Lionel Hautier

Variability and constraint in the mammalian vertebral column

Patterns of vertebral variation across mammals have seldom been quantified, making it difficult to test hypotheses of covariation within the axial skeleton and mechanisms behind the high level of vertebral conservatism among mammals. We examined variation in vertebral counts within 42 species of mammals, representing monotremes, marsupials and major clades of placentals. These data show that xenarthrans and afrotherians have, on average, a high proportion of individuals with meristic deviations from species’ median series counts. Monotremes, xenarthrans, afrotherians and primates show relatively high variation in thoracolumbar vertebral count. Among the clades sampled in our dataset, rodents are the least variable, with several species not showing any deviations from median vertebral counts, or vertebral anomalies such as asymmetric ribs or transitional vertebrae. Most mammals show significant correlations between sacral position and length of the rib cage; only a few show a correlation between sacral position and number of sternebrae. The former result is consistent with the hypothesis that adult axial skeletal structures patterned by distinct mesodermal tissues are modular and covary; the latter is not. Variable levels of correlation among these structures may indicate that the boundaries of prim/abaxial mesodermal precursors of the axial skeleton are not uniform across species. We do not find evidence for a higher frequency of vertebral anomalies in our sample of embryos or neonates than in post‐natal individuals of any species, contrary to the hypothesis that stabilizing selection plays a major role in vertebral patterning.

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.

Zegdoumyidae (Rodentia, Mammalia), stem anomaluroid rodents from the Early to Middle Eocene of Algeria (Gour Lazib, Western Sahara): new dental evidence

The Palaeogene fossil record of rodents in Africa is very poor compared to that of North America or Eurasia. Despite this, Africa has long appeared to be a centre of adaptive radiation for two distinct groups of Rodentia: Hystricognathi and Anomaluroidea. The >45-million-year-old enigmatic Zegdoumyidae is the oldest and only rodent family known of this age from Africa (Algeria and Tunisia). Zegdoumyids have been tentatively regarded as a possible early African stem group for Anomaluridae, a link that has never been clearly established because of the highly fragmentary nature of zegdoumyid fossils, as well as the major temporal and morphological gaps between zegdoumyids and the first true anomaluroids from the Late Eocene. About 200 rodent teeth have been sorted after acid treatment of indurated sediments from several new localities in the Gour Lazib of western Algeria dating from the late Early or early Middle Eocene. These new fossils allow us to better describe the morphology of the Zegdoumyidae (especially Glibia and Zegdoumys) and to identify a new taxon, Lazibemys zegdouensis gen. et sp. nov. With this material, we investigated the phylogenetic position of the Zegdoumyidae in a high-level rodent phylogeny with cladistic assessment of the dental evidence. Our analyses have yielded six equally most-parsimonious trees in which zegdoumyids represent the earliest offshoots (pectinately arranged) of a large clade that embraces Eocene anomaluroids plus stem and crown Anomaluridae. This phylogenetic assumption underscores the great antiquity of the Anomaluroidea clade in Africa, as expected given the high morphological divergence of the Late Eocene African anomaluroids. Zegdoumyids exhibit a variety of dental morphologies and provide some suggestions on evolutionary trends within the Anomaluroidea (early stages of pentalophodonty, incisor enamel microstructure transitional from the pauciserial to the uniserial condition). The source of Zegdoumyidae is still unclear inasmuch as there is no well-identified sister group among early Palaeogene rodents. Zegdoumyids seem to share a common ancestry with both stem Myodonta and North American Sciuravidae. Given the high degree of dental specialization of zegdoumyids, we cannot exclude the possibility that zegdoumyids are rooted in a more primitive, as yet unknown, African rodent lineage older than the Early-Middle Eocene.

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.

