Floréal Solé

Roles of dental development and adaptation in rodent evolution

In paleontology, many changes affecting morphology, such as tooth shape in mammals, are interpreted as ecological adaptations that reflect important selective events. Despite continuing studies, the identification of the genetic bases and key ecological drivers of specific mammalian dental morphologies remains elusive. Here we focus on the genetic and functional bases of stephanodonty, a pattern characterized by longitudinal crests on molars that arose in parallel during the diversification of murine rodents. We find that overexpression of Eda or Edar is sufficient to produce the longitudinal crests defining stephanodonty in transgenic laboratory mice. Whereas our dental microwear analyses show that stephanodonty likely represents an adaptation to highly fibrous diet, the initial and parallel appearance of stephanodonty may have been facilitated by developmental processes, without being necessarily under positive selection. This study demonstrates how combining development and function can help to evaluate adaptive scenarios in the evolution of new morphologies.

New proviverrine genus from the Early Eocene of Europe and the first phylogeny of Late Palaeocene–Middle Eocene hyaenodontidans (Mammalia)

A new genus and new species of Proviverrinae from the Early Eocene of Europe, Morlodon vellerei, is described. This new taxon is morphologically close to the Middle Eocene genus Matthodon, with which it shares tendencies towards a robust dentition; the two genera also share the reduction of P1. In order to examine the phylogenetic relationships of the new genus Morlodon with Early and Middle Eocene European Proviverrinae, a phylogenetic analysis of the earliest hyaenodontidans was conducted. The taxa analysed range from Late Palaeocene to Middle Eocene and are from Africa, Asia, Europe and North America. The new phylogeny of earliest hyaenodontans clarifies the systematics of the paraphyletic assemblage ‘Proviverrinae’ and results in the recognition of five major clades. The monophyly of the Limnocyoninae and Koholiinae is supported, and two new subfamilies are erected from the ‘Proviverrinae’: Sinopaninae and Arfianinae. A new definition of the Proviverrinae is proposed: only European hyaenodontidans from Early and Middle Eocene are included in this subfamily. However, the phylogenetic relationships between the five subfamilies remain to be established. An ancestral morphotype for the Hyaenodontida is proposed in order to identify the different subfamilies. On the basis of the analysis and of data presently available, an African origin for Hyaenodontida is proposed. Hyaenodontidans are involved in the faunal dispersals that occurred around the Palaeocene–Eocene (P/E) boundary. They dispersed from Africa to Asia during the Late Palaeocene (Limnocyoninae), and at the P/E boundary from Africa to Europe (Proviverrinae) and to North America through Europe (Sinopaninae and Arfianinae). Proviverrinae remain an endemic European group, whereas Sinopaninae, Limnocyoninae and Arfianinae mainly evolved in North America. Koholiinae represents the sole endemic African group. The probable African origin of the Hyaenodontida supports the diphyletism of ‘Creodonta’ and abandonment of this taxon. http://zoobank.org/urn:lsid:zoobank.org:pub:450D4FAB-42F0-4824-9DE0-DEED591C0D14

First Clarkforkian equivalent Land Mammal Age in the latest Paleocene basal Sparnacian facies of Europe: fauna, flora, paleoenvironment and (bio)stratigraphy.

