Julien Benoit

Cranial Remain from Tunisia Provides New Clues for the Origin and Evolution of Sirenia (Mammalia, Afrotheria) in Africa

Sea cows (manatees, dugongs) are the only living marine mammals to feed solely on aquatic plants. Unlike whales or dolphins (Cetacea), the earliest evolutionary history of sirenians is poorly documented, and limited to a few fossils including skulls and skeletons of two genera composing the stem family of Prorastomidae (Prorastomus and Pezosiren). Surprisingly, these fossils come from the Eocene of Jamaica, while stem Hyracoidea and Proboscidea - the putative sister-groups to Sirenia - are recorded in Africa as early as the Late Paleocene. So far, the historical biogeography of early Sirenia has remained obscure given this paradox between phylogeny and fossil record. Here we use X-ray microtomography to investigate a newly discovered sirenian petrosal from the Eocene of Tunisia. This fossil represents the oldest occurrence of sirenians in Africa. The morphology of this petrosal is more primitive than the Jamaican prorastomids’ one, which emphasizes the basal position of this new African taxon within the Sirenia clade. This discovery testifies to the great antiquity of Sirenia in Africa, and therefore supports their African origin. While isotopic analyses previously suggested sirenians had adapted directly to the marine environment, new paleoenvironmental evidence suggests that basal-most sea cows were likely restricted to fresh waters.

The petrosal of the earliest elephant-shrew Chambius (Macroscelidea: Afrotheria) from the Eocene of Djebel Chambi (Tunisia) and the evolution of middle and inner ear of elephant-shrews

Macroscelidea (elephant-shrews or sengis) are small insectivorous mammals restricted to Africa; they belong to the super-cohort Afrotheria along with other insectivorans (aardvarks, tenrecs and golden moles) and ungulates (elephants, sea cows and hyraxes). Though their fossil record extends back to the Eocene, cranial remains of Palaeogene elephant-shrews, including the middle and inner ear structure, remain unknown. Two macroscelid isolated petrosal bones are described from the late Early–early Middle Eocene Djebel Chambi locality in Tunisia. Chambius kasserinensis is the only macroscelid represented in this locality. A cladistic analysis based on petrosal and inner ear characters highlights the crucial interest of the petrosal and inner ear morphology for understanding the evolution of Macroscelididae. It confirms the attribution of these isolated petrosals to C. kasserinensis. This hypothesis is supported by a common pattern of circulatory system, the morphology of the rostral and caudal tympanic processes, and the shape of the cochlea. In addition, Chambius appears to be the basal-most taxon among the macroscelid sample; this position is supported by the lack of some specializations of the middle ear such as inflated ossicular bones and pneumatized bulla. The presence of a secondary common crus in Chambius suggests a convergent loss of this structure, at least in Macroscelidea and Tenrecoidea. The petrosal and inner ear characters support the clade Afroinsectivora, which gathers macroscelids with other endemic African insectivorans (tenrecs and golden moles), reinforcing the hypothesis of an African origin of macroscelids. The petrosal bone and inner ear characters provide further morphological support for the debated clade (Petrodromus, Elephantulus rozeti, Macroscelides). New data underlines the fact that the cranial arterial pattern of the Eocene macroscelid Chambius was already similar to that of modern macroscelid species. It also suggests that early elephant-shrews were probably not as capable of hearing low frequencies as their extant representatives.

New insights into the ear region anatomy and cranial blood supply of advanced stem Strepsirhini: Evidence from three primate petrosals from the Eocene of Chambi, Tunisia

