Basicranial evidence suggests picrodontid mammals are not stem primates.

The Picrodontidae from the middle Palaeocene of North America are enigmatic placental mammals that were allied with various mammalian groups but are generally now considered to have close affinities to paromomyid and palaechthonid plesiadapiforms based on proposed dental synapomorphies. The picrodontid fossil record consists entirely of dental and gnathic remains except for one partial cranium of Zanycteris paleocenus (AMNH 17180). Here, we use µCT technology to unveil previously undocumented morphology in AMNH 17180, describe and compare the basicranial morphology of a picrodontid for the first time, and incorporate these new data into cladistic analyses. The basicranial morphology of Z. paleocenus is distinct from plesiadapiforms and shares similarities with the Palaeogene Apatemyidae and Nyctitheriidae. Results of cladistic analyses incorporating these novel data suggest picrodontids are not stem primates nor euarchontan mammals and that the proposed dental synapomorphies uniting picrodontids with plesiadapiforms and, by extension, primates evolved independently. Results highlight the need to scrutinize proposed synapomorphies of highly autapomorphic taxa with limited fossil records.

The virtual brain endocast of Trogosus (Mammalia, Tillodontia) and its relevance in understanding the extinction of archaic placental mammals.

After successfully diversifying during the Paleocene, the descendants of the first wave of mammals that survived the end-Cretaceous mass extinction waned throughout the Eocene. Competition with modern crown clades and intense climate fluctuations may have been part of the factors leading to the extinction of these archaic groups. Why these taxa went extinct has rarely been studied from the perspective of the nervous system. Here, we describe the first virtual endocasts for the archaic order Tillodontia. Three species from the middle Eocene of North America were analyzed: Trogosus hillsii, Trogosus grangeri, and Trogosus castoridens. We made morphological comparisons with the plaster endocast of another tillodont, Tillodon fodiens, as well as groups potentially related to Tillodontia: Pantodonta, Arctocyonidae, and Cimolesta. Trogosus shows very little inter-specific variation with the only potential difference being related to the fusion of the optic canal and sphenorbital fissure. Many ancestral features are displayed by Trogosus, including an exposed midbrain, small neocortex, orbitotemporal canal ventral to rhinal fissure, and a broad circular fissure. Potential characteristics that could unite Tillodontia with Pantodonta, and Arctocyonidae are the posterior position of cranial nerve V3 exit in relation to the cerebrum and the low degree of development of the subarcuate fossa. The presence of large olfactory bulbs and a relatively small neocortex are consistent with a terrestrial lifestyle. A relatively small neocortex may have put Trogosus at risk when competing with artiodactyls for potentially similar resources and avoiding predation from archaic carnivorans, both of which are known to have had larger relative brain and neocortex sizes in the Eocene. These factors may have possibly exacerbated the extinction of Tillodontia, which showed highly specialized morphologies despite the increase in climate fluctuations throughout the Eocene, before disappearing during the middle Eocene.

The ear region of the Philippine flying lemur Cynocephalus volans (Placentalia, Dermoptera).

The placental order Dermoptera, which includes two extant species, the Philippine and Sunda flying lemurs, Cynocephalus volans and Galeopterus variegatus, respectively, is generally held to be the sister group of Primates. Yet, little has been reported on their cranial anatomy. Here, the anatomy of the ear region is described and illustrated for a juvenile and adult C. volans based on CT scans. The inclusion of a juvenile is essential as nearly all cranial sutures are fused in the adult. Soft tissues are reconstructed based on sectioned histological pre- and postnatal specimens previously reported by the author. Numerous unusual features are identified, including: a small parasphenoid beneath the basisphenoid, a tensor tympani fossa on the epitympanic wing of the squamosal, a cavum supracochleare for the geniculate ganglion of the facial nerve that is not enclosed in the petrosal bone, a secondary facial foramen between the petrosal and squamosal, a secondary posttemporal foramen leading to the primary one, a subarcuate fossa that is floored in part by a large contribution from the squamosal, a body of the incus larger than the head of the malleus, and a crus longum of the incus that lacks an osseous connection to the lenticular process. Documentation of the anatomy of the Philippine flying lemur ear region is an essential first step in morphological phylogenetic analyses where features of the basicranium are widely sampled.

The origin of placental mammal life histories.

