Elodie Renvoisé

Replaying evolutionary transitions from the dental fossil record

The evolutionary relationships of extinct species are ascertained primarily through the analysis of morphological characters. Character inter-dependencies can have a substantial effect on evolutionary interpretations, but the developmental underpinnings of character inter-dependence remain obscure because experiments frequently do not provide detailed resolution of morphological characters. Here we show experimentally and computationally how gradual modification of development differentially affects characters in the mouse dentition. We found that intermediate phenotypes could be produced by gradually adding ectodysplasin A (EDA) protein in culture to tooth explants carrying a null mutation in the tooth-patterning gene Eda. By identifying development-based character inter-dependencies, we show how to predict morphological patterns of teeth among mammalian species. Finally, in vivo inhibition of sonic hedgehog signalling in Eda null teeth enabled us to reproduce characters deep in the rodent ancestry. Taken together, evolutionarily informative transitions can be experimentally reproduced, thereby providing development-based expectations for character-state transitions used in evolutionary studies.

EVOLUTION OF MAMMAL TOOTH PATTERNS: NEW INSIGHTS FROM A DEVELOPMENTAL PREDICTION MODEL

The study of mammalian evolution is often based on insights into the evolution of teeth. Developmental studies may attempt to address the mechanisms that guide evolutionary changes. One example is the new developmental model proposed by Kavanagh et al. (2007), which provides a high-level testable model to predict mammalian tooth evolution. It is constructed on an inhibitory cascade model based on a dynamic balance of activators and inhibitors, regulating differences in molar size along the lower dental row. Nevertheless, molar sizes in some mammals differ from this inhibitory cascade model, in particular in voles. The aim of this study is to point out arvicoline and murine differences within this model and to suggest an alternative model. Here we demonstrate that the inhibitory cascade is not followed, due to the arvicolines greatly elongated first lower molar. We broaden the scope of the macroevolutionary model by projecting a time scale onto the developmental model. We demonstrate that arvicoline evolution is rather characterized by a large gap from the oldest vole to more recent genera, with the rapid acquisition of a large first lower molar contemporaneous to their radiation. Our study provides alternative evolutionary hypotheses for mammals with different trajectories of development.

Morphological modularity and assessment of developmental processes within the vole dental row (Microtus arvalis, Arvicolinae, Rodentia)

SUMMARY Knowledge of mammalian tooth formation is increasing, through numerous genetic and developmental studies. The prevalence of teeth in fossil remains has led to an intensive description of evolutionary patterns within and among lineages based on tooth morphology. The extent to which developmental processes have influenced tooth morphologies and therefore the role of these processes in these evolutionary patterns are nonetheless challenging. Recent methodological advances have been proposed allowing the inference of developmental processes from adult morphologies and the characterization of the degree of developmental integration/modularity of morphological traits by studying the patterns of variation within and among individuals. This study focuses on the geometric shape of the lower molars of the vole species Microtus arvalis. Our results suggest (i) quasi‐independence of each molar at the developmental level (developmental modules), even slightly stronger for the third molar supporting some genetic and developmental hypotheses and (ii) more pervasive integration processes among molars at the morphological level.

The changing pace of insular life: 5000 years of microevolution in the Orkney vole (Microtus arvalis orcadensis).

Island evolution may be expected to involve fast initial morphological divergence followed by stasis. We tested this model using the dental phenotype of modern and ancient common voles (Microtus arvalis), introduced onto the Orkney archipelago (Scotland) from continental Europe some 5000 years ago. First, we investigated phenotypic divergence of Orkney and continental European populations and assessed climatic influences. Second, phenotypic differentiation among Orkney populations was tested against geography, time, and neutral genetic patterns. Finally, we examined evolutionary change along a time series for the Orkney Mainland. Molar gigantism and anterior‐lobe hypertrophy evolved rapidly in Orkney voles following introduction, without any transitional forms detected. Founder events and adaptation appear to explain this initial rapid evolution. Idiosyncrasy in dental features among different island populations of Orkney voles is also likely the result of local founder events following Neolithic translocation around the archipelago. However, against our initial expectations, a second marked phenotypic shift occurred between the 4th and 12th centuries AD, associated with increased pastoral farming and introduction of competitors (mice and rats) and terrestrial predators (foxes and cats). These results indicate that human agency can generate a more complex pattern of morphological evolution than might be expected in island rodents.