Skeletal ossification and sequence heterochrony in xenarthran evolution

Previous analyses of how mammals vary in their ossification sequences have focused on monotremes, marsupials, and boreoeutherian placentals. Here, we focus on the sequence of cranial and postcranial ossification events during growth in the xenarthran skull and skeleton, including armadillos, anteaters, and sloths. We use two different methods to quantify sequence heterochrony: sequence analysis of variance (ANOVA) and event‐paring/Parsimov. Our results indicate that Parsimov is conservative and does not detect clear heterochronic shifts between xenarthran and boreoeutherian placentals. Sequence‐ANOVA performs better, but both methods exhibit sensitivity to the artifactual accumulation of ties. By controlling for ties and taking into account results that the methods have in common, our analysis suggests that xenarthrans significantly differ from other placentals by a late ossification of the sternum and an early ossification of the phalanges and pubis. We interpret these differences as showing that heterochrony plays a role in the skeletal development of xenarthrans, a change from previous studies that have emphasized the developmental homogeneity of the skeleton across placental mammals.

Masticatory muscle architecture in the Laotian rock rat Laonastes aenigmamus (Mammalia, Rodentia): new insights into the evolution of hystricognathy

We present the first descriptive comparison of the skull, mandible and jaw muscles of the recently recovered Laotian rock rat Laonastes aenigmamus. The gross anatomy of five specimens captured in Laos and internal architecture of the jaw musculature were studied using dissections. The following muscles are described: temporal, masseter, pterygoids, digastric, mylohyoid, geniohyoid and transverse mandibular. The description of the masticatory apparatus of L. aenigmamus offers a rare opportunity to assess the order of establishment of the morphological characters during the evolution of Ctenohystrica. Striking convergences have occurred during the evolution of Diatomyidae and L. aenigmamus presents a unique combination of myological features that corresponds to a mixture of sciurognathous and hystricognathous characters. If L. aenigmamus is a sciurognathous rodent, we have to assume that it independently acquired a pars reflexa of the superficial masseter. We show for the first time that the development of this pars reflexa has occurred several times during the evolution of Ctenohystrica and can no longer be considered a synapomorphic feature of ‘Hystricognathi’. These results bring new insights into the evolution of hystricognathy and have profound implications for the interpretation of the fossil record of early hystricognath rodents.

Mandible shape and dwarfism in squirrels (Mammalia, Rodentia): interaction of allometry and adaptation

Squirrels include several independent lineages of dwarf forms distributed into two ecological groups: the dwarf tree and flying squirrels. The mandible of dwarf tree squirrels share a highly reduced coronoid process and a condylar process drawn backwards. Dwarf flying squirrels on the other hand, have an elongated coronoid process and a well-differentiated condylar process. To interpret such a difference, Elliptic Fourier Transform was used to evaluate how mandible shape varies with dwarfism in sciurids. The results obtained show that this clear-cut difference cannot be explained by a simple allometric relationship in relation with size decrease. We concluded that the retention of anteriorly positioned eye sockets, in relation with distance estimation, allowed the conservation of a well-differentiated coronoid process in all flying species, despite the trend towards its reduction observed among sciurids as their size decreases.

Do Developmental Constraints and High Integration Limit the Evolution of the Marsupial Oral Apparatus

Developmental constraints can have significant influence on the magnitude and direction of evolutionary change, and many studies have demonstrated that these effects are manifested on macroevolutionary scales. Phenotypic integration, or the strong interactions among traits, has been similarly invoked as a major influence on morphological variation, and many studies have demonstrated that trait integration changes through ontogeny, in many cases decreasing with age. Here, we unify these perspectives in a case study of the ontogeny of the mammalian cranium, focusing on a comparison between marsupials and placentals. Marsupials are born at an extremely altricial state, requiring, in most cases, the use of the forelimbs to climb to the pouch, and, in all cases, an extended period of continuous suckling, during which most of their development occurs. Previous work has shown that marsupials are less disparate in adult cranial form than are placentals, particularly in the oral apparatus, and in forelimb ontogeny and adult morphology, presumably due to functional selection pressures on these two systems during early postnatal development. Using phenotypic trajectory analysis to quantify prenatal and early postnatal cranial ontogeny in 10 species of therian mammals, we demonstrate that this pattern of limited variation is also apparent in the development of the oral apparatus of marsupials, relative to placentals, but not in the skull more generally. Combined with the observation that marsupials show extremely high integration of the oral apparatus in early postnatal ontogeny, while other cranial regions show similar levels of integration to that observed in placentals, we suggest that high integration may compound the effects of the functional constraints for continuous suckling to ultimately limit the ontogenetic and adult disparity of the marsupial oral apparatus throughout their evolutionary history.

