Adaptive radiation of multituberculate mammals before the extinction of dinosaurs

The Cretaceous-Paleogene mass extinction approximately 66 million years ago is conventionally thought to have been a turning point in mammalian evolution. Prior to that event and for the first two-thirds of their evolutionary history, mammals were mostly confined to roles as generalized, small-bodied, nocturnal insectivores, presumably under selection pressures from dinosaurs. Release from these pressures, by extinction of non-avian dinosaurs at the Cretaceous-Paleogene boundary, triggered ecological diversification of mammals. Although recent individual fossil discoveries have shown that some mammalian lineages diversified ecologically during the Mesozoic era, comprehensive ecological analyses of mammalian groups crossing the Cretaceous-Paleogene boundary are lacking. Such analyses are needed because diversification analyses of living taxa allow only indirect inferences of past ecosystems. Here we show that in arguably the most evolutionarily successful clade of Mesozoic mammals, the Multituberculata, an adaptive radiation began at least 20 million years before the extinction of non-avian dinosaurs and continued across the Cretaceous-Paleogene boundary. Disparity in dental complexity, which relates to the range of diets, rose sharply in step with generic richness and disparity in body size. Moreover, maximum dental complexity and body size demonstrate an adaptive shift towards increased herbivory. This dietary expansion tracked the ecological rise of angiosperms and suggests that the resources that were available to multituberculates were relatively unaffected by the Cretaceous-Paleogene mass extinction. Taken together, our results indicate that mammals were able to take advantage of new ecological opportunities in the Mesozoic and that at least some of these opportunities persisted through the Cretaceous-Paleogene mass extinction. Similar broad-scale ecomorphological inventories of other radiations may help to constrain the possible causes of mass extinctions.     

Ferns diversified in the shadow of angiosperms

The rise of angiosperms during the Cretaceous period is often portrayed as coincident with a dramatic drop in the diversity and abundance of many seed-free vascular plant lineages, including ferns. This has led to the widespread belief that ferns, once a principal component of terrestrial ecosystems, succumbed to the ecological predominance of angiosperms and are mostly evolutionary holdovers from the late Palaeozoic/early Mesozoic era. The first appearance of many modern fern genera in the early Tertiary fossil record implies another evolutionary scenario; that is, that the majority of living ferns resulted from a more recent diversification. But a full understanding of trends in fern diversification and evolution using only palaeobotanical evidence is hindered by the poor taxonomic resolution of the fern fossil record in the Cretaceous. Here we report divergence time estimates for ferns and angiosperms based on molecular data, with constraints from a reassessment of the fossil record. We show that polypod ferns (> 80% of living fern species) diversified in the Cretaceous, after angiosperms, suggesting perhaps an ecological opportunistic response to the diversification of angiosperms, as angiosperms came to dominate terrestrial ecosystems.     

Earliest evidence for efficient oral processing in a terrestrial herbivore

Herbivores can increase their digestion rate by mechanically reducing particle size through oral trituration. Groups of terrestrial vertebrates with the greatest capacity to reduce tough plant foods orally are also the most abundant and diverse, as exemplified by ornithopod dinosaurs during the Mesozoic and extant artiodactyl and perissodactyl mammals. Thus, the effective oral processing of high-fibre plant material seems to represent an evolutionary innovation of both functional and macroevolutionary significance. However, evidence for oral processing is poorly documented in the fossil record, especially during the initial stages of terrestrial vertebrate diversification. Here we report on the basal anomodont Suminia getmanovi, the only known Palaeozoic vertebrate in which unequivocal specializations in its cranium and teeth for high-fibre herbivory are well preserved. We propose that the capacity to comminute tough plant foods was critical to the diversification of anomodonts, the most diverse, widely dispersed and abundant group of Palaeozoic terrestrial vertebrates, and to the onset of modern terrestrial ecosystems.     

A Chinese triconodont mammal and mosaic evolution of the mammalian skeleton

Here we describe a new triconodont mammal from the Late Jurassic/Early Cretaceous period of Liaoning, China. This new mammal is represented by the best-preserved skeleton known so far for triconodonts which form one of the earliest Mesozoic mammalian groups with high diversity. The postcranial skeleton of this new triconodont shows a mosaic of characters, including a primitive pelvic girdle and hindlimb but a very derived pectoral girdle that is closely comparable to those of derived therians. Given the basal position of this taxon in mammalian phylogeny, its derived pectoral girdle indicates that homoplasies (similarities resulting from independent evolution among unrelated lineages) are as common in the postcranial skeleton as they are in the skull and dentition in the evolution of Mesozoic mammals. Limb structures of the new triconodont indicate that it was probably a ground-dwelling animal.     

