Athena Review Vol. 5, no. 1
Records of Life: Fossils as Original Sources
24. Stem Mammals
By the late Triassic, the Therapsid
carnivores such as Diarthrognathus had become small, about the size of a weasel or rabbit. The
majority of the mammal species that existed in the Mesozoic Era were
nocturnal insectivores, the direct ancestors of multituberculates and
primates.Mammals are first seen in the fossil record at the end of the Triassic period and in the Early Jurassic period (225-180 mya) with close ties to the cynodont Tritylodontidae taxa previously described. In terms of their overall development from cynodonts, mammals are currently defined by paleontologists as the common ancestry of all extant mammals and Sinoconodon. The latter, found in Yunnan province, China, is considered as the most basal of mammal-like cynodonts (Kielan-Jaworoska et al. 2004). Sinocodon is one of several "stem" mammals, whose fossil attributes show a clear transition between advanced cynodonts of the Middle and Upper Triassic, and the earliest mammals.
Fig.1: Relations of stem mammals, leading from mammaliaformes to mammals.
Other stem mammals, described below, include the genera Adelobasileus and Hadrocodium, and the families of morgonucodonts and docodonts, each with several genera. These do not comprise a closely related or monophyletic group, but are resolved into a series of branches or clades ranked in successively closer order to the main, or crown mammal group, in the following order (fig.1) Adelobasileus, Sinoconodon, morganucodonts, docodontans, and Hadriocodium (Luo et al. 2002; Kielan-Jaworoska et al. 2004).
Sinoconodon
Sinoconodon ("Chinese tooth") is a small stem mammal dating from the early Jurassic period (208-191 mya). Sinoconodon is regarded as the most basal of the mammaliaforms, and the sister−taxon to a clade that includes Mo
rganucodon and the living mammals (fig.1; Luo et al
2002). Sinoconodon rigneyi appears in the fossil record of Yunnan province, China in the dark red beds of the Lower Lufeng Series, representing the Sinemurian stage of the Early Jurassic period (193 mya). Its holotype consists of a poorly preserved skull (fig.2) and post-cranial fragments from several individuals. Three other species of Sinoconodon have also been defined from the Lower Lufeng Series.
Fig.2: Skull of Sinoconodon rigneyi (after Patterson and Olson 1961)
Its anatomy shows a unique combination of reptilian and mammalian features. The skull length of Sinocodon was 22-62 mm, and its body weight estimated from 13 to 517 grams. Regarding the development of the middle ear, a key early mammalian trait, S. rigneyi had three petrosal bones, but only the stapes was inside the ear. The incus and malleus still formed part of a multi-boned lower jaw. It possessed a secondarily evolved jaw joint between the dentary and the squamosal bones, which had replaced the primitive reptilian joint between the articular and quadrate bones. It retained the double jaw joint seen in other advanced Cyndonts. Here, however, while the reptilian jaw joint was still present (though tiny), the mammalian jaw joint was stronger, with a large dentary condyle fitting into a distinct fossa on the squamosal. This refinement of the jaw joint is the main criterion for identifying Sinoconodon as a Mammaliaform.
Its eye socket was now fully mammalian, with a closed medial wall. It has an expanded hindbrain, one of the key traits of early mammals. Although the animal appears closely related to more mammalian Morganucodon, it differed substantially from it in in its dental and growth habits. Like mammals, it had permanent cheekteeth or molars. At the same time, like the reptiles, Sinocodon was polyphyodont, replacing many of its teeth throughout its lifetime, and it seems to have grown slowly but continuously until its death. Even the smallest known individuals had already began the teething cycle in their front teeth.
Adelobasileus
Fossils of Adelobasileus cromptoni were discovered by Lucas and Hunt
(1990) in Texas in the form of a partial cranium or skull, and teeth.
The fossils were found near Kalgary in Crosby County, Texas in layers
from the Tecovas Member of the Dockum Formation, dated as Late Triassic
(Late Carnian phase), about 225 mya. The Adelobasileus fossils
are thus considered at least ten million years older than than those of
any previously described, proposed mammal (Lucas and Luo
1993). The skull fragment of Adelobasileus (fig.3), about 1.7 cm long, represents a very small animal. While the lower, rear part of the skull (basicranium) shares numerous traits with early Jurassic mammals, other cranial features such as the petrosal region, which has only a small or incipient promontorium housing the ear cochlea, indicate only an intermediate stage of the character transformation from non-mammalian cynodonts to mammals. Since the full development of the mammalian ear is not present, Adelobasileus has been excluded from the group including Sinocodon and all extant mammals (Lucas and Luo 1993; Luo et al. 2002). The fossil remains of Adelobasileus are presently considered insufficient for any more precise identification (Kielan-Jarowoska et al. 2004).
Fig.3: Skull fragment of Adelobasileus cromptoni (after Spencer and Luo 1993).
