Rodent Macroevolution in the context of Major Miocene Environmental Changes – RoMa

This project examines the evolutionary history and diversification of rodent species, focusing on their biogeographical movements, morphological adaptations, and macroevolutionary patterns. The study focuses on several rodent families that benefited from the land bridge between Eurasia and Africa. These include ctenodactylines, rhizomyines, zapodids, sciurids, gerbillines, murines, glirids, thryonomyids, and pedetids, whose evolution is analyzed using either morphological or molecular data, or both, from the fossil record and living rodents.

Taxonomic studies will be conducted to build morphological datasets for phylogenetic analysis, examining the evolutionary role of climatic and biotic factors in rodent diversification.

Fossil material from Miocene sites in Lebanon, Israel, Greece, and Turkey, as well as extensive collections from museums in France, Spain, the UK, and Germany, are being used. Extant rodent specimens are being incorporated.

Geometric morphometrics involves the use of 2D and 3D techniques to analyze rodent molar shapes, particularly the occlusal surfaces. This is achieved using 2D outline-based methods, which leverage high-resolution images obtained through the Leica M205C microimaging system. Points along the molar outlines are digitized using TPSdig, and Fourier analysis of these shapes is performed using the Momocs R package. Additionally, 3D descriptors are extracted from µCT scan data and processed using software like AVISO, while analytical packages such as Morpho and mesheR in R allow further exploration of molar geometry.

To obtain 3D morphological data, micro-CT scanning is employed with advanced imaging systems. These systems capture high-resolution models that are further analyzed for functional attributes such as sharpness, complexity, and relief using the molaR package.

Phylogenetic and evolutionary relationships are explored using Bayesian approaches (BEAST and Mr Bayes) integrating extinct and extant taxa for phylogenetic inference and divergence time estimation.

Biogeographic analyses rely on dispersal-extinction-cladogenesis (DEC) models, which use time-calibrated phylogenies and paleogeographic scenarios to model the connectivity and dispersal events of rodent clades. These models are implemented through advanced C++ extensions for robust biogeographic reconstructions.

To study diversification rates, probabilistic models such as BAMM and PyRate are used. These models estimate rates of speciation, extinction, and preservation by analyzing fossil occurrence data and phylogenetic branch lengths. The results of these models are cross-referenced with climatic and morphological datasets to test macroevolutionary hypotheses.

Statistical and computational analyses are performed in the R environment, with various packages enabling data visualization, statistical modeling, and phylogenetic manipulations.

Interdisciplinary research integrating paleontology and molecular biology to evaluate evolutionary patterns in extinct vertebrates remains relatively uncommon. To address this gap, ANR RoMa team researchers have carried out a review highlighting the latest methods that can now be applied by paleontologists to adopt a holistic approach to understanding long-term evolutionary patterns and mechanisms (López-Antoñanzas et al., 2022).

For the moment, we have already compiled a large morphological database for several groups of rodents, as detailed below:

1-Cricetodontinae: This extinct group of rodents was studied using morphological and phylogenetic approaches. We compared phylogenetic tree topologies derived from classical and Bayesian methods. The results demonstrated that Miocene cooling events influenced the evolution of Cricetodontinae, promoting dispersal and leading to significant origination and extinction events (López-Antoñanzas et al., 2024a; López-Antoñanzas & Peláez-Campomanes, 2022).

2-Cricetinae: We conducted research on the origin and early diversification of these rodents using Miocene and Pliocene fossils and employing Bayesian and parsimony methods. This work resolved systematic uncertainties and provided insights into relationships among several genera (Dirnberger et al., 2024).

3-Muroidae: This superfamily, which includes mice and rats, was examined using a morphological database of fossils combined with molecular data. We proposed new age estimates for major clades, such as the Muridae and Cricetodontinae, integrating fossil data to refine the timing of their emergence. This study also revealed significant biogeographic dynamics, with frequent dispersals, particularly into East Asia during the Miocene (López-Antoñanzas et al., 2024b).

4-Muridae in Iran: In collaboration with a researcher from the University of Tehran, we have explored the evolution and geographic history of murids in Iran. Molecular analysis dated the divergence of primary groups to approximately 12.3 million years ago, with gerbils diverging later, around 10 million years ago, in alignment with fossil data. This study highlighted the role of the Zagros and Alborz mountain formations in driving speciation among Iranian rodents (Afzali & López-Antoñanzas, 2024).

These studies emphasize the importance of integrating morphological data from fossils with information from extant species to better understand the evolutionary history of rodents and the geographic events that shaped their diversification.

RoMa aims to address fundamental gaps in understanding the evolutionary history of rodents by integrating comprehensive morphological, molecular, and ecological data within innovative analytical frameworks.

One of the foremost challenges in evolutionary studies is the lack of detailed morphological databases, particularly for fossil taxa and even for extant species. These gaps hinder accurate phylogenetic reconstructions, limiting our ability to understand evolutionary relationships and diversification processes. To tackle this, the ANR project RoMa focuses on systematically collecting dental morphological data for various muroid groups.

Key efforts include gathering data for primitive rodent taxa with cricetid dental patterns or murid rodents. For instance, despite their significance, the phylogeny of many fossil representatives of murines remains unresolved, with limited studies sampling both extinct and extant taxa across broad temporal and geographic ranges. Preliminary phylogenetic analyses suggests discrepancies between molecular evidence and the fossil record. For example, groups like the Rattini, considered basal murines molecularly, only appear in the Pliocene, whereas groups like the Apodemyini, deemed more derived molecularly, are among the earliest murines in the fossil record. These inconsistencies underscore the need for integrative approaches combining molecular and morphological datasets. To address this, the project employs a “morpho-molecular clock” framework, starting with murines and aiming to extend this methodology to other rodent groups. This total evidence approach strengthens phylogenetic hypotheses, providing a more comprehensive view of rodent evolution.

Additionally