We report the discovery of three isolated primate petrosal fragments from the fossiliferous locality of Chambi (Tunisia), a primate-bearing locality dating from the late early to the early middle Eocene. These fossils display a suite of anatomical characteristics otherwise found only in strepsirhines, and as such might be attributed either to Djebelemur or/and cf. Algeripithecus, the two diminutive stem strepsirhine primates recorded from this locality. Although damaged, the petrosals provide substantial information regarding the ear anatomy of these advanced stem strepsirhines (or pre-tooth-combed primates), notably the patterns of the pathway of the arterial blood supply. Using μCT-scanning techniques and digital segmentation of the structures, we show that the transpromontorial and stapedial branches of the internal carotid artery (ICA) were present (presence of bony tubes), but seemingly too small to supply enough blood to the cranium alone. This suggests that the ICA was not the main cranial blood supply in stem strepsirhines, but that the pharyngeal or vertebral artery primitively ensured a great part of this role instead, an arterial pattern that is reminiscent of modern cheirogaleid, lepilemurid lemuriforms and lorisiforms. This could explain parallel loss of the ICA functionality among these families. Specific measurements made on the cochlea indicate that the small strepsirhine primate(s) from Chambi was (were) highly sensitive to high frequencies and poorly sensitive to low frequencies. Finally, variance from orthogonality of the plane of the semicircular canals (SCs) calculated on one petrosal (CBI-1-569) suggests that Djebelemur or cf. Algeripithecus likely moved (at least its head) in a way similar to that of modern mouse lemurs.

Petrosal and Bony Labyrinth Morphology Supports Paraphyly of Elephantulus Within Macroscelididae (Mammalia, Afrotheria)

Interest in the phylogeny of Macroscelididae (sengis or elephant shrews) has been prompted by molecular studies indicating that Elephantulus rozeti is best placed as the sister group of Petrodromus tetradactylus (this clade being in turn the sister taxon to Macroscelides proboscideus) than among other species of the genus Elephantulus. Until now, no discrete morphological characters have been proposed to support the grouping of E. rozeti, Petrodromus, and Macroscelides into this single so-called ‘Panelephantulus’ clade. Here, we employed μCT scanning in order to investigate the petrosal and bony labyrinth (bony capsule of the inner ear) morphology of most species of extant Macroscelididae. We performed a cladistic analysis on ear traits and found that despite some convergences (e.g., concerning the bony arterial canals in Macroscelides and Rhynchocyon) the middle and inner ear morphology furnishes significant support for the ‘Panelephantulus’ clade. In our analysis, this clade is unambigously supported by the presence of a fully ossified stapediofacial tube. Two additional characters (the presence of a bony septum at the mouth of the fenestra cochleae dividing the D3 sinus into two distinct cavities and the absence of an accessory lateral pneumatic fossa) could also support ‘Panelephantulus.’ These newly discovered morphological characters support the molecular phylogenies published and highlight the importance of coding hitherto difficult to sample morphologies within cladistic analyses using micro-CT techniques. Taxonomic implications are briefly discussed.

Comparative Anatomy and Three-Dimensional Geometric-Morphometric Study of the Bony Labyrinth of Bibymalagasia (Mammalia, Afrotheria)

ABSTRACT Plesiorycteropus (Malagasy aardvarks) is the sole genus belonging to an extinct mammalian order, the Bibymalagasia, that lived in Madagascar in the Quaternary. Its systematic and phylogenetic position is controversial because Plesiorycteropus morphologically resembles aardvarks (Tubulidentata), whereas a recent molecular analysis proposed that it belongs to Tenrecoidea, along with Tenrecidae (tenrecs and otter shrews) and Chrysochloridae (golden moles). This context of competing phylogenetic hypotheses is stimulating for the investigation of new characters for phylogenetic inferences. Here we used the noninvasive methods of micro-computed tomography scanning, digital reconstruction, and three-dimensional geometric-morphometric analysis of shape to investigate the morphology of the bony labyrinth (osseous inner ear) of the holotype skulls of both known species of Bibymalagasia: Plesiorycteropus madagascariensis and P. germainepetterae. Firstly, by comparisons with their extant relatives, we find that the characters of the bony labyrinth that distinguish P. madagascariensis and P. germainepetterae could only represent intraspecific variation. Secondly, we find that the bony labyrinth of Bibymalagasia is distinctive from those of other Afrotherians examined, supporting their ordinal distinctiveness. Indeed, the principal component analysis on labyrinthine shape data shows that the bony labyrinths of both Plesiorycteropus species are in fact intermediate between those of tubulidentates and other Afrotherian insectivores. Finally, we investigated the evolution of the secondary common crus (partial fusion of the lateral and posterior semicircular canals) in Afrotherians and found that this character is present in tubulidentates and potamogaline tenrecs, supporting the hypothesis that its presence is primitive for Afrotherians. In contrast, Plesiorycteropus displays the derived condition (i.e., loss of the secondary common crus).

