Jean-Pierre Aguilar

Mosaic convergence of rodent dentitions

Background Understanding mechanisms responsible for changes in tooth morphology in the course of evolution is an area of investigation common to both paleontology and developmental biology. Detailed analyses of molar tooth crown shape have shown frequent homoplasia in mammalian evolution, which requires accurate investigation of the evolutionary pathways provided by the fossil record. The necessity of preservation of an effective occlusion has been hypothesized to functionally constrain crown morphological changes and to also facilitate convergent evolution. The Muroidea superfamily constitutes a relevant model for the study of molar crown diversification because it encompasses one third of the extant mammalian biodiversity. Methodology/Principal Findings Combined microwear and 3D-topographic analyses performed on fossil and extant muroid molars allow for a first quantification of the relationships between changes in crown morphology and functionality of occlusion. Based on an abundant fossil record and on a well resolved phylogeny, our results show that the most derived functional condition associates longitudinal chewing and non interlocking of cusps. This condition has been reached at least 7 times within muroids via two main types of evolutionary pathways each respecting functional continuity. In the first type, the flattening of tooth crown which induces the removal of cusp interlocking occurs before the rotation of the chewing movement. In the second type however, flattening is subsequent to rotation of the chewing movement which can be associated with certain changes in cusp morphology. Conclusion/Significance The reverse orders of the changes involved in these different pathways reveal a mosaic evolution of mammalian dentition in which direction of chewing and crown shape seem to be partly decoupled. Either can change in respect to strong functional constraints affecting occlusion which thereby limit the number of the possible pathways. Because convergent pathways imply distinct ontogenetic trajectories, new Evo/Devo comparative studies on cusp morphogenesis are necessary.

Morphological evolution, ecological diversification and climate change in rodents

Among rodents, the lineage from Progonomys hispanicus to Stephanomys documents a case of increasing size and dental specialization during an approximately 9 Myr time-interval. On the contrary, some contemporaneous generalist lineages like Apodemus show a limited morphological evolution. Dental shape can be related to diet and can be used to assess the ecological changes along the lineages. Consequently, size and shape of the first upper molar were measured in order to quantify the patterns of morphological evolution along both lineages and compare them to environmental trends. Climatic changes do not have a direct influence on evolution, but they open new ecological opportunities by changing vegetation and allow the evolution of a specialist like Stephanomys. On the other hand, environmental changes are not dramatic enough to destroy the habitat of a long-term generalist like Apodemus. Hence, our results exemplify a case of an influence of climate on the evolution of specialist species, although a generalist species may persist without change.

Rodents and climate. 1. A model for estimating past temperatures using arvicolids (Mammalia: Rodentia)

Abstract Analysis of 253 extant mammalian local faunas shows that the number of arvicoline species in each fauna is related to temperature parameters. The very high correlation allows us to propose a method to estimate the temperature for fossil faunas bearing arvicoline species from temperate areas. To illustrate this method, mean annual temperatures were estimated for Late Pleistocene Hungarian localities and for a sequence from the Baume de Gigny (Jura, France). These were compared with results obtained by other techniques (multivariate analysis of rodent associations and synthetic analysis of pollen, faunal, and sedimentological data).

A succession of Miocene rodent assemblages from fissure fillings in southern France: palaeoenvironmental interpretation and comparison with Spain

Abstract An Early to Late Miocene sequence of rodent assemblages from southern France has been quantitatively studied. The resulting pattern seems very similar to a contemporary sequence from central Spain (Calatayud–Teruel Basin). The fossil mammal-bearing localities are of different types: mainly karst infills in France and localities situated in sedimentary basins in Spain. In order to interpret the fossil record, a comparison has been made between southern France faunas of similar age but collected in karst infills and in basin deposits. There seems to be no difference between the two kinds of faunas and thus there is no indication that karst infills systematically give a picture of drier and more open environments. Both types of localities may give a similar relative abundance of taxa and when differences exist they can be attributed to local conditions. The comparison between southern France and the Calatayud–Teruel Basin (central Spain) shows that: (1) similar trends occurred in the two areas; (2) differences between spectra were more important during the late Early Miocene than during the Middle Miocene; (3) the shift between the late Early Miocene and the Middle Miocene environments in southern France does not seem to be correlated with a general drop in temperatures as inferred from the analysis of central Spain faunas.

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.