The Paleocene-Eocene Thermal Maximum (PETM) is correlated with the first occurrences of earliest modern mammals in the Northern Hemisphere. The latest Paleocene Clarkforkian North American Land Mammal Age, that has yielded rodents and carnivorans, is the only exception to this rule. However, until now no pre-PETM localities have yielded modern mammals in Europe or Asia. We report the first Clarkforkian equivalent Land Mammal Age in the latest Paleocene deposits of the basal Sparnacian facies at Rivecourt, in the north-central part of the Paris Basin. The new terrestrial vertebrate and macroflora assemblages are analyzed through a multidisciplinary study including sedimentologic, stratigraphic, isotopic, and palynological aspects in order to reconstruct the paleoenvironment and to evaluate biochronologic and paleogeographic implications. The mammals are moderately diverse and not abundant, contrary to turtles and champsosaurs. The macroflora is exceptional in preservation and diversity with numerous angiosperms represented by flowers, fruits, seeds and wood preserved as lignite material, revealing an abundance of Arecaceae, Betulaceae, Icacinaceae, Menispermaceae, Vitaceae and probably Cornaceae. Results indicate a Late Paleocene age based on carbon isotope data, palynology and vertebrate occurrences such as the choristoderan Champsosaurus, the arctocyonid Arctocyon, and the plesiadapid Plesiadapis tricuspidens. However, several mammal species compare better with the earliest Eocene. Among these, the particular louisinid Teilhardimys musculus, also recorded from the latest Paleocene of the Spanish Pyrenees, suggests a younger age than the typical MP6 reference level. Nevertheless, the most important aspect of the Rivecourt fauna is the presence of dental remains of a rodent and a “miacid” carnivoran, attesting to the presence of two modern mammalian orders in the latest Paleocene of Europe. Interestingly, these two groups are also the only modern groups recorded from the latest Paleocene of North America, making Rivecourt the first direct equivalent to the Clarkforkian Land Mammal Age outside of North America.

UNDER PRESSURE? DENTAL ADAPTATIONS TO TERMITOPHAGY AND VERMIVORY AMONG MAMMALS

The extant mammals have evolved highly diversified diets associated with many specialized morphologies. Two rare diets, termitophagy and vermivory, are characterized by unusual morphological and dental adaptations that have evolved independently in several clades. Termitophagy is known to be associated with increases in tooth number, crown simplification, enamel loss, and the appearance of intermolar diastemata. We observed similar modifications at the species level in vermivorous clades, although interestingly the vermivorous mammals lack secondarily derived tools that compensate for the dentitions reduced function. We argue that the parallel dental changes in these specialists are the result of relaxed selection on occlusal functions of the dentition, which allow a parallel cascade of changes to occur independently in each clade. Comparison of the phenotypes of Rhynchomys, a vermivorous rat, and strains of mice whose ectodysplasin (EDA) pathway has been mutated revealed several shared dental features. Our results point to the likely involvement of this genetic pathway in the rapid, parallel morphological specializations in termitophagous and vermivorous species. We show that diets or feeding mechanisms in other mammals that are linked to decreased reliance on complex can lead to similar cascades of change.

The hyaenodontidans from the Gour Lazib area (?Early Eocene, Algeria): implications concerning the systematics and the origin of the Hyainailourinae and Teratodontinae

The Algerian localities of the Gour Lazib area (Early or early Middle Eocene) have yielded an important mammalian fauna. The Hyaenodontida are well represented in this fauna: three species–two are new– are reported. The genus Glibzegdouia, which has been previously described as a possible Carnivora, is now clearly referred to the Hyaenodontida. It appears morphologically close to Masrasector and Dissopsalis. A new genus, Furodon, is described. It appears morphologically close to the oldest Pterodon species. This discovery supports an African origin for the hyainailourine genus Pterodon and related genera (e.g. Hyainailouros, Akhnatenavus). Two very small lower molars are referred to a new genus Parvavorodon, which is also referred to Hyainailourinae. The localities of the Gour Lazib area therefore show important hyaenodontid diversity for the Early or early Middle Eocene. We performed a new phylogenetic analysis to question the relationships between the African, Asian, North American and European hyaenodontidans. Our study supports the endemism and originality of the Asian ‘proviverrines’ Indohyaenodon, Paratritemnodon, Kyawdawia and Yarshea; we propose a new subfamily: Indohyaenodontinae. The African ‘proviverrines’ (e.g. Masrasector, Anasinopa, Dissopsalis and Glibzegdouia), which are notably characterized by large premolars and the presence of a wide talonid on the molars, are close to the enigmatic African Teratodon. We therefore propose to refer them to Teratodontinae. The Hyainailourinae, which include the new genus Furodon, are characterized by the presence of secant dentition related to a hypercarnivorous diet. They appear phylogenetically close to the African Koholiinae. The genus Metapterodon is referred to Koholiinae based on the phylogenetic analysis. The African origin of the Teratodontinae and Hyainailourinae is supported by Glibzegdouia and Furodon. The origination of several subfamilies in Africa supports the hypothesis of an African origin for the Hyaenodontida. The origination of the Teratodontinae in Africa contradicts the previous hypotheses of Afro-Asian ‘proviverrines’.