A new method of estimating brain mass through cranial capacity in extinct proboscideans to account for the non-neural tissues surrounding their brain

ABSTRACT Endocranial casts are the only available material to study the evolution of brain morphology through geologic time. However, these are not just casts of brain tissues but also include, e.g., meningeal tissues, blood vessels, and nerves. Tissues surrounding the brain are particularly thick in proboscideans, making the estimation of brain size in extinct proboscideans very tentative. Here the regression of brain mass over cranial capacity—based on data on intraindividual comparison between those two metrics in the literature—is used to estimate the ‘true’ brain mass of extinct mammals. This regression reveals that cranial capacity is allometrically related to brain mass in mammals. The larger the brain, the greater is the difference between brain mass and cranial capacity. Applied to proboscideans, this new method suggests that the thickness of non-neural tissues surrounding the brain has been greatly overestimated in extinct proboscidean species, resulting in the underestimation of brain mass. This data set suggests that a comparatively small brain is likely primitive for Proboscidea and that the representatives of the clade Elephantimorpha have inherited their large brain from their last common ancestor. The largest brain proportional to mass of all Proboscidea belongs to the Quaternary dwarf elephant of Sicily, which would have been comparable to modern humans in encephalization quotient.

New material of Seggeurius amourensis (Paenungulata, Hyracoidea), including a partial skull with intact basicranium

ABSTRACT Seggeurius is the basal-most hyracoid known to date, and one of the earliest known fossil afrotherians. This taxon has a dramatic importance in mammalian phylogeny, but until now it was known from dental remains only. Here we describe previously unpublished material of Seggeurius, including some mandibular and maxillary fragments, and a braincase. This study is the first to thoroughly describe and discuss the morphology of the ear region and osseous inner ear of a Paleogene hyracoid. It allows a reappraisal of some important characters that are often used in cladistic analyses of Paenungulata. In particular, it seems that in stem hyracoids the orbit is located caudally, the eustachian sac is absent or reduced, the course of the internal carotid artery is intrabullar and medial, and a deep epitympanic sinus, a basisphenoid contribution to the bulla, and the stapedial artery are present. The cochlear canal is rather flattened, and the secondary common crus was rapidly lost. A cladistic analysis of stem placental mammals highlights three derived traits shared by Seggeurius and stem sirenians (the tuber-shaped postglenoid process, the squared and massive mastoid apophysis of the petrosal, and the presence of a swelling on the septum metacochleare) and supports molecular analysis that hypothesizes a Hyracoidea-Sirenia sister-group relationship. This study demonstrates how useful the petrosal and labyrinthine characters of fossils can be for mammalian phylogenetic inference.

Endocranial Casts of Pre-Mammalian Therapsids Reveal an Unexpected Neurological Diversity at the Deep Evolutionary Root of Mammals

The origin and evolution of the mammalian brain has long been the focus of scientific enquiry. Conversely, little research has focused on the palaeoneurology of the stem group of Mammaliaformes, the Permian and Triassic non-mammaliaform Therapsida (NMT). This is because the majority of the NMT have a non-ossified braincase, making the study of their endocranial cast (sometimes called the “fossil brain”) problematic. Thus, descriptions of the morphology and size of NMT endocranial casts have been based largely on approximations rather than reliable determination. Accordingly, here we use micro-CT scans of the skulls of 1 Dinocephalia and 3 Biarmosuchia, which are NMT with a fully ossified braincase and thus a complete endocast. For the first time, our work enables the accurate determination of endocranial shape and size in NMT. This study suggests that NMT brain size falls in the upper range of the reptilian and amphibian variation. Brain size in the dicynodont Kawingasaurus is equivalent to that of early Mammaliaformes, whereas the Dinocephalia show evidence of a secondary reduction of brain size. In addition, unlike other NMT in which the endocast has a tubular shape and its parts are arranged in a linear manner, the biarmosuchian endocast is strongly flexed at the level of the midbrain, creating a near right angle between the fore- and hindbrain. These data highlight an unexpected diversity of endocranial size and morphology in NMT, features that are usually considered conservative in this group.