THE CHANGING PACE OF INSULAR LIFE

Island evolution may be expected to involve fast initial morphological divergence followed by stasis. We tested this model using the dental phenotype of modern and ancient common voles (Microtus arvalis), introduced onto the Orkney archipelago (Scotland) from continental Europe some 5000 years ago. First, we investigated phenotypic divergence of Orkney and continental European populations and assessed climatic influences. Second, phenotypic differentiation among Orkney populations was tested against geography, time, and neutral genetic patterns. Finally, we examined evolutionary change along a time series for the Orkney Mainland. Molar gigantism and anterior‐lobe hypertrophy evolved rapidly in Orkney voles following introduction, without any transitional forms detected. Founder events and adaptation appear to explain this initial rapid evolution. Idiosyncrasy in dental features among different island populations of Orkney voles is also likely the result of local founder events following Neolithic translocation around the archipelago. However, against our initial expectations, a second marked phenotypic shift occurred between the 4th and 12th centuries AD, associated with increased pastoral farming and introduction of competitors (mice and rats) and terrestrial predators (foxes and cats). These results indicate that human agency can generate a more complex pattern of morphological evolution than might be expected in island rodents.

When less means more: evolutionary and developmental hypotheses in rodent molars

Tooth number in rodents is an example of reduction in evolution. All rodents have a toothless diastema lacking canine and most premolars present in most other mammals. Whereas some rodent lineages retained one premolar (p4), many others lost it during evolution. Recently, an ‘inhibitory cascade’ developmental model (IC) has been used to predict how the first molar (m1) influences the number and relative sizes of the following distal molars (m2 and m3). The model does not, however, consider the presence of premolars, and here we examine whether the premolar could influence and constrain molar proportions during development and evolution. By investigating a large data set of both extinct and extant rodent families over more than 40 million years, we show that the basal phenotype is characterized by the presence of premolars together with equally sized molars. More recent rodent families, with and without premolar, show more unequal molar sizes. Analysing molar areas, we demonstrated that (i) rodents harbour almost all the molar proportions known in mammals, and the IC model can explain about 80% of taxa in our data set; (ii) proportions of molars are influenced by the presence or absence of p4; and (iii) the most variable teeth in the dental row are m1 and m3, whether p4 is present or not. Moreover, m1 can represent up to half of the total molar area when p4 is absent. We hypothesize that p4 loss during evolution released the constraint on m1 development, resulting in a more variable size of m1 and thereby having an indirect effect on the evolution of the whole molar row.

Isotopic partitioning by small mammals in the subnivium

Abstract In the Arctic, food limitation is one of the driving factors behind small mammal population fluctuations. Active throughout the year, voles and lemmings (arvicoline rodents) are central prey in arctic food webs. Snow cover, however, makes the estimation of their winter diet challenging. We analyzed the isotopic composition of ever‐growing incisors from species of voles and lemmings in northern Finland trapped in the spring and autumn. We found that resources appear to be reasonably partitioned and largely congruent with phylogeny. Our results reveal that winter resource use can be inferred from the tooth isotopic composition of rodents sampled in the spring, when trapping can be conducted, and that resources appear to be partitioned via competition under the snow.

Mechanical constraint from growing jaw facilitates mammalian dental diversity.

Significance Good examples of the relative autonomy of organ development are teeth, and for decades researchers have cultured isolated mouse teeth on a petri dish by starting from the earliest recognizable stage. We have cultured cheek teeth of voles, another species of rodent, and show how the cultured vole teeth lack their species-specific morphology. Based on computational modeling, 3D imaging, and experiments in which we culture mouse and vole teeth between microscopic braces, we suggest that the development of vole tooth shape requires the lateral support of the jaw. Because mice lack the vole-specific morphology, the requirement of the jaw for tooth shape has not been possible to uncover previously. Comparative studies are required for the understanding of organogenesis. Much of the basic information about individual organ development comes from studies using model species. Whereas conservation of gene regulatory networks across higher taxa supports generalizations made from a limited number of species, generality of mechanistic inferences remains to be tested in tissue culture systems. Here, using mammalian tooth explants cultured in isolation, we investigate self-regulation of patterning by comparing developing molars of the mouse, the model species of mammalian research, and the bank vole. A distinct patterning difference between the vole and the mouse molars is the alternate cusp offset present in the vole. Analyses of both species using 3D reconstructions of developing molars and jaws, computational modeling of cusp patterning, and tooth explants cultured with small braces show that correct cusp offset requires constraints on the lateral expansion of the developing tooth. Vole molars cultured without the braces lose their cusp offset, and mouse molars cultured with the braces develop a cusp offset. Our results suggest that cusp offset, which changes frequently in mammalian evolution, is more dependent on the 3D support of the developing jaw than other aspects of tooth shape. This jaw–tooth integration of a specific aspect of the tooth phenotype indicates that organs may outsource specific aspects of their morphology to be regulated by adjacent body parts or organs. Comparative studies of morphologically different species are needed to infer the principles of organogenesis.