After the end-Cretaceous extinction, placental mammals quickly diversified1, occupied key ecological niches2,3 and increased in size4,5, but this last was not true of other therians6. The uniquely extended gestation of placental young7 may have factored into their success and size increase8, but reproduction style in early placentals remains unknown. Here we present the earliest record of a placental life history using palaeohistology and geochemistry, in a 62 million-year-old pantodont, the clade including the first mammals to achieve truly large body sizes. We extend the application of dental trace element mapping9,10 by 60 million years, identifying chemical markers of birth and weaning, and calibrate these to a daily record of growth in the dentition. A long gestation (approximately 7 months), rapid dental development and short suckling interval (approximately 30-75 days) show that Pantolambda bathmodon was highly precocial, unlike non-placental mammals and known Mesozoic precursors. These results demonstrate that P. bathmodon reproduced like a placental and lived at a fast pace for its body size. Assuming that P. bathmodon reflects close placental relatives, our findings suggest that the ability to produce well-developed, precocial young was established early in placental evolution, and that larger neonate sizes were a possible mechanism for rapid size increase in early placentals.

Brawn before brains in placental mammals after the end-Cretaceous extinction.

Mammals are the most encephalized vertebrates, with the largest brains relative to body size. Placental mammals have particularly enlarged brains, with expanded neocortices for sensory integration, the origins of which are unclear. We used computed tomography scans of newly discovered Paleocene fossils to show that contrary to the convention that mammal brains have steadily enlarged over time, early placentals initially decreased their relative brain sizes because body mass increased at a faster rate. Later in the Eocene, multiple crown lineages independently acquired highly encephalized brains through marked growth in sensory regions. We argue that the placental radiation initially emphasized increases in body size as extinction survivors filled vacant niches. Brains eventually became larger as ecosystems saturated and competition intensified.

A monotreme-like auditory apparatus in a Middle Jurassic haramiyidan.

Among extant vertebrates, mammals are distinguished by having a chain of three auditory ossicles (the malleus, incus and stapes) that transduce sound waves and promote an increased range of audible-especially high-frequencies1. By contrast, the homologous bones in early fossil mammals and relatives also functioned in chewing through their bony attachments to the lower jaw2. Recent discoveries of well-preserved Mesozoic mammals have provided glimpses into the transition from the dual (masticatory and auditory) to the single auditory function for the ossicles, which is now widely accepted to have occurred at least three times in mammal evolution3-6. Here we report a skull and postcranium that we refer to the haramiyidan Vilevolodon diplomylos (dating to the Middle Jurassic epoch (160 million years ago)) and that shows excellent preservation of the malleus, incus and ectotympanic (which supports the tympanic membrane). After comparing this fossil with other Mesozoic and extant mammals, we propose that the overlapping incudomallear articulation found in this and other Mesozoic fossils, in extant monotremes and in early ontogeny in extant marsupials and placentals is a morphology that evolved in several groups of mammals in the transition from the dual to the single function for the ossicles.

Skeleton of a Cretaceous mammal from Madagascar reflects long-term insularity.

The fossil record of mammaliaforms (mammals and their closest relatives) of the Mesozoic era from the southern supercontinent Gondwana is far less extensive than that from its northern counterpart, Laurasia1,2. Among Mesozoic mammaliaforms, Gondwanatheria is one of the most poorly known clades, previously represented by only a single cranium and isolated jaws and teeth1-5. As a result, the anatomy, palaeobiology and phylogenetic relationships of gondwanatherians remain unclear. Here we report the discovery of an articulated and very well-preserved skeleton of a gondwanatherian of the latest age (72.1-66 million years ago) of the Cretaceous period from Madagascar that we assign to a new genus and species, Adalatherium hui. To our knowledge, the specimen is the most complete skeleton of a Gondwanan Mesozoic mammaliaform that has been found, and includes the only postcranial material and ascending ramus of the dentary known for any gondwanatherian. A phylogenetic analysis including the new taxon recovers Gondwanatheria as the sister group to Multituberculata. The skeleton, which represents one of the largest of the Gondwanan Mesozoic mammaliaforms, is particularly notable for exhibiting many unique features in combination with features that are convergent on those of therian mammals. This uniqueness is consistent with a lineage history for A. hui of isolation on Madagascar for more than 20 million years.

Good Vibrations: The Evolution of Whisking in Small Mammals.