Multiple routes to mammalian diversity

The radiation of the mammals provides a 165-million-year test case for evolutionary theories of how species occupy and then fill ecological niches. It is widely assumed that species often diverge rapidly early in their evolution, and that this is followed by a longer, drawn-out period of slower evolutionary fine-tuning as natural selection fits organisms into an increasingly occupied niche space. But recent studies have hinted that the process may not be so simple. Here we apply statistical methods that automatically detect temporal shifts in the rate of evolution through time to a comprehensive mammalian phylogeny and data set of body sizes of 3,185 extant species. Unexpectedly, the majority of mammal species, including two of the most speciose orders (Rodentia and Chiroptera), have no history of substantial and sustained increases in the rates of evolution. Instead, a subset of the mammals has experienced an explosive increase (between 10- and 52-fold) in the rate of evolution along the single branch leading to the common ancestor of their monophyletic group (for example Chiroptera), followed by a quick return to lower or background levels. The remaining species are a taxonomically diverse assemblage showing a significant, sustained increase or decrease in their rates of evolution. These results necessarily decouple morphological diversification from speciation and suggest that the processes that give rise to the morphological diversity of a class of animals are far more free to vary than previously considered. Niches do not seem to fill up, and diversity seems to arise whenever, wherever and at whatever rate it is advantageous.     

Highly specialized mammalian skulls from the Late Cretaceous of South America

Dryolestoids are an extinct mammalian group belonging to the lineage leading to modern marsupials and placentals. Dryolestoids are known by teeth and jaws from the Jurassic period of North America and Europe, but they thrived in South America up to the end of the Mesozoic era and survived to the beginnings of the Cenozoic. Isolated teeth and jaws from the latest Cretaceous of South America provide mounting evidence that, at least in western Gondwana, dryolestoids developed into strongly endemic groups by the Late Cretaceous. However, the lack of pre-Late Cretaceous dryolestoid remains made study of their origin and early diversification intractable. Here we describe the first mammalian remains from the early Late Cretaceous of South America, including two partial skulls and jaws of a derived dryolestoid showing dental and cranial features unknown among any other group of Mesozoic mammals, such as single-rooted molars preceded by double-rooted premolars, combined with a very long muzzle, exceedingly long canines and evidence of highly specialized masticatory musculature. On one hand, the new mammal shares derived features of dryolestoids with forms from the Jurassic of Laurasia, whereas on the other hand, it is very specialized and highlights the endemic, diverse dryolestoid fauna from the Cretaceous of South America. Our specimens include only the second mammalian skull known for the Cretaceous of Gondwana, bridging a previous 60-million-year gap in the fossil record, and document the whole cranial morphology of a dryolestoid, revealing an unsuspected morphological and ecological diversity for non-tribosphenic mammals.     

A Mesozoic gliding mammal from northeastern China

Gliding flight has independently evolved many times in vertebrates. Direct evidence of gliding is rare in fossil records and is unknown in mammals from the Mesozoic era. Here we report a new Mesozoic mammal from Inner Mongolia, China, that represents a previously unknown group characterized by a highly specialized insectivorous dentition and a sizable patagium (flying membrane) for gliding flight. The patagium is covered with dense hair and supported by an elongated tail and limbs; the latter also bear many features adapted for arboreal life. This discovery extends the earliest record of gliding flight for mammals to at least 70 million years earlier in geological history, and demonstrates that early mammals were diverse in their locomotor strategies and lifestyles; they had experimented with an aerial habit at about the same time as, if not earlier than, when birds endeavoured to exploit the sky.     

Large Mesozoic mammals fed on young dinosaurs

Mesozoic mammals are commonly portrayed as shrew- or rat-sized animals that were mainly insectivorous, probably nocturnal and lived in the shadow of dinosaurs. The largest known Mesozoic mammal represented by substantially complete remains is Repenomamus robustus, a triconodont mammal from the Lower Cretaceous of Liaoning, China. An adult individual of R. robustus was the size of a Virginia opossum. Here we report a new species of the genus, represented by a skeleton with most of the skull and postcranium preserved in articulation. The new species is 50% larger than R. robustus in skull length. In addition, stomach contents associated with a skeleton of R. robustus reveal remains of a juvenile Psittacosaurus, a ceratopsian dinosaur. Our discoveries constitute the first direct evidence that some triconodont mammals were carnivorous and fed on small vertebrates, including young dinosaurs, and also show that Mesozoic mammals had a much greater range of body sizes than previously known. We suggest that Mesozoic mammals occupied diverse niches and that some large mammals probably competed with dinosaurs for food and territory.     

