Guillaume Billet

Middle Eocene rodents from Peruvian Amazonia reveal the pattern and timing of caviomorph origins and biogeography

The long-term isolation of South America during most of the Cenozoic produced a highly peculiar terrestrial vertebrate biota, with a wide array of mammal groups, among which caviomorph rodents and platyrrhine primates are Mid-Cenozoic immigrants. In the absence of indisputable pre-Oligocene South American rodents or primates, the mode, timing and biogeography of these extraordinary dispersals remained debated. Here, we describe South Americas oldest known rodents, based on a new diverse caviomorph assemblage from the late Middle Eocene (approx. 41 Ma) of Peru, including five small rodents with three stem caviomorphs. Instead of being tied to the Eocene/Oligocene global cooling and drying episode (approx. 34 Ma), as previously considered, the arrival of caviomorphs and their initial radiation in South America probably occurred under much warmer and wetter conditions, around the Mid-Eocene Climatic Optimum. Our phylogenetic results reaffirm the African origin of South American rodents and support a trans-Atlantic dispersal of these mammals during Middle Eocene times. This discovery further extends the gap (approx. 15 Myr) between first appearances of rodents and primates in South America.

High morphological variation of vestibular system accompanies slow and infrequent locomotion in three-toed sloths.

The semicircular canals (SCs), part of the vestibular apparatus of the inner ear, are directly involved in the detection of angular motion of the head for maintaining balance, and exhibit adaptive patterns for locomotor behaviour. Consequently, they are generally believed to show low levels of intraspecific morphological variation, but few studies have investigated this assumption. On the basis of high-resolution computed tomography, we present here, to our knowledge, the first comprehensive study of the pattern of variation of the inner ear with a focus on Xenarthra. Our study demonstrates that extant three-toed sloths show a high level of morphological variation of the bony labyrinth of the inner ear. Especially, the variation in shape, relative size and angles of their SCs greatly differ from those of other, faster-moving taxa within Xenarthra and Placentalia in general. The unique pattern of variation in three-toed sloths suggests that a release of selection and/or constraints on their organ of balance is associated with the observed wide range of phenotypes. This release is coincident with their slow and infrequent locomotion and may be related, among other possible factors, to a reduced functional demand for a precise sensitivity to movement.

Phylogeny of the Notoungulata (Mammalia) based on cranial and dental characters

The Notoungulata is the richest order of South American endemic placentals, but phylogenetic relationships within this order are unclear. This work provides short descriptions of new cranial characters useful for phylogenetic research on notoungulates, argues for a redefinition of some characters on the dental cristae, and provides a long overdue treatment of notoungulate relationships – the most complete thus far – via a cladistic phylogenetic analysis comprising 50 notoungulate genera and 133 morphological characters of the skull and teeth. The monophyly of the Notoungulata (including Pyrotherium) is well supported by numerous cranial and dental apomorphies. The validity of most traditional notoungulates suprageneric taxa is tested, and the monophyly of the two traditional notoungulate suborders Toxodontia and Typotheria is supported. These two taxa are united in a clade supported by an original character on the morphology of the ectopterygoid crests. The Henricosborniidae, Isotemnidae and Oldfieldthomasiidae are paraphyletic, reflecting the fact that these families are mostly defined by plesiomorphic characters. The monophyly of Notohippidae is questioned, as well as the possibility of a close relationship between leontiniids and toxodontids on the basis of cranial arguments. It is observed that two major subclades diverge early within the Typotheria: the Interatheriidae and the clade Archaeohyracidae + Mesotheriidae + Hegetotheriidae. This new phylogeny of the notoungulates from cranial and dental anatomy is an essential step towards reconstructing the ancestral morphotype of the Notoungulata, and is crucial for research on the origin and phylogenetic affinities of these South American ungulates within the Placentalia.

