Zhe-Xi Luo

The earliest known eutherian mammal

The skeleton of a eutherian (placental) mammal has been discovered from the Lower Cretaceous Yixian Formation of northeastern China. We estimate its age to be about 125 million years (Myr), extending the date of the oldest eutherian records with skull and skeleton by about 40–50 Myr. Our analyses place the new fossil at the root of the eutherian tree and among the four other known Early Cretaceous eutherians, and suggest an earlier and greater diversification of stem eutherians that occurred well before the molecular estimate for the diversification of extant placental superorders (104–64 Myr). The new eutherian has limb and foot features that are known only from scansorial (climbing) and arboreal (tree-living) extant mammals, in contrast to the terrestrial or cursorial (running) features of other Cretaceous eutherians. This suggests that the earliest eutherian lineages developed different locomotory adaptations, facilitating their spread to diverse niches in the Cretaceous.

Transformation and diversification in early mammal evolution

Evolution of the earliest mammals shows successive episodes of diversification. Lineage-splitting in Mesozoic mammals is coupled with many independent evolutionary experiments and ecological specializations. Classic scenarios of mammalian morphological evolution tend to posit an orderly acquisition of key evolutionary innovations leading to adaptive diversification, but newly discovered fossils show that evolution of such key characters as the middle ear and the tribosphenic teeth is far more labile among Mesozoic mammals. Successive diversifications of Mesozoic mammal groups multiplied the opportunities for many dead-end lineages to iteratively evolve developmental homoplasies and convergent ecological specializations, parallel to those in modern mammal groups.

A Jurassic eutherian mammal and divergence of marsupials and placentals

Placentals are the most abundant mammals that have diversified into every niche for vertebrates and dominated the world’s terrestrial biotas in the Cenozoic. A critical event in mammalian history is the divergence of eutherians, the clade inclusive of all living placentals, from the metatherian–marsupial clade. Here we report the discovery of a new eutherian of 160 Myr from the Jurassic of China, which extends the first appearance of the eutherian–placental clade by about 35 Myr from the previous record, reducing and resolving a discrepancy between the previous fossil record and the molecular estimate for the placental–marsupial divergence. This mammal has scansorial forelimb features, and provides the ancestral condition for dental and other anatomical features of eutherians.

Dual origin of tribosphenic mammals

Marsupials, placentals and their close therian relatives possess complex (tribosphenic) molars that are capable of versatile occlusal functions. This functional complex is widely thought to be a key to the early diversification and evolutionary success of extant therians and their close relatives (tribosphenidans). Long thought to have arisen on northern continents, tribosphenic mammals have recently been reported from southern landmasses. The great age and advanced morphology of these new mammals has led to the alternative suggestion of a Gondwanan origin for the group. Implicit in both biogeographic hypotheses is the assumption that tribosphenic molars evolved only once in mammalian evolutionary history. Phylogenetic and morphometric analyses including these newly discovered taxa suggest a different interpretation: that mammals with tribosphenic molars are not monophyletic. Tribosphenic molars evolved independently in two ancient (holotherian) mammalian groups with different geographic distributions during the Jurassic/Early Cretaceous: an australosphenidan clade endemic to Gondwanan landmasses, survived by extant monotremes; and a boreosphenidan clade of Laurasian continents, including extant marsupials, placentals and their relatives.

Fossil Evidence on Origin of the Mammalian Brain

Evidence from two early fossils suggests that brain enlargement and specialization proceeded in three pulses. Many hypotheses have been postulated regarding the early evolution of the mammalian brain. Here, x-ray tomography of the Early Jurassic mammaliaforms Morganucodon and Hadrocodium sheds light on this history. We found that relative brain size expanded to mammalian levels, with enlarged olfactory bulbs, neocortex, olfactory (pyriform) cortex, and cerebellum, in two evolutionary pulses. The initial pulse was probably driven by increased resolution in olfaction and improvements in tactile sensitivity (from body hair) and neuromuscular coordination. A second pulse of olfactory enhancement then enlarged the brain to mammalian levels. The origin of crown Mammalia saw a third pulse of olfactory enhancement, with ossified ethmoid turbinals supporting an expansive olfactory epithelium in the nasal cavity, allowing full expression of a huge odorant receptor genome.

A swimming mammaliaform from the Middle Jurassic and ecomorphological diversification of early mammals.

A docodontan mammaliaform from the Middle Jurassic of China possesses swimming and burrowing skeletal adaptations and some dental features for aquatic feeding. It is the most primitive taxon in the mammalian lineage known to have fur and has a broad, flattened, partly scaly tail analogous to that of modern beavers. We infer that docodontans were semiaquatic, convergent to the modern platypus and many Cenozoic placentals. This fossil demonstrates that some mammaliaforms, or proximal relatives to modern mammals, developed diverse locomotory and feeding adaptations and were ecomorphologically different from the majority of generalized small terrestrial Mesozoic mammalian insectivores.