While most mammals have whiskers, some tactile specialists-mainly small, nocturnal, and arboreal species-can actively move their whiskers in a symmetrical, cyclic movement called whisking. Whisking enables mammals to rapidly, tactually scan their environment to efficiently guide locomotion and foraging in complex habitats. The muscle architecture that enables whisking is preserved from marsupials to primates, prompting researchers to suggest that a common ancestor might have had moveable whiskers. Studying the evolution of whisker touch sensing is difficult, and we suggest that measuring an aspect of skull morphology that correlates with whisking would enable comparisons between extinct and extant mammals. We find that whisking mammals have larger infraorbital foramen (IOF) areas, which indicates larger infraorbital nerves and an increase in sensory acuity. While this relationship is quite variable and IOF area cannot be used to solely predict the presence of whisking, whisking mammals all have large IOF areas. Generally, this pattern holds true regardless of an animal's substrate preferences or activity patterns. Data from fossil mammals and ancestral character state reconstruction and tracing techniques for extant mammals suggest that whisking is not the ancestral state for therian mammals. Instead, whisking appears to have evolved independently as many as seven times across the clades Marsupialia, Afrosoricida, Eulipotyphla, and Rodentia, with Xenarthra the only placental superordinal clade lacking whisking species. However, the term whisking only captures symmetrical and rhythmic movements of the whiskers, rather than all possible whisker movements, and early mammals may still have had moveable whiskers. Anat Rec, 2018. © 2018 American Association for Anatomy.

Virtual endocranial and inner ear endocasts of the Paleocene 'condylarth' Chriacus: new insight into the neurosensory system and evolution of early placental mammals.

The end-Cretaceous mass extinction allowed placental mammals to diversify ecologically and taxonomically as they filled ecological niches once occupied by non-avian dinosaurs and more basal mammals. Little is known, however, about how the neurosensory systems of mammals changed after the extinction, and what role these systems played in mammalian diversification. We here use high-resolution computed tomography (CT) scanning to describe the endocranial and inner ear endocasts of two species, Chriacus pelvidens and Chriacus baldwini, which belong to a cluster of 'archaic' placental mammals called 'arctocyonid condylarths' that thrived during the ca. 10 million years after the extinction (the Paleocene Epoch), but whose relationships to extant placentals are poorly understood. The endocasts provide new insight into the paleobiology of the long-mysterious 'arctocyonids', and suggest that Chriacus was an animal with an encephalization quotient (EQ) range of 0.12-0.41, which probably relied more on its sense of smell than vision, because the olfactory bulbs are proportionally large but the neocortex and petrosal lobules are less developed. Agility scores, estimated from the dimensions of the semicircular canals of the inner ear, indicate that Chriacus was slow to moderately agile, and its hearing capabilities, estimated from cochlear dimensions, suggest similarities with the extant aardvark. Chriacus shares many brain features with other Paleocene mammals, such as a small lissencephalic brain, large olfactory bulbs and small petrosal lobules, which are likely plesiomorphic for Placentalia. The inner ear of Chriacus also shares derived characteristics of the elliptical and spherical recesses with extinct species that belong to Euungulata, the extant placental group that includes artiodactyls and perissodactyls. This lends key evidence to the hypothesized close relationship between Chriacus and the extant ungulate groups, and demonstrates that neurosensory features can provide important insight into both the paleobiology and relationships of early placental mammals.

An Early Cretaceous eutherian and the placental-marsupial dichotomy.

Molecular estimates of the divergence of placental and marsupial mammals and their broader clades (Eutheria and Metatheria, respectively) fall primarily in the Jurassic period. Supporting these estimates, Juramaia-the oldest purported eutherian-is from the early Late Jurassic (160 million years ago) of northeastern China. Sinodelphys-the oldest purported metatherian-is from the same geographic area but is 35 million years younger, from the Jehol biota. Here we report a new Jehol eutherian, Ambolestes zhoui, with a nearly complete skeleton that preserves anatomical details that are unknown from contemporaneous mammals, including the ectotympanic and hyoid apparatus. This new fossil demonstrates that Sinodelphys is a eutherian, and that postcranial differences between Sinodelphys and the Jehol eutherian Eomaia-previously thought to indicate separate invasions of a scansorial niche by eutherians and metatherians-are instead variations among the early members of the placental lineage. The oldest known metatherians are now not from eastern Asia but are 110 million years old from western North America, which produces a 50-million-year ghost lineage for Metatheria.

First cranial remains of a gondwanatherian mammal reveal remarkable mosaicism.