Oldest cingulate skulls provide congruence between morphological and molecular scenarios of armadillo evolution

The cingulates of the mammalian order Xenarthra present a typical case of disagreement between molecular and morphological phylogenetic studies. We report here the discovery of two new skulls from the Late Oligocene Salla Beds of Bolivia (approx. 26 Ma), which are the oldest known well-preserved cranial remains of the group. A new taxon is described: Kuntinaru boliviensis gen. et sp. nov. A phylogenetic analysis clusters K. boliviensis together with the armadillo subfamily Tolypeutinae. These skulls document an early spotty occurrence for the Tolypeutinae at 26 Ma, in agreement with the temporal predictions of previous molecular studies. The fossil record of tolypeutines is now characterized by a unique occurrence in the Late Oligocene, and a subsequent 12 Myr lack in the fossil record. It is noteworthy that the tolypeutines remain decidedly marginal in the Late Palaeogene and Early Neogene deposits, whereas other cingulate groups diversify. Also, the anatomical phylogenetic analysis herein, which includes K. boliviensis, is congruent with recent molecular phylogenetic analyses. Kuntinaru boliviensis is the oldest confident calibration point available for the whole Cingulata.

The inner ear of Megatherium and the evolution of the vestibular system in sloths.

Extant tree sloths are uniquely slow mammals with a very specialized suspensory behavior. To improve our understanding of their peculiar evolution, we investigated the inner ear morphology of one of the largest and most popular fossil ground sloths, Megatherium americanum. We first address the predicted agility of this animal from the scaling of its semicircular canals (SC) relative to body mass, based on recent work that provided evidence that the size of the SC in mammals correlates with body mass and levels of agility. Our analyses predict intermediate levels of agility for Megatherium, contrasting with the extreme slowness of extant sloths. Secondly, we focus on the morphology of the SC at the inner ear scale and investigate the shape and proportions of these structures in Megatherium and in a large diversity of extant xenarthrans represented in our database. Our morphometric analyses demonstrate that the giant ground sloth clearly departs from the SC morphology of both extant sloth genera (Choloepus, Bradypus) and is in some aspects closer to that of armadillos and anteaters. Given the close phylogenetic relationships of Megatherium with the extant genus Choloepus, these results are evidence of substantial homoplasy of the SC anatomy in sloths. This homoplasy most likely corresponds to an outstanding convergent evolution between extant suspensory sloth genera.

No evidence for an afrotherian-like delayed dental eruption in South American notoungulates

The fossil South American ungulates are of great interest relative to the new phylogenetic framework elaborated for living placental mammals. In particular, studies on these endemic taxa can allow for testing congruence between southern placental phylogeny and plate tectonics, beyond what has already been suggested in the Atlantogenata hypothesis based on extant afrotherians and xenarthrans. The presence of delayed dental eruption relative to skull growth is one feature characterizing the extant afrotherians and possibly the xenarthrans. Late dental eruption has been mentioned previously in South American notoungulates, thus suggesting possible resemblance with afrotherians and perhaps xenarthrans. We provide here a detailed study of the dental eruption pattern relative to the skull growth in the notoungulates. In contrast to previous statements, our results demonstrate that there is currently no evidence for an afrotherian-like delayed dental eruption in this group. For now, the inferred absence of a delayed dental eruption in notoungulates does not support atlantogenatan/afrotherian affinities for the Notoungulata, but other atlantogenatan/afrotherian characteristics remain to be explored in more detail in this group and other South American ungulates.

The phylogenetic affinities of the extinct glyptodonts

Among the fossils of hitherto unknown mammals that Darwin collected in South America between 1832 and 1833 during the Beagle expedition were examples of the large, heavily armored herbivores later known as glyptodonts. Ever since, glyptodonts have fascinated evolutionary biologists because of their remarkable skeletal adaptations and seemingly isolated phylogenetic position even within their natural group, the cingulate xenarthrans (armadillos and their allies). In possessing a carapace comprised of fused osteoderms, the glyptodonts were clearly related to other cingulates, but their precise phylogenetic position as suggested by morphology remains unresolved. To provide a molecular perspective on this issue, we designed sequence-capture baits using in silico reconstructed ancestral sequences and successfully assembled the complete mitochondrial genome of Doedicurus sp., one of the largest glyptodonts. Our phylogenetic reconstructions establish that glyptodonts are in fact deeply nested within the armadillo crown-group, representing a distinct subfamily (Glyptodontinae) within family Chlamyphoridae. Molecular dating suggests that glyptodonts diverged no earlier than around 35 million years ago, in good agreement with their fossil record. Our results highlight the derived nature of the glyptodont morphotype, one aspect of which is a spectacular increase in body size until their extinction at the end of the last ice age.