A Jurassic mammal from South America

The Jurassic period is an important stage in early mammalian evolution, as it saw the first diversification of this group, leading to the stem lineages of monotremes and modern therian mammals. However, the fossil record of Jurassic mammals is extremely poor, particularly in the southern continents. Jurassic mammals from Gondwanaland are so far only known from Tanzania and Madagascar, and from trackway evidence from Argentina. Here we report a Jurassic mammal represented by a dentary, which is the first, to our knowledge, from South America. The tiny fossil from the Middle to Late Jurassic of Patagonia is a representative of the recently termed Australosphenida, a group of mammals from Gondwanaland that evolved tribosphenic molars convergently to the Northern Hemisphere Tribosphenida, and probably gave rise to the monotremes. Together with other mammalian evidence from the Southern Hemisphere, the discovery of this new mammal indicates that the Australosphenida had diversified and were widespread in Gondwanaland well before the end of the Jurassic, and that mammalian faunas from the Southern Hemisphere already showed a marked distinction from their northern counterparts by the Middle to Late Jurassic.     

Fast evolution of growth hormone receptor in primates and ruminants

Pituitary growth hormone (GH) evolves very slowly in most of mammals, but the evolutionary rates appear to have increased markedly on two occasions during the evolution of primates and ruminants. To investigate the evolutionary pattern of growth hormone receptor (GHR), we sequenced the extracellular domain of GHR genes from four primate species. Our results suggested that GHR in mammal also shows an episodic evolutionary pattern, which is consistent with that observed in pituitary growth hormone. Further analysis suggested that this pattern of rapid evolution observed in primates and ruminants is likely the result of coevolution between pituitary growth hormone and its receptor.     

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.     

Convergent dental adaptations in pseudo-tribosphenic and tribosphenic mammals

Tribosphenic molars of basal marsupials and placentals are a major adaptation, with the protocone (pestle) of the upper molar crushing and grinding in the talonid basin (mortar) on the lower molar. The extinct pseudo-tribosphenic mammals have a reversed tribosphenic molar in which a pseudo-talonid is anterior to the trigonid, to receive the pseudo-protocone of the upper molar. The pseudo-protocone is analogous to the protocone, but the anteriorly placed pseudo-talonid is opposite to the posterior talonid basin of true tribosphenic mammals. Here we describe a mammal of the Middle Jurassic period with highly derived pseudo-tribosphenic molars but predominantly primitive mandibular and skeletal features, and place it in a basal position in mammal phylogeny. Its shoulder girdle and limbs show fossorial features similar to those of mammaliaforms and monotremes, but different compared with those of the earliest-known Laurasian tribosphenic (boreosphenid) mammals. The find reveals a much greater range of dental evolution in Mesozoic mammals than in their extant descendants, and strengthens the hypothesis of homoplasy of 'tribosphenic-like' molars among mammals.     

A lamprey from the Devonian period of South Africa

Lampreys are the most scientifically accessible of the remaining jawless vertebrates, but their evolutionary history is obscure. In contrast to the rich fossil record of armoured jawless fishes, all of which date from the Devonian period and earlier, only two Palaeozoic lampreys have been recorded, both from the Carboniferous period. In addition to these, the recent report of an exquisitely preserved Lower Cretaceous example demonstrates that anatomically modern lampreys were present by the late Mesozoic era. Here we report a marine/estuarine fossil lamprey from the Famennian (Late Devonian) of South Africa, the identity of which is established easily because many of the key specializations of modern forms are already in place. These specializations include the first evidence of a large oral disc, the first direct evidence of circumoral teeth and a well preserved branchial basket. This small agnathan, Priscomyzon riniensis gen. et sp. nov., is not only more conventionally lamprey-like than other Palaeozoic examples, but is also some 35 million years older. This finding is evidence that agnathans close to modern lampreys had evolved before the end of the Devonian period. In this light, lampreys as a whole appear all the more remarkable: ancient specialists that have persisted as such and survived a subsequent 360 million years.     

卧龙自然保护区的兽类研究

本文记录了卧龙自然保护区的兽类95种或亚种,隶属7目23科65属;分折了兽类区系组成、生态类群与空间的关系、地理分布及其特点,以及种群的相对数量,对进一步研究卧龙的兽类和自然保护管理有理论和实践意义。     

Mammal teeth from the Cretaceous of Africa

We report here the discovery of two mammal teeth from the early Cretaceous of Cameroon. These, and some jaw fragments, all from Cameroon, are the only fossil evidence of mammalian evolution from Africa between late Jurassic and Paleocene, a span of at least 85 million years. A triangular upper tooth lacks the principal internal cusp of marsupials and placentals and is therefore of a similar evolutionary grade to most Jurassic and early Cretaceous therian mammals, but more primitive than the metatherian-eutherian grade. Early Cretaceous, or older, therian mammals are now known from all southern continents except Antarctica. The new find from Cameroon is consistent with the hypothesis that marsupials, the dominant living mammals of South America and Australia, were not present on any Gondwana continents until after the early Cretaceous separation of Africa by the opening of the South Atlantic.     

