origin of Mammals
The first fully terrestrial vertebrates were the amniotes. Unlike earlier tetrapods, they had eggs with
internal membranes, allowing the embryo to breath while still retaining water [54] [55], and the eggs laid
on dry. They arose in the Late Carboniferous and split into two lineages, Sauropsida (reptiles and birds),
and Synapsida [7] [56] [57] [58]. Mammals fall within the Clade Synapsida [6], which also includes many
other extinct taxa traditionally called ‘mammal-like reptiles’. Synapsids are characterised by having a
single temporal fenestra behind each eye orbit, and differentiated teeth [6] [59] [60]. They came to
dominate the terrestrial fauna in the Permian, with the ‘pelycosaurs’ dominating the Early Permian, and
the more advanced therapsids dominating the Late Permian [6].
The therapsids differed from earlier pelycosaurs in several features of the skull, including larger temporal
fenestrae and incisors of equal size. The therapsid lineage leading to mammals gradually changed from
pelycosaurs-like animals, to mammal-like animals. Acquisition of mammalian traits included the gradual
development of a bony secondary palate, which may have been involved in the development of a faster
metabolism; the dentary becoming the main bone of the lower jaw, with the reduction of other lower jaw
bones (which would eventually form the bones of the middle-ear); and the evolution of erect limb posture
(although this process was erratic; indeed, modern monotremes still have a semi-sprawling gait) [8].
The Permian-Triassic extinction wiped out the majority of synapsids, with only three therapsid clades
surviving, the dicynodonts, therocephalians, and cynodonts [61]. However, the remaining synapsids were
soon overtaken as the dominant land vertebrates by the archosauran sauropsids during the ‘Triassic
takeover’ [62]. The archosaurs may have been able to diversify and radiate more quickly than synapsids
due to glandless skin and ability to eliminate nitrogenous waste as a solid uric acid paste with very little
water. This would have been an advantage over the synapsids, which excreted urine with lots of water, in
the increasingly dry climate [9].
The therocephalians only lasted into the early Triassic, and the dicynodont went extinct by the end of the
Triassic, leaving the cynodonts as the only living synapsid lineage. The clade Eucynodontia, was divided
into two clades, Cynognathia (such as Cynognathus) and the Probainognathia [63]. During the late
Triassic, most of the large cynodonts disappeared, and the remaining became smaller and increasingly
mammal-like. The probainognathans gave rise to the mammaliaforms at the Late Triassic [48] [64].

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Box 2. What is a mammal?
The exact definition of Mammalia is not entirely uniform [65]. Some authors restrict the term Mammalia to
grown group mammals only (the group comprising of the common ancestor of all modern mammals and
of all its decedents – sometimes referred to as ‘true mammals’) [2] [66]. Basal families, such as the
morganucodonts, docodonts and kuehneotherians, are not included in this definition. To accommodate
those taxa falling outside this group, but which are more closely related to crown group mammals than to
any other taxa, the group Mammaliaformes was defined as comprising “the last common ancestor of
Morganucodontidae and Mammalia and all its descendants”. Some tradition, trait-based mammalian
taxa, such as Abelobaselius and Sinoconodon still fall outside of this definition. They are therefore
included with the grouped Mammaliamorpha, defined as the clade originating with the last common
ancestor of Tritylodontidae and the crow group mammals (Figure i) [2] [66].
Figure i. Mammaliamorph cladogram
However, many authors continue to use the traditional, morphological definition, which includes all of the
non-mammalian mammaliaforms as mammals [6] [64]. Other authors do not define mammals by the
crown group. For example, Kielan-Jawrowska et al. (2004) define Mammalia as the group originating
with the last common ancestor of Sinoconodon and living mammals, which would therefore include most
of the mammaliaforms within Mammalia [37].
The basal mammaliamorphs include the tritylodontids, Adelobasileus and Sinoconodon. The tritylodonts
were small, highly mammal-like, and are the most basal mammaliamorphs, although they retained the
reptilian quadrate-articular joint. They arose at the end of the Late Triassic and disappeared in the Late
Cretaceous [48] [67]. Adelobasileus is from the Late Triassic of Texas, and only known from a partial
skull. Its distinct cranial feature indicate it being close to mammals, possibly close to the common
ancestor of mammals, with some authors originally describing it as the oldest known mammal [49] [68].
Sinocnbodon was from the Early Jurassic, and had a dentary-squamosal jaw joint. This would put it
closer to mammals than the morganucodnts, however it was polyphylodont, like reptiles, and may thus
be more basal. It is possible that the jaw joint evolved independently [37] [69].