Morphological diversity of the bony labyrinth (inner ear) in extant Xenarthrans and its relation to phylogeny

We present a survey of the morphological diversity of the bony labyrinth of the inner ear in Xenarthra, including the fossil ground sloth Megatherium. Using a combination of traditional and geometric morphometrics, correlation analyses, and qualitative observations, we attempt to extract independent and informative phylogenetic characters of the bony labyrinth for the superorder. Geometric morphometric analyses demonstrate a strong imprint of phylogenetic history on the shape of the bony labyrinth of xenarthrans and a weak influence of allometry. Discrete characters mapped on a consensus cladogram for xenarthrans show support for many traditional nodes within the superorder and may also provide critical information for problematic nodes within Cingulata. A relatively large lateral semicircular canal may, for instance, represent a synapomorphy for the molecular clade allying fairy armadillos (Chlamyphorinae) to the Tolypeutinae. Striking convergences were detected when comparing Megatherium, the giant ground sloth, with extant armadillos and Chlamyphorus, the pink fairy armadillo, with the extant three- and two-toed sloths. These findings have the potential to help understand the phylogenetic relationships of fossil xenarthrans.

External and Internal Anatomy of a Petrosal from the Late Paleocene of Itaboraí, Brazil, Referred to Notoungulata (Placentalia)

ABSTRACT We describe the earliest petrosal bone referred to the South American endemic Notoungulata, from the late Paleocene-early Eocene Beds of Itaboraí, which provides a critical basis for assessing their enigmatic origins. As indicated by our phylogenetic analysis, the fossil belongs to a taxon most likely close to the ancestral root of the Notoungulata. We describe the entire external anatomy of this isolated ear bone and also investigate the bony labyrinth of the inner ear through computed tomographic scan reconstruction. Within Notoungulata, the specimen retains a number of features considered plesiomorphic, such as a narrow medial flange on the tympanic surface, the presence of a petromastoid canal, and a rather deep fossa subarcuata. We also present a survey of the petrosal anatomy of early diverging notoungulates compared with other members of Eutheria. Features regarded as plesiomorphic in Notoungulata comprise a low stapedial ratio, a cavity for the trigeminal ganglion, a secondary crus commune, a ramus superior of stapedial artery (although reduced) and arteria diploëtica magna, and the tegmen tympani pierced by a canal. Derived features include notably a laterally located tensor tympani fossa, a bean-shaped promontorium and adjoining flattened medial flange, and a stapedial fossa poorly separated from the postpromontorial tympanic sinus. A number of derived notoungulate characters are interestingly shared with the extant hyrax Procavia. Further investigation of this anatomical region in other eutherians is required in order to fully exploit the phylogenetic potential of our new observations. This is especially needed for other groups of South American endemic ungulates possibly related to Notoungulata.

New Interatheres (Mammalia, Notoungulata) from the Late Oligocene Salla Beds of Bolivia

Abstract Two new Deseadan interatheriine genera (Interatheriidae, Notoungulata) from the late Oligocene Salla Beds of Bolivia are described. Both are monotypic and one is known from a partial skeleton, a rarity among known pre-Santacrucian interathere taxa. Phylogenetically, both taxa nest well within Interatheriinae, showing characteristically bilobed p3–4. Both taxa also have derived characters (hypselodont cheeckteeth, persistent lingual sulcus on upper molars) relative to basal interatheriines such as Santiagorothia and Proargyrohyrax but are clearly plesiomorphic with respect to younger, more highly derived Santacrucian interatheriine taxa such as Interatherium and Protypotherium. New species Brucemacfaddenia boliviensis is on average larger than the other new Salla interatheriine, Federicoanaya sallaensis, although they do overlap in size. Distinguishing between the two new taxa based purely on molar morphology is confounded by lack of diagnostic characters on the molar teeth and the overlap in size between the taxa. We overcome this difficulty of identifying specimens that preserve only molars by using discriminant analysis. We present a few of the simpler yet still robust discriminant functions we used so that future workers have a means of identifying problematic specimens. Analysis of Salla interathere specimens and stratigraphic provenance indicates both taxa experienced a modest increase in body size upsection, the driving mechanism for which remains unknown, but could be environmental changes or simple drift. These two new taxa help emphasize the fact that while the Salla fauna shares elements with roughly contemporaneous Deseadan faunas from more southerly latitudes, important faunal distinctions mark the two regions as well.