Previously known only from isolated teeth and lower jaw fragments recovered from the Cretaceous and Palaeogene of the Southern Hemisphere, the Gondwanatheria constitute the most poorly known of all major mammaliaform radiations. Here we report the discovery of the first skull material of a gondwanatherian, a complete and well-preserved cranium from Upper Cretaceous strata in Madagascar that we assign to a new genus and species. Phylogenetic analysis strongly supports its placement within Gondwanatheria, which are recognized as monophyletic and closely related to multituberculates, an evolutionarily successful clade of Mesozoic mammals known almost exclusively from the Northern Hemisphere. The new taxon is the largest known mammaliaform from the Mesozoic of Gondwana. Its craniofacial anatomy reveals that it was herbivorous, large-eyed and agile, with well-developed high-frequency hearing and a keen sense of smell. The cranium exhibits a mosaic of primitive and derived features, the disparity of which is extreme and probably reflective of a long evolutionary history in geographic isolation.

Response to comment on "The placental mammal ancestor and the post-K-Pg radiation of placentals".

Tree-building with diverse data maximizes explanatory power. Application of molecular clock models to ancient speciation events risks a bias against detection of fast radiations subsequent to the Cretaceous-Paleogene (K-Pg) event. Contrary to Springer et al., post-K-Pg placental diversification does not require "virus-like" substitution rates. Even constraining clade ages to their model, the explosive model best explains placental evolution.

The placental mammal ancestor and the post-K-Pg radiation of placentals.

To discover interordinal relationships of living and fossil placental mammals and the time of origin of placentals relative to the Cretaceous-Paleogene (K-Pg) boundary, we scored 4541 phenomic characters de novo for 86 fossil and living species. Combining these data with molecular sequences, we obtained a phylogenetic tree that, when calibrated with fossils, shows that crown clade Placentalia and placental orders originated after the K-Pg boundary. Many nodes discovered using molecular data are upheld, but phenomic signals overturn molecular signals to show Sundatheria (Dermoptera + Scandentia) as the sister taxon of Primates, a close link between Proboscidea (elephants) and Sirenia (sea cows), and the monophyly of echolocating Chiroptera (bats). Our tree suggests that Placentalia first split into Xenarthra and Epitheria; extinct New World species are the oldest members of Afrotheria.

A reexamination of the Carnivora malleus (Mammalia, Placentalia).

Authoritative anatomical references depict domestic dogs and cats as having a malleus with a short rostral (anterior) process that is connected via a ligament to the ectotympanic of the auditory bulla. Similar mallei have been reported for representatives of each of the 15 extant families of Carnivora, the placental order containing dogs and cats. This morphology is in contrast to a malleus with a long rostral process anchored to the ectotympanic that is considered to be primitive for mammals. Our reexamination of extant carnivorans found representatives from 12 families that possess an elongate rostral process anchored to the ectotympanic. Consequently, the malleus also is a component of the bulla. In a subset of our carnivoran sample, we confirmed that the elongate rostral process on the ectotympanic is continuous with the rest of the malleus through a thin osseous lamina. This morphology is reconstructed as primitive for Carnivora. Prior inaccurate descriptions of the taxa in our sample having mallei continuous with the bulla were based on damaged mallei. In addition to coupling to the ectotympanic, the rostral process of the malleus was found to have a hook-like process that fits in a facet on the skull base in representatives from seven families (felids, nandiniids, viverrids, canids, ursids, procyonids, and mustelids); its occurrence in the remaining families could not be ascertained. This feature is named herein the mallear hook and is likewise reconstructed to be primitive for Carnivora. We also investigated mallei in one additional placental order reported to have mallei not connected to the ectotympanic, Pholidota (pangolins), the extant sister group of Carnivora. We found pholidotans to also have anchored mallei with long rostral processes, but lacking mallear hooks. In light of our results, other mammals previously reported to have short rostral processes should be reexamined.

The Miocene mammal Necrolestes demonstrates the survival of a Mesozoic nontherian lineage into the late Cenozoic of South America.