Ecological constraints on diversification in a model adaptive radiation

Taxonomic diversification commonly occurs through adaptive radiation, the rapid evolution of a single lineage into a range of genotypes or species each adapted to a different ecological niche. Radiation size (measured as the number of new types) varies widely between phylogenetically distinct taxa and between replicate radiations within a single taxon where the ecological opportunities available seem to be identical. Here we show how variation in energy input (productivity) and environmental disturbance combine to determine the extent of diversification in a single radiating lineage of Pseudomonas fluorescens adapting to laboratory conditions. Diversity peaked at intermediate rates of both productivity and disturbance and declined towards the extremes in a manner reminiscent of well-known ecological patterns. The mechanism responsible for the decrease in diversity arises from pleiotropic fitness costs associated with niche specialization, the effects of which are modulated by gradients of productivity and disturbance. Our results indicate that ecological gradients may constrain the size of adaptive radiations, even in the presence of the strong diversifying selection associated with ecological opportunity, by decoupling evolutionary diversification from ecological coexistence.     

Fossil that fills a critical gap in avian evolution

Despite the discoveries of well-preserved Mesozoic birds, a key part of avian evolution, close to the radiation of all living birds (Aves), remains poorly represented. Here we report on a new taxon from the Late Cretaceous locality of Ukhaa Tolgod, Mongolia, that offers insight into this critically unsampled period. Apsaravis and the controversial alvarezsaurids are the only avialan taxa known from the continental deposits at Ukhaa Tolgod, which have produced hundreds of fossil mammals, lizards and other small dinosaurs. The new taxon, Apsaravis ukhaana, is the best-preserved specimen of a Mesozoic ornithurine bird discovered in over a century. It provides data important for assessing morphological evolution across Avialae, with implications for, first, the monophyly of Enantiornithes and Sauriurae; second, the proposition that the Mesozoic sister taxa of extant birds, as part of an 'ecological bottleneck', inhabited exclusively near-shore and marine environments; and third, the evolution of flight after its origin.     

Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont

The transference of post-dentary jaw elements to the cranium of mammals as auditory ossicles is one of the central topics in evolutionary biology of vertebrates. Homologies of these bones among jawed vertebrates have long been demonstrated by developmental studies; but fossils illuminating this critical transference are sparse and often ambiguous. Here we report the first unambiguous ectotympanic (angular), malleus (articular and prearticular) and incus (quadrate) of an Early Cretaceous eutriconodont mammal from the Jehol Biota, Liaoning, China. The ectotympanic and malleus have lost their direct contact with the dentary bone but still connect the ossified Meckel's cartilage (OMC); we hypothesize that the OMC serves as a stabilizing mechanism bridging the dentary and the detached ossicles during mammalian evolution. This transitional mammalian middle ear narrows the morphological gap between the mandibular middle ear in basal mammaliaforms and the definitive mammalian middle ear (DMME) of extant mammals; it reveals complex changes contributing to the detachment of ear ossicles during mammalian evolution.     

Absolute measures of the completeness of the fossil record

Measuring the completeness of the fossil record is essential to understanding evolution over long timescales, particularly when comparing evolutionary patterns among biological groups with different preservational properties. Completeness measures have been presented for various groups based on gaps in the stratigraphic ranges of fossil taxa and on hypothetical lineages implied by estimated evolutionary trees. Here we present and compare quantitative, widely applicable absolute measures of completeness at two taxonomic levels for a broader sample of higher taxa of marine animals than has previously been available. We provide an estimate of the probability of genus preservation per stratigraphic interval, and determine the proportion of living families with some fossil record. The two completeness measures use very different data and calculations. The probability of genus preservation depends almost entirely on the Palaeozoic and Mesozoic records, whereas the proportion of living families with a fossil record is influenced largely by Cenozoic data. These measurements are nonetheless highly correlated, with outliers quite explicable, and we find that completeness is rather high for many animal groups.     

A new family of primitive mammal from the Mesozoic of western Liaoning, China

A fairly well-preserved specimen of a new primitive mammal, Repenomamus robustus gen. et sp. nov., has been described from the Yixian Formation (Lower Cretaceous), western Liaoning, China. This animal has several derived characteristics, such as well-developed den-tary/squamosal articulation, reduced number of tooth, differentiation of premolars and molars in postcanine teeth, presence of a dorsal process of the premaxilla that is not in contact with the nasal, closed medial wall of the orbit, and presence of fingerlike promontorium on the petrosal. It also retains some primitive reptile-like features. It is the most primitive taxon among the three mammals known from the Jehol Biota, and also represents the largest mammal of Mesozoic age over the world.