A new symmetrodont mammal from China and its implications for mammalian evolution

A new symmetrodont mammal has been discovered in the Mesozoic era (Late Jurassic or Early Cretaceous period) of Liaoning Province, China. Archaic therian mammals, including symmetrodonts, are extinct relatives of the living marsupial and placental therians. However, these archaic therians have been mostly documented by fragmentary fossils. This new fossil taxon, represented by a nearly complete postcranial skeleton and a partial skull with dentition, is the best-preserved symmetrodont mammal yet discovered. It provides a new insight into the relationships of the major lineages of mammals and the evolution of the mammalian skeleton. Our analysis suggests that this new taxon represents a part of the early therian radiation before the divergence of living marsupials and placentals; that therians and multituberculates are more closely related to each other than either group is to other mammalian lineages; that archaic therians lacked the more parasagittal posture of the forelimb of most living therian mammals; and that archaic therians, such as symmetrodonts, retained the primitive feature of a finger-like promontorium (possibly with a straight cochlea) of the non-therian mammals. The fully coiled cochlea evolved later in more derived therian mammals, and is therefore convergent to the partially coiled cochlea of monotremes.

A new eutriconodont mammal and evolutionary development in early mammals

Detachment of the three tiny middle ear bones from the reptilian mandible is an important innovation of modern mammals. Here we describe a Mesozoic eutriconodont nested within crown mammals that clearly illustrates this transition: the middle ear bones are connected to the mandible via an ossified Meckel’s cartilage. The connected ear and jaw structure is similar to the embryonic pattern in modern monotremes (egg-laying mammals) and placental mammals, but is a paedomorphic feature retained in the adult, unlike in monotreme and placental adults. This suggests that reversal to (or retention of) this premammalian ancestral condition is correlated with different developmental timing (heterochrony) in eutriconodonts. This new eutriconodont adds to the evidence of homoplasy of vertebral characters in the thoraco-lumbar transition and unfused lumbar ribs among early mammals. This is similar to the effect of homeobox gene patterning of vertebrae in modern mammals, making it plausible to extrapolate the effects of Hox gene patterning to account for homoplastic evolution of vertebral characters in early mammals.

A Jurassic mammaliaform and the earliest mammalian evolutionary adaptations

The earliest evolution of mammals and origins of mammalian features can be traced to the mammaliaforms of the Triassic and Jurassic periods that are extinct relatives to living mammals. Here we describe a new fossil from the Middle Jurassic that has a mandibular middle ear, a gradational transition of thoracolumbar vertebrae and primitive ankle features, but highly derived molars with a high crown and multiple roots that are partially fused. The upper molars have longitudinal cusp rows that occlude alternately with those of the lower molars. This specialization for masticating plants indicates that herbivory evolved among mammaliaforms, before the rise of crown mammals. The new species shares the distinctive dental features of the eleutherodontid clade, previously represented only by isolated teeth despite its extensive geographic distribution during the Jurassic. This eleutherodontid was terrestrial and had ambulatory gaits, analogous to extant terrestrial mammals such as armadillos or rock hyrax. Its fur corroborates that mammalian integument had originated well before the common ancestor of living mammals.

Relationships of Cetacea to Terrestrial Ungulates and the Evolution of Cranial Vasculature in Cete

Concomitant with the evolution of numerous aquatic adaptations, extant cetaceans have developed a cranial vascular system that is very different from those of terrestrial mammals. Terrestrial mammals rely on the internal carotid, external carotid, and vertebral arteries for blood supply to the brain. In extant cetaceans, however, these cranial vessels are either lost or extremely reduced early in ontogeny (such as the internal carotid and its branch the stapedial artery), or ramify along part of their course into anastomotic networks of small arteries (such as the vertebral artery and branches of the external carotid). These networks of arteries, and their morphologically similar complexes of veins, are termed retia mirabile, “wonderful nets.” In contrast to the typical ungulate cranial circulation in which a few large arteries make up the main supply channels to the brain, the cetacean cranial circulation is characterized by a series of the retia mirabile. The cranial vascular patterns of cetaceans (Boenninghaus, 1904; Slijper, 1936; Walmsley, 1938; Vogl and Fisher, 1981a) are so different from those of terrestrial eutherian mammals (Sisson, 1921; Miller et al., 1964; Bugge, 1974; Gray, 1974; Hunt, 1974; Presley, 1979; MacPhee, 1981; Wible, 1987) that they have attracted the attention of morphologists since the first half of the nineteenth century (Breschet, 1836; Stannius, 1841).