Topographic maps applied to comparative molar morphology: the case of murine and cricetine dental plans (Rodentia, Muroidea)

Abstract We developed a new method to generate topographic maps of tooth crowns from X-ray synchrotron microtomographic data. Maps are drawn after cervix-plane orientation of tooth image stacks, without the need for a geographic information system. Classical topographic maps with contour lines are complemented by slope maps and angularity maps. Cartography allows precise comparisons of cusps morphologies, and quantification of the directions of cusp axis elongation and slope. Application of this method to muroid rodents with cricetine and murine dental patterns reveals clear-cut differences in cusps morphology that are indicative of the direction of the chewing movement, in agreement with wear facet analyses. Rodents with a murine dental pattern were derived from ancestors with a cricetine pattern, and their origin is associated with important changes in cusp morphology and organization. In order to understand such evolutionary change, our investigation is applied to a sample of extant and fossil muroid rodents that are characterized by either a murine dental plan or a cricetine one, or a dental pattern intermediate between those of cricetines and murines.

Présence de Progonomys (Muridae, Rodentia, Mammalia) dans une association de rongeurs de la fin du Miocène moyen (Castelnou 1B; Pyrénées-orientales, France)

The fossil mammal bearing locality of Castelnou 1 B, a filling of a karstic cavity in the Pyrenees-Orientales (France), yields several species of rodents which are considered as not younger than Late Middle Miocene (Megacricetodon and Democricetodon) together with Progonomys cf. hispanicus, which is up to now found only in the Upper Miocene. The hypothesis that the fauna of Castelnou 1 B results from a mixture of at least two faunas of different age is rejected. Its Late Middle Miocene age raises the question of the date of Progonomys immigration into Europe. A discussion of available data about this event allows to conclude that Progonomys cf. hispanicus of Castelnou 1 B may be at least 12 millions years old.

Évolution géodynamique messino-pliocène en Languedoc central: le paléo-réseau hydrographique de l'Orb et de l'Hérault (sud de la France)

Abstract The proposed reinterpretation of the Upper Neogene geodynamics in central Languedoc is based on both new paleontological and field data. Rodents from the newly discovered fossil mammal-bearing locality of Aigues-Vives and those recently extracted from the site of Servian give the chronological frame. The cartography of the sediments linked to the Messinian erosional phase, as well as those of the Pliocene sequence synthetized the field observations. A precise plotting is given both for the river system cut during the Messinian crisis (Orb, Herault, and some of their tributary streams) and for the Pliocene shoreline especially in the case of the rias formed at the time of the marine transgression. During the Messinian crisis, the bed of the Herault river was incised less than the other river beds because the limestones of the immediate upper part of the area allowed a deep burying of the water table. Central Languedoc illustrates a geodynamical evolution according to Clauzons model of the Messinian endoreic eustatism for the Mediterranean.

Les sciuridés des gisements karstiques du Miocène inférieur à moyen du sud de la France : nouvelles espèces, phylogénie, paléoenvironnement

Resume nous decrivons les sciurides du Miocene inferieur et moyen des gisements karstiques du sud de la France. Quatre nouveaux taxons y sont reconnus : Atlantoxerus martini nov. sp., Atlantoxerus sp. 1, Freudenthalia cuencae nov. sp. et Aragoxerus nov. sp. Ces deux derniers genres sont signales pour la premiere fois dans le sud de la France. Une comparaison avec la Peninsule Iberique est effectuee, elle aborde les problemes de la diversite specifique, de la phylogenie des taxons et de l’origine du peuplement. Des hypotheses concernant la predation de ces ecureuils terrestres et le paleoenvironnement sont proposees.

Intraspecific variation and micro-macroevolution connection: illustration with the late Miocene genus Progonomys (Rodentia, Muridae)

Abstract Recent progresses in our knowledge of mouse odontogenesis have enhanced rodent tooth morphology as a model for Evo-Devo studies. Deciphering the connection between macroevolution and microevolution, however, especially in the case of mammalian teeth, requires examples to illustrate how morphological differences among species, or higher taxa, can stem from population-level processes. In this paper we use paleontological material to study intraspecific variation of tooth morphology in the late Miocene species Progonomys clauzoni, over a short span of geological time in a restricted area. Progonomys is of particular interest as a stem genus of all murine rodents (Old World rats and mice). We use morphometrical and statistical methods to illustrate how change in the amplitude in variation at the population level through geological time is associated with the emergence of new characters. Some of these new characters, including functional ones, become fixed in parallel in distinct murine lineages. Nine million years ago, Progonomys clauzoni displayed variational properties of the developmental system shared by the Murinae, which can also explain some singular tooth characteristics that now are scattered among the diverse lineages. Further morphometric studies, however, are necessary to explain how the variety of cusp patterns observed in Progonomys clauzoni can be explained by developmental properties.