The early Miocene mammal Necrolestes patagonensis from Patagonia, Argentina, was described in 1891 as the only known extinct placental "insectivore" from South America (SA). Since then, and despite the discovery of additional well-preserved material, the systematic status of Necrolestes has remained in flux, with earlier studies leaning toward placental affinities and more recent ones endorsing either therian or specifically metatherian relationships. We have further prepared the best-preserved specimens of Necrolestes and compared them with newly discovered nontribosphenic Mesozoic mammals from Argentina; based on this, we conclude that Necrolestes is related neither to marsupials nor placentals but is a late-surviving member of the recently recognized nontherian clade Meridiolestida, which is currently known only from SA. This conclusion is supported by a morphological phylogenetic analysis that includes a broad sampling of therian and nontherian taxa and that places Necrolestes within Meridiolestida. Thus, Necrolestes is a remnant of the highly endemic Mesozoic fauna of nontribosphenic mammals in SA and extends the known record of meridiolestidans by almost 45 million years. Together with other likely relictual mammals from earlier in the Cenozoic of SA and Antarctica, Necrolestes demonstrates the ecological diversity of mammals and the mosaic pattern of fauna replacement in SA during the Cenozoic. In contrast to northern continents, the Cenozoic faunal history of SA was characterized by a long period of interaction between endemic mammalian lineages of Mesozoic origin and metatherian and eutherian lineages that probably dispersed to SA during the latest Cretaceous or earliest Paleocene.

Petrosal anatomy and inner ear structures of the Late Jurassic Henkelotherium (Mammalia, Cladotheria, Dryolestoidea): insight into the early evolution of the ear region in cladotherian mammals.

The petrosal anatomy and inner ear structure of Jurassic cladotherian mammals represent the ancestral morphological conditions (groundplan) from which modern therian mammals (marsupials and placentals) have evolved. We present the reconstruction of the petrosal and inner ear features of the Late Jurassic dryolestoid mammal Henkelotherium guimarotae from high-resolution computed tomography and three-dimensional imaging analysis. This study of Henkelotherium revealed a combination of derived and primitive features, including: cladotherian apomorphies, such as the promontorial sulcus for the internal carotid artery and reduced lateral trough; trechnotherian characters, such as an enclosed cochlear canaliculus for the perilymphatic duct, post-promontorial tympanic sinus and caudal tympanic process; in addition to plesiomorphic mammalian features, such as the cavum supracochleare and prootic canal. The inner ear of Henkelotherium shows a division between the utricle and saccule, a cochlear canal coiled through at least 270 degrees, a distinctive primary bony lamina for the basilar membrane, and a secondary bony lamina. The development of the primary and secondary bony laminae in the cochlear canal is suggested here to be correlated with the concurrent coiling of the bony canal and membranous duct of the inner ear cochlea, apomorphies of the more inclusive cladotherian clade that also represent the ancestral morphotype of modern therian mammals. Because these features are crucial for high-frequency hearing in extant therian mammals, their early appearance in Late Jurassic cladotherians suggests a more ancient origination for high-frequency hearing in mammalian history than previously thought.

A Late Jurassic digging mammal and early mammalian diversification.

A fossil mammal from the Late Jurassic Morrison Formation, Colorado, has highly specialized teeth similar to those of xenarthran and tubulidentate placental mammals and different from the generalized insectivorous or omnivorous dentitions of other Jurassic mammals. It has many forelimb features specialized for digging, and its lumbar vertebrae show xenarthrous articulations. Parsimony analysis suggests that this fossil represents a separate basal mammalian lineage with some dental and vertebral convergences to those of modern xenarthran placentals, and reveals a previously unknown ecomorph of early mammals.

Stem Lagomorpha and the antiquity of Glires.

We describe several fossils referable to Gomphos elkema from deposits close to the Paleocene-Eocene boundary at Tsagan Khushu, Mongolia. Gomphos shares a suite of cranioskeletal characters with extant rabbits, hares, and pikas but retains a primitive dentition and jaw compared to its modern relatives. Phylogenetic analysis supports the position of Gomphos as a stem lagomorph and excludes Cretaceous taxa from the crown radiation of placental mammals. Our results support the hypothesis that rodents and lagomorphs radiated during the Cenozoic and diverged from other placental mammals close to the Cretaceous-Tertiary boundary.

An Early Cretaceous tribosphenic mammal and metatherian evolution.

Derived features of a new boreosphenidan mammal from the Lower Cretaceous Yixian Formation of China suggest that it has a closer relationship to metatherians (including extant marsupials) than to eutherians (including extant placentals). This fossil dates to 125 million years ago and extends the record of marsupial relatives with skeletal remains by 50 million years. It also has many foot structures known only from climbing and tree-living extant mammals, suggesting that early crown therians exploited diverse niches. New data from this fossil support the view that Asia was likely the center for the diversification of the earliest metatherians and eutherians during the Early Cretaceous.