Evolutionary and Biological Implications of Dental Mesial Drift in Rodents: The Case of the Ctenodactylidae (Rodentia, Mammalia)

Dental characters are importantly used for reconstructing the evolutionary history of mammals, because teeth represent the most abundant material available for the fossil species. However, the characteristics of dental renewal are presently poorly used, probably because dental formulae are frequently not properly established, whereas they could be of high interest for evolutionary and developmental issues. One of the oldest rodent families, the Ctenodactylidae, is intriguing in having longstanding disputed dental formulae. Here, we investigated 70 skulls among all extant ctenodactylid genera (Ctenodactylus, Felovia, Massoutiera and Pectinator) by using X-ray conventional and synchrotron microtomography in order to solve and discuss these dental issues. Our study clearly indicates that Massoutiera, Felovia and Ctenodactylus differ from Pectinator not only by a more derived dentition, but also by a more derived eruptive sequence. In addition to molars, their dentition only includes the fourth deciduous premolars, and no longer bears permanent premolars, conversely to Pectinator. Moreover, we found that these premolars are lost during adulthood, because of mesial drift of molars. Mesial drift is a striking mechanism involving migration of teeth allowed by both bone remodeling and dental resorption. This dental innovation is to date poorly known in rodents, since it is only the second report described. Interestingly, we noted that dental drift in rodents is always associated with high-crowned teeth favoring molar size enlargement. It can thus represent another adaptation to withstand high wear, inasmuch as these rodents inhabit desert environments where dust is abundant. A more accurate study of mesial drift in rodents would be very promising from evolutionary, biological and orthodontic points of view.

Evolution of the hypercarnivorous dentition in mammals (Metatheria, Eutheria) and its bearing on the development of tribosphenic molars

One major innovation of mammals is the tribosphenic molar, characterized by the evolution of a neomorphic upper cusp (=protocone) and a lower basin (=talonid) that occlude and provide shearing and crushing functions. This type of molar is an evolutionarily flexible structure that enabled mammals to achieve complex dental adaptations. Among carnivorous mammals, hypercarnivory is a common trend that evolved several times among therians (marsupials, placentals, and stem relatives). Hypercarnivory involves an important simplification of the carnassial molar pattern from the ancestral tribosphenic molar pattern, with the modification of the triangular tooth crown, and the loss of several cusps and cuspids typical of the tribosphenic molar. These losses confer to the molars of the hypercarnivorous mammals a plesiomorphic/paedomorphic morphology that resembles more the earliest mammaliaforms than the earliest therians. Here, we demonstrate that the modification of the molar morphology is fully explained by a patterning cascade mode of cusp development. Contrary to what was previously proposed, our study concludes that the metaconid (mesiolingual cusp of lower molars, associated with a puncturing function) does not influence cusp development of the talonid (distal crushing heel of lower molars). Moreover, it provides a new example of how heterochronic changes were crucial to the evolution of mammal dentition. To overcome the difficulty of applying behavioral or ecological definitions of diets to fossil animals, we characterize hypercarnivorous dentitions on the basis of the molar morphology and more particularly on the loss or retention of crushing structures, each dentition resulting from adaptations to a distinct ecomorphotype. Despite repeated and convergent evolution of hypercarnivorous forms, hypercarnivory appears as a highly constrained specialization (i.e., “dead end”) that is unlikely to evolve back to omnivorous dentition, especially when the crushing structures are lost.