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Box 3. Mesozoic Mammaliaforms
The morgnucodonts, named after the type species Morganucodon watsoni, were some of the first
mammaliaforms, appearing at the end of the Triassic, and are considered the most basal of the
mammaliaforms. They had an unusual ‘double-joint’ jaw structure, with the jaw articulation being made
up of a dentary-squamosal joint as well as a quadrate-articular joint [70]. The articular and the quadrate
would become the melleus and the incus in modern mammals. The double joint clearly shows the
transition from a ‘reptile-like’ jaw to a ‘mammalian-like’ jaw. Morganucodonts were also diphyodont
(having only two sets of teeth, like modern mammals), and the postcanine teeth were replaced with
molars and premolars, as in modern mammals [71].
The docodonts arose during the Middle Jurassic, and were among the most common mammaliaforms
until the Early Cretaceous, and exhibited a fair degree of diversity. They are distinguished by their
relatively sophisticated set of molars [72]. They are generally insectivorous or herbivorous.
Hadrocodium from the Early Jurassic may be very close the origin of mammals. Its jaw consists of only
the squamosal and dentary bones, with the articular and quadrate bones forming a nearly complete
middle-ear structure. It also had a relatively large brain case [50].
Comprising of the traditional clade ‘Symmetrodonta’ along with Kuehneotherium and Woutersia, the
kuehneotherians form the Late Triassic to Early Jurassic are known only from teeth and a few jaw
fragments. They are also potentially very close to the origin of mammals, with evidence from teeth
putting them closer to mammals than Hadrocodium [24] [69], although Kuehneotherium seems to retain
the plesiomorphic articular-quadrate jaw join, which would suggest it be more basal [37].
Kuehneotherium also appeared to specialise in eating soft bodied insects, such as moths [24].

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Box 4. Crown-group Mammals
Auatralosphenida contains the monotremes (such as modern echidnas and platypus) and the enigmatic
clade Ausktribosphenidae [6]. The ausktribosphenids are strange in having tribosphenic molars,
otherwise only found in therians [73]. However, they come from the Early to Middle Cretaceous of
Australia, whereas the therians were confined in the northern hemisphere until much later. Therefore
their position within mammals is uncertain [69] [74]. The australosphenids represent the most basal
crown-group mammals, originating in the Early to Middle Jurassic, with Asfaltomylos being a potential
basal member, and were once widespread in the southern hemisphere [75]. Teinolophos and
Steropodon of the Early Cretaceous are the earliest monotremes.
Figure ii. Grown-group mammal cladogram
The eutriconodonts and the multitubercilates were the most common and diverse mammals of the
Mesozoic, with cosmopolitan distributions [76]. The eutriconodonts were named for their molars with
three main cusps in a row, and were a diverse group which occupied a variety of niches. The
multituberculates are so named for the multiple tubercles on their molars, and share many convergent
characteristics with rodents, often being called the ‘rodents of the Mesozoic’ [6] [37] [41]. They were very
diverse and existed for around 120 million years, from the late Jurassic [77] to the early Oligocene, when
they were outcompeted by rodents. There is also some evidence, based on the shape of the pelvic
bones, that the multituberculates gave birth to tiny, undeveloped young, similar to modern marsupials
[37] [41].
Most analyses place the multituberculates as being closer to therians than eutriconodonts, though some
authors have found that the multituberculates fall outside of crown-group mammals, perhaps even further
than the morganucodonts [42]. Others have put the eutriconodonts as closer to therians, within the clade
Holotheria [44] [78] [79]. The multituberculates, along with the gondwanatherians and haramiyids, form
the large and diverse group Allotheria, forming a sister group to Holotheria (which includes therians and
relatives) (Figure ii) [42] [69].
Theria contains eutherians and metatherians. They are characterised as having no clavicle or coracoid
bones, and having tribospenic molars and a crurotarsal-like ankle joint. The metatherians include
marsupials, as well as related extinct groups. The oldest know metatherian is Sinodelphis, from the Early
Cretaceous of China. The eutherians include placental mammals, as well as various extinct groups. The
oldest known eutherians are Juramaia from the Late Jurassic and Eomaia from the Early Cretaceous [6]
[37]. The oldest confirmed placental is Protungulatum, dating to the K-Pg boundary [80].

26
Figure 1. Steps in finite element analysis. From Rayfield (2007).

27
Figure 2. Diversity of Mezoic mammals. a) Phylogenies showing successive radiations of mammaliforms
through the Mesozoic. b) Ecomorpholotypes of Mesozoic mammals in comparison to modern analogues,
showing small, insectivorous stereotype and many newly discovered ecomorphologypes. Also shows
iterative evolution. From Luo (2007).
A
B

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Glossary
Adaptive radiation: process whereby organisms diversify rapidly, filling many new
ecological niches. Cf. radiation.
Amniote: tetrapods with eggs that have an amnion, allowing eggs to be laid on land.
Includes modern day reptiles, birds and mammals.
Apomorphy: or derived state, an innovation which can be used to diagnose a clade.
Apomorphies derived in individual taxa are autapomorphies, and do not express anything
about relationships between groups. Synapomorphies are apomorphies which are shared
by two or more taxa and inferred to have been present in the most recent common
ancestor, but whose own ancestor lacked them. Synapomorphies can show relationships
between taxa.
Arborealism: living in trees
Archosaurs: group of diapsid reptiles, including dinosaurs (and modern day birds) and
crocodilians among others.
Canines: long, pointed teeth used to hold food to tear it apart.
Carnassials: large teeth in many carnivorous animals used for shearing flesh. Modified
fourth upper premolar and first lower molar.
Carnivory: deriving nutrition primarily from animal tissue.