Life in Burrows Channelled the Morphological Evolution of the Skull in Rodents: the Case of African Mole-Rats (Bathyergidae, Rodentia)

African mole-rats are fossorial rodents that consist of five chisel-tooth digging genera (Heterocephalus, Heliophobius, Georychus, Fukomys, and Cryptomys) and one scratch digger (Bathyergus). They are characterized by striking physiological, morphological, and behavioral adaptations intimately related to their subterranean life. The influence of their mode of life in shaping the cranial morphology has yet to be evaluated in comparison to other Ctenohystrica, especially fossorial genera, which include the subterranean genera Spalacopus and Ctenomys. In our study, we seek to determine to what extent subterranean life affects the morpho-functional properties of the skull among fossorial ctenohystricans. 3D geometric morphometric analyses were performed on 277 skulls, encompassing 63 genera of Ctenohystrica, and complemented by biomechanical studies. African mole-rats and other subterranean Ctenohystrica, especially chisel-tooth diggers, have a short snout, a wide cranium with enlarged zygomatic arches, and a strongly hystricognathous mandible. Even if convergences are also manifest between most fossorial Ctenohystrica, subterranean rodents departed from the main ctenohystrican allometric trends in having a skull shape less size-dependent, but under stronger directional selection with intense digging activity as a major constraint. African mole-rats, notably chisel-tooth diggers, show important mechanical advantage for the temporalis muscles favoring higher forces at the bite point, while mechanical advantage of the superficial masseter muscles is lower compared to other Ctenohystrica. If subterranean species can be clearly discriminated based on their skull morphology, the intrinsic mosaic of anatomical characters of each genus (e.g., skull, teeth, and muscles) can be understood only in the light of their ecology and evolutionary history.

Orientation of the lateral semicircular canal in Xenarthra and its links with head posture and phylogeny: COUTIER et al.

The orientation of the semicircular canals of the inner ear in the skull of vertebrates is one of the determinants of the capacity of this system to detect a given rotational movement of the head. Past functional studies on the spatial orientation of the semicircular canals essentially focused on the lateral semicircular canal (LSC), which is supposedly held close to horizontal during rest and/or alert behaviors. However, they generally investigated this feature in only a few and distantly related taxa. Based on 3D‐models reconstructed from µCT‐scans of skulls, we examined the diversity of orientations of the LSC within one of the four major clades of placental mammals, that is, the superorder Xenarthra, with a data set that includes almost all extant genera and two extinct taxa. We observed a wide diversity of LSC orientations relative to the basicranium at both intraspecific and interspecific scales. The estimated phylogenetic imprint on the orientation of the LSC was significant but rather low within the superorder, though some phylogenetic conservatism was detected for armadillos that were characterized by a strongly tilted LSC. A convergence between extant suspensory sloths was also detected, both genera showing a weakly tilted LSC. Our preliminary analysis of usual head posture in extant xenarthrans based on photographs of living animals further revealed that the LSC orientation in armadillos is congruent with a strongly nose‐down head posture. It also portrayed a more complex situation for sloths and anteaters. Finally, we also demonstrate that the conformation of the cranial vault and nuchal crests as well as the orientation of the posterior part of the petrosal may covary with the LSC orientation in Xenarthra. Possible inferences for the head postures of extinct xenarthrans such as giant ground sloths are discussed in the light of these results.