Morganucodonts
Morganucodonts ("Morgan's tooth"), named for a site in Glanmorgan, Wales, includes some of the earliest and most widespread mammalians from the the Late Triassic to Middle Jurassic (~ 220-180 mya). Three main genera are known, Morganucodon, Eozostrodon, and Haldanodon, representing a diverse family with global distribution in the northern hemisphere (Laurasia), as well as Africa and India in the southern, Gondwanan region (Kielan-Jaworoska et al. 2004).
The species Morganucodon watsoni was discovered and named in 1949 by Walter Georg Kuhne from fossils found in fissure fillings of Duchy Quarry in Glanmorgan, later dated by Kermack et al. (1981) to be from the Early Jurassic Sinemurian phase (200-190 mya). Kuhne also found tooth fossils from this period at the Holwell Quarry in England of the related Eozostrodon genus. Other Morganucodonts have since been found in Switzerland and France showing a high level of species diversity (Clemens 1986; Kielan-Jaworoska et al. 2004). In China, 1941 explorations in the Lower Lufang formation in Yunnan province revealed a complete skull of Morganucodon, i
dentified by E.T. Oehler in 1948, and later described
by W. H. Rigney as Morganucodon oehleri (fig.4). Additional taxa of Morganucodonts have been found in South Africa, including Megazostrodon (Crompton and Jenkins 1968). t Megazostrodon has a well-developed lingual cingulum and cingular cusps on the lower molars showing possible links to Docadonta, Other, more isolated examples of Morganucodonts have been found in Greenland (Jenkins et al 1994), and central Russia (Gambarayan and Averianov 2001; Kielan-Jaworoska et al. 2004).
Fig. 4: skull of Morganucodon oehleri (after Rowe et al. 2001)
Morganucodonts were small, with skulls 27-38 mm long and body weight estimated at ranging from 27-80 grams (Luo, Crompton, and Sun 2001). They have many features in their skull representing general mammalian traits, which first appear in morganocodonts (in cladistic terms, are primitive to them). Like some advanced cynodonts, they have a double or compound jaw joint. This includes the mammalian joint, with the condyle or knob of the dentary bone in articulation with the recess or fossa of the squamosal bone ( the primary diagnostic feature for early mammals). It also includes a retention of the reptilian jaw joint between the articular and quadrate bones. In their skull anatomy, the orbit around the eye (orbitosphenoid region) is fully enclosed, as in all mammals.
In their basioccipital region (lower back of the skull), there is a petrosal area with a small mound or promontorium, a trait shared by mammals and some advanced cynodonts. There too, in the area of the ear and petrosal, is a juncture of small postdentary bones. In Morganucodon, these bones, notably, lie enclosed in a postdentary trough, which is a primitive character of non-mammalian cynodonts (Kermack et al. 1973; Kielan-Jaworoska et al. 2004). The trough forms a concavity on the side of the mandible, into which fits the angular bone and the malleus, part of the middle ear (Crompton and Luo 1993).
Fig.5: Lower jaw of Morganucodon, showing Meckel's groove and the post-dentary trough.
A diagnostic feature of reptilian jaws called Meckel's groove (fig.5), which contains Meckel's cartilage, appears in mammals only during early weeks of embryonic growth around the development of the ear region. An attenutated version of Meckel's groove is also present in the adult Morganucodonts, as a primitive feature extending forward from the postdentary trough. These (the postdentary trough, and Meckel's groove) are among the most diagnostic landmarks of the lower jaw bones, which enable the accurate classification of fossils as either early mammals, mammaliformes (called stem mammals), cynodonts, or other non-mammals. In the case of morganuconodonts, both Meckel's groove and the angular bone in the trough are more reduced than in Sinoconodon or nonmamalian cynodonts (Luo 1994; Kielan-Jaworoska et al. 2004).
In many aspects, the teeth of morganucodonts are also distinct from those of Sinoconodon. Morganucodonts do not have multiple replacement of anterior teeth, a primitive trait found in Sinocodon and synodonts, and today retained by reptiles. Also unlike the latter, the cheek teeth of morganucodonts are divided into triangular-cusped molars and premolars, which have precise occlusion or surface matching in upper and lower teeth (Crompton 1974). All three traits - the lack of multiple tooth replacement, division of cheek teeth in molars and premolars, and precise occlusion of cheek teeth - are all fully mammalian. Based on some primitive cranial features, however, such as retention of the double jaw joint, and some postcranial elements, Morganucodonts are not included in the large group of mammals related to today's mammals (called the Crown Mammallia, in cladistic parlance) (Luo et al. 2002).
Docodonta
Docodonts are considered to be one of the most archaic mammalian groups. Their remains were first discovered more than a century ago in the Late Jurassic Morrison Formation of Wyoming and Colorado, where they are found together with the bones of giant sauropod dinosaurs. They have subsequently been discovered at several sites in Europe and Asia. Docodonts are characterized by complicated lower molars. They also had the mammalian dentary-squamosal jaw joint.
