Gareth Coleman gc12847 EASC30048 Palaeobiology Analytical Project Literature Review 1 The Ecomorphological diversity of Mesozoic mammals Gareth Andrew Coleman [email protected]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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Gareth Coleman gc12847 EASC30048 Palaeobiology Analytical Project Literature Review
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The Ecomorphological diversity of Mesozoic mammals
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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].
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Figure 1. Steps in finite element analysis. From Rayfield (2007).
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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.
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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.
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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.
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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.
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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’)
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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’.