29
Cladistics: biological classification where organisms are grouped together based on
shared characteristics that come from the groups last common ancestors. Cf.
phylogenetics.
Cladogram: tree diagram used in cladistics to show relations among organisms.
Convergent evolution: independent evolution of similar characters in different lineages.
Known as homoplasy in cladistics.
Crown group: in cladistics and phylogenetics, a group which contains modern
representatives, there most recent common ancestor, and all of its descendants.
Cynodonts: a group of mammals-like therapsids, first appearing in the Late Permian.
Includes mammals.
Dentary-squamosal joint: joint between the dentary bone in the lower jaw, and the
squamosal bone in the back of the skull. Jaw joint typical of mammals.
Diapsids: amniotes with two temporal fenestrae in each side of the skull. Includes reptiles
and birds.
Discretisation: process of breaking down a continuous structure into discrete parts.

30
Ecomorphology: the relationship between the ecological role of an organism and its
morphology or morphological adaptations.
Exaptation: shift in function of a trait during evolution.
Fossorial: organisms adapted to digging and living underground.
Generalised: uspecialised, exploits a variety of different ecological niches.
Herbivory: deriving nutrition primarily from plant matter.
Heterodont: having differentiated teeth/ different kinds of teeth.
Homoplasy: see convergent evolution.
Incus: bone in the mammalian middle ear, developed from the quadrate bone. Cf.
quadrate- articular joint.
Insectivory: deriving nutrition primarily from insects.
Malleus: bone in the mammalian middle ear, developed from the articular bone. Cf.
quadrate- articular joint.
Mammaliaforms: group of cynodonts containing mammals. See Box 2.

31
Mammaliamorphs: group of cynodonts containing mammaliforms. See Box 2.
Mesozoic: geological era lasting from 252 to 66 mya. Often called the age of reptiles or
the age of the dinosaurs. Dinosaurs (including birds), mammals, crocodilians, pterosaurs
and marine reptiles evolved during this time. Many of these groups went extinct at the end
of the Mesozoic, with mammals, birds and crocodilians surviving.
Monophyly: in pylogenetics and cladistics, a clade which includes and ancestral species
and all of its descendants. Mammals (Class Mammalia) are monophyletic.
Morphology: physical form and structure of an organism.
Myrmecophagy: feeding primarily on ants or termites.
Opsin: group of light sensitive proteins in the photoreceptor cells of the retina.
Paraphyly: a clade or group consisting of a common ancestor and some of its
descendants, but not others. The traditional grouping of reptiles (Class Reptilia) is
paraphyletic as it doesn’t include birds or mammals, but does include their ancestors, and
the most recent common ancestor between them and modern reptiles. Paraphyletic
groups are discouraged in cladistics and phylogenetics, although they are sometimes
useful, especially in relation to stem lineages and evolutionary grades.
Pelycosaurs: paraphyletic group of ‘primitive’ synapsids, contrasted with the more
‘advanced’ therapsids.

32
Plesiomorphy: or ancestral state, character state that a taxon has retained from its
ancestors. When two or more taxa that are not nested within each other share this a
plesiomorphy, it is called a symplesiomorphy. Cf. apomorphy.
Piscivorous: primarily feeding on fish.
Quadrate-articular joint: joint between the quadrate bone in the lower jaw, and the
articular bone in the back of the skull. Jaw joint typical of reptiles. Quadrate and articular
bones become the incus and malleus bones of the mammalian middle ear respectively.
Radiation: see adaptive radiation
Sauropsids: group of amniotes containing diapsids and relatives, and possibly anapsids
such as turtles.
Scansorial: lifestyle where the animal is adapted or specialised for climbing.
Secondary palate: anatomical structure which divides the nasal and oral cavities.
Specialised: adaptived to exploit specific niche.
Synapsids: amniotes with one temporal fenestra in each side of the skull. Includes
mammals and their extinct relatives (often referred to as ‘mammal-like reptiles’)

33
Taxon: groups of organisms which form a unit, e.g. species, family, class etc.
Temporal fenestrae: openings in the temporal bone in vertebrate skulls.
Therapsids: group of synapsids. More ‘advanced’ (or derived) in contrast to ‘pelycosaurs’.
Volant: capable of flying of gliding.

Ecomorphological diversity of Mesozoic mammals

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