Most docodonts are known solely from the dentition, which includes complex, broad cheek teeth. The teeth of docodonts have been cited as evidence that the group evolved from morganucodonts (e.g., Crompton and Jenkins, 1979). The morganucodont Megazostrodon, which has a well-developed lingual cingulum and cingular cusps on the l
ower molars, represents a plausible morphologic stage from which
docodonts might have evolved (Crompton, 1974). Docodonts also evolved precise molar occlusion in
association with their complex molar crowns. Haldanodon, the best-known docodont, was found in Late Jurassic Guimarota lignites (swamp deposits) of Portugal (Lillegraven and Krusat, 1991; Martin and Krebs, 2000). These include dozens of jaws, several skulls, and one skeleton (fig.6). Based on its robust limb skeleton, including a short broad humerus and short, stocky phalanges, this animal was likely adapted for digging. Given the swampy conditions which then prevailed at thise location, Haldanodon may well have been a semi-aquatic, riverine animal (Krusat, 1991; Martin, 2005).
Haldanodon resembles cynodonts in several cranial features that are present in more derived states in morganucodontids. Lillegraven and Krusat (1991) suggested that Haldanodon could have acquired many of its "mammalian" traits earlier than, and independently from, morganucodontids.
Fig.6: Skull of Haldanodon (after Lillegraven and Crusat 1991)
Casterocauda, from the Middle Jurassic of China (Ji et al., 2006), is known from a partial skeleton showing it to be the largest known docodont, almost half a meter long. Its skeleton is adapted for swimming and burrowing, supporting the interpretation that docodonts were semiaquatic. Castorocauda is also the oldest mammal preserving evidence of fur.
Hadrocodium
Hadrocodium is a tiny, early mammaliaform insectivore from the Early Jurassic (195 mya) of China, with a significantly large brain size, indicated by the wide shape of its skull (Luo 2001). The type speceis, Hadrocodium wui ("full head") is named for its very large brain capacity, and for Dr. X-C Wui, discover of the fossil taxon in 1985. The holotype, a nearly complete skull, was found in the Lower Lufang Formation in Yunnan, China, dating from the Sinemurian phase of the Early Jurassic in what was a possibly estuarine enviornment. It was originally classified as Morganucodon sp., then renamed Hadrocodium wui by Luo et al (2001).
With a skull length of only 12 mm, and an estimated body weight of 2 grams, Hadrocodium ranks among the smallest known mammals, and is considered the smallest mammal yet discovered in the Mesozoic. The very small size of Hadrocodium contrasts to its contemporary mammaliaforms such as Sinconodon and Morganucodon, showing diversity in the specialization of triconodont-like insectivores in the Lufeng mammaliaform fauna
Hadrocodium wui has triconodont-like teeth, and is considered by Luo et al (2002) to shed significant light on the evolution of the mammalian middle ear. It is the earliest known taxon that lacks the primitive attachment of the middle ear bones to the mandible but has an enlarged brain vault (suggestive of a large brain).
Fig.7: Skull of Hadrocodum wui (after Luo et al. 2001).
Luo et al. (2002) determined that the brain vault of Hadrocodium is larger than expected for the mammals of its comparable skull width, and far wider than in any other Triassic-Jurassic mammaliaforms, including Sinoconodon, Morganucodon. and Haldanodon (Lillegraven and Krusat 1991). The brain vault in the parietal region in Hadrocodium is comparable to those of Triconodontidae, multituberculates, and the mammalian crown group.
Based on an extensive analysis by Luo et al (2002), Hadrocodium is seen as the sister taxon to the clade of triconodontids and extant Mammalia. Among 15 comparative taxa, it is more closely related to living mammals than are Adelobasileus, Sinoconodon, morganucodontids, and Haldanodon. Hadrocodium shows a key correlation between a) the separation of the middle ear bones from the mandible and b) the expanded brain vault. Its skull features show that several key mammalian evolutionary innovations in the ear region, the temporo mandibular joint, and the brain vault evolved incrementally through mammaliaform evolution, long before the differentiation of the living mammal groups.
This extends the first appearance of these modern mammalian features back to the Early Jurassic, some 45 million years earlier than the next oldest mammals that have preserved such derived features, such as Triconodon from the Late Jurassic. All other nonmammalian mammaliaforms with small brain vaults have retained the mandibular attachment of the middle ear bones, whereas Hadrocodium and living mammals with larger brain vaults have lost the mandibular attachment to the middle ear (Luo et al. 2001)
Crown-Group Mammalia
This group (covered in the next section) is defined by Luo et al. (2002) as the common ancestor of all living mammals and all its descendants. Among other traits shared by all fossil and living members of this clade are the fujlly developed mammalian jaw joint; the mammalian middle ear with three ossicles (malleus, incus, and stapes); presence of four tooth types; presence of occlusal surfaces that match precisely between upper and lower molars upon eruption; and enlarged cerebral hemispheres (Rowe 1988; Rowe and Gauthier 1992; McKenna and Bell 1997).
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