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.
Investigating life history traits in mammals is crucial to understand their survival in changing environments. However, these parameters are hard to estimate in a macroevolutionary context. Here we ...show that the use of dental ontogenetic parameters can provide clues to better understand the adaptive nature of phenotypic traits in extinct species such as South American notoungulates. This recently extinct order of mammals evolved in a context of important geological, climatic, and environmental variations. Interestingly, notoungulates were mostly herbivorous and acquired high-crowned teeth very early in their evolutionary history. We focused on the variations in crown height, dental eruption pattern, and associated body mass of 69 notoungulate taxa, placed in their phylogenetic and geological contexts. We showed that notoungulates evolved higher crowns several times between 45 and 20 Ma, independently of the variation in body mass. Interestingly, the independent acquisitions of ever-growing teeth were systematically accompanied by eruption of molars faster than permanent premolars. These repeated associations of dental innovations have never been documented for other mammals and raise questions on their significance and causal relationships. We suggest that these correlated changes could originate from ontogenetic adjustments favored by structural constraints, and may indicate accelerated life histories. Complementarily, these more durable and efficient dentitions could be selected to cope with important ingestions of abrasive particles in the context of intensified volcanism and increasing aridity. This study demonstrates that assessing both life history and ecological traits allows a better knowledge of the specializations of extinct mammals that evolved under strong environmental constraints.
Xenarthrans are unique among mammals in retaining simplified teeth that are rootless and homodont, which makes it difficult to determine dental homologies. We apply computerized tomography to ...prenatal developmental series of extant sloths, Bradypus and Choloepus, to further elucidate the patterns of morphological variation in their dentition. We also propose new criteria based on sequences of dental mineralization, and the presence of vestigial teeth, to distinguish between caniniforms and postcaniniforms. We report for the first time the presence of vestigial incisors in Bradypus. We also show the presence of a vestigial tooth in front of the lower caniniform in both extant sloth genera and the existence of two generations for the upper caniniform in Choloepus. The study of their sequence of mineralization indicates that the lower and upper caniniform teeth are not homologous in sloths, and suggests that upper caniniforms are not homologous between the two extant sloth genera. Our results show that assessing the developmental processes and functional constraints remains crucial to understand the dental variations observed in sloths, and more generally, tooth class homology issues in mammals. Applied to the tooth row of all extinct sloths, these developmental data illuminate a potentially ancestral dental formula for sloths.
Rodents show a wide range of anatomical, physiological, and behavioral adaptations to life underground. Cranial and postcranial bone morphologies are deeply impacted by the modes of digging, which ...can involve either incisors or claws. However, the morphological variation of these elements still needs to be accurately quantified to assess the degree of specializations of the fossorial rodent families in regards to their respective evolution. Here, we focus on the morpho-functional characteristics of the masticatory apparatus in two families of subterranean rodents, the Spalacidae and Bathyergidae. We quantify skull shape in five spalacid genera using geometric morphometric methods, as well as biomechanical estimates for adductor muscles, which are compared with data previously published on bathyergids. We show that skull shape of spalacids has a greater disparity and lower biomechanical estimates than bathyergids, in which the fossorial activity, notably chisel-tooth digging, more significantly impacted the evolution of the skull. Among spalacids,
Spalax
shows the most extreme specializations to life underground and displays the highest number of morphological convergences with chisel-tooth digging bathyergids, especially regarding its cranial shape and high biomechanical estimate for the temporalis muscle. Fewer morphological convergences were observed between other spalacids and bathyergids. Different evolutionary histories can potentially explain discrepancies observed between the two families, the first bathyergid morphological adaptations to fossorial life being much older than those of spalacids.
Understanding the origins of morphological specializations in mammals is a key goal in evolutionary biology. It can be accomplished by studying dental homology, which is at the core of most ...evolutionary and developmental studies. Here, we focused on the evolution and development of the specialized dentition of hyraxes for which dental homologies have long been debated, and could have implications on early placental evolution. Specifically, we analysed dental mineralization sequences of the three living genera of hyraxes and 17 fossil species using X‐ray computed microtomography. Our results point out the labile position of vestigial upper teeth on jaw bones in extant species, associated with the frequently unusual premolar shape of deciduous canines over 50 Ma of hyracoid evolution. We proposed two evolutionary and developmental hypotheses to explain these original hyracoid dental characteristics. (a) The presence of a vestigial teeth on the maxilla in front of a complex deciduous canine could be interpreted as extra‐teeth reminiscent of early placental evolution or sirenians, an order phylogenetically close to hyracoids and showing five premolars. (b) These vestigial teeth could also correspond to third incisors with a position unusually shifted on the maxilla, which could be explained by the dual developmental origin of these most posterior incisors and their degenerated condition. This integrative study allows discussion on the current evolutionary and developmental paradigms associated with the mammalian dentition. It also highlights the importance of nonmodel species to understand dental homologies.
Illustration of vestigial teeth in an embryo of extant hyrax (Heterohyrax)
Notoungulates are an extinct clade of South American mammals, comprising a large diversity of body sizes and skeletal morphologies, and including taxa with highly specialized dentitions. The ...evolutionary history of notoungulates is characterized by numerous dental convergences, such as continuous growth of both molars and incisors, which repeatedly occurred in late-diverging families to counter the effects of abrasion. The main goal of this study is to determine if the acquisition of high-crowned incisors in different notoungulate families was accompanied by significant and repeated changes in their enamel microstructure. More generally, it aims at identifying evolutionary patterns of incisor enamel microstructure in notoungulates. Fifty-eight samples of incisors encompassing 21 genera of notoungulates were sectioned to study the enamel microstructure using a scanning electron microscope. We showed that most Eocene taxa were characterized by an incisor schmelzmuster involving only radial enamel. Interestingly, derived schmelzmusters involving the presence of Hunter-Schreger bands (HSB) and of modified radial enamel occurred in all four late-diverging families, mostly in parallel with morphological specializations, such as crown height increase. Despite a high degree of homoplasy, some characters detected at different levels of enamel complexity (e.g., labial versus lingual sides, upper versus lower incisors) might also be useful for phylogenetic reconstructions. Comparisons with perissodactyls showed that notoungulates paralleled equids in some aspects related to abrasion resistance, in having evolved transverse to oblique HSB combined with modified radial enamel and high-crowned incisors.
Contrary to their reptilian ancestors, which had numerous dental generations, mammals are known to usually develop only two generations of teeth. However, a few mammal species have acquired the ...ability to continuously replace their dentition by the constant addition of supernumerary teeth moving secondarily toward the front of the jaw. The resulting treadmill-like replacement is thus horizontal, and differs completely from the vertical dental succession of other mammals and their extinct relatives. Despite the developmental implications and prospects regarding the origin of supernumerary teeth, this striking innovation remains poorly documented. Here we report another case of continuous dental replacement in an African rodent, Heliophobius argenteocinereus, which combines this dental system with the progressive eruption of high-crowned teeth. The escalator-like mechanism of Heliophobius constitutes an original adaptation to hyper-chisel tooth digging involving high dental wear. Comparisons between Heliophobius and the few mammals that convergently acquired continuous dental replacement reveal that shared inherited traits, including dental mesial drift, delayed eruption, and supernumerary molars, comprise essential prerequisites to setting up this dental mechanism. Interestingly, these dental traits are present to a lesser extent in humans but are absent in mouse, the usual biological model. Consequently, Heliophobius represents a suitable model to investigate the molecular processes leading to the development of supernumerary teeth in mammals, and the accurate description of these processes could be a significant advance for further applications in humans, such as the regeneration of dental tissues.
The study of convergences in mammals is crucial to understand the evolutionary processes underlying the origin of shared traits. A classic example is the independent evolution in the pygmy ...rock-wallaby, the silvery mole-rat, and manatees of continuous dental replacement to compensate for high dental wear. The origins of continuous dental replacement in mammals remain unresolved. As the functional study of a trait may permit pinpointing the adaptive nature of its independent evolution, we aimed at comparing first the morpho-functional characteristics of the masticatory apparatus between the pygmy rock-wallaby and their closest relatives, and then with some published data on the silvery mole-rat. 3D geometric morphometric and biomechanical analyses were complemented by dental microwear analyses. Our results showed that the pygmy rock-wallaby clearly departs from its relatives in having a wider skull, a shorter snout, and a dentition situated more distally. These cranial modifications, previously observed in the silvery mole-rat, are probably linked with a neotenic development. Because of higher developmental constraints on marsupial skulls, such adjustment in the pygmy rock-wallaby may have improved the force generated by adductor muscles at molars for comminution of tough and abrasive plants. In contrast, the strong attrition combined with the ingestion of dust during high activity of digging and feeding might contribute to both molar damage and high wear in the silvery mole-rat. Our results stress the importance of combining morphological, developmental, and functional data to show that different behaviors related to ecology can explain the convergent occurrence of continuous dental replacement in mammals.
Mice from the Orkney archipelago exhibit an important diversity regarding molar shape. While on some islands mice display a usual dental pattern, teeth from other islands display additional cusplets ...and unusual phenotypes that may constitute case studies for evaluating the potential functional relevance of dental changes. We developed a multifaceted approach combining 2D and 3D geometric morphometrics, dental topography, dental wear, biomechanics, estimations of masticatory muscles force, and in vivo bite force on wild-derived lab descendants exemplifying the two extreme dental morphologies. The two strains differed in the geometry of the upper and lower tooth rows, and in the topography of the upper row only. Surprisingly, the most unusual tooth morphology appeared as the least complex because tooth simplification overwhelmed the signal provided by the occurrence of additional cusplets. No difference in bite force nor muscle force was evidenced, showing that the important change in dental morphology was accommodated without major changes in the rest of the masticatory apparatus. The evolution of unusual dental phenotypes was possibly fueled by drift and inbreeding in small and isolated populations on remote islands of the archipelago. No functional counter-selection impeded this diversification, since the unusual dental phenotypes did not disrupt occlusion and mastication.
Evolutionary changes in vertebrates are linked to genetic alterations that often affect tooth crown shape, which is a criterion of speciation events. The Notch pathway is highly conserved between ...species and controls morphogenetic processes in most developing organs, including teeth. Epithelial loss of the Notch-ligand Jagged1 in developing mouse molars affects the location, size and interconnections of their cusps that lead to minor tooth crown shape modifications convergent to those observed along Muridae evolution. RNA sequencing analysis revealed that these alterations are due to the modulation of more than 2000 genes and that Notch signaling is a hub for significant morphogenetic networks, such as Wnts and Fibroblast Growth Factors. The modeling of these tooth crown changes in mutant mice, via a three-dimensional metamorphosis approach, allowed prediction of how Jagged1-associated mutations in humans could affect the morphology of their teeth. These results shed new light on Notch/Jagged1-mediated signaling as one of the crucial components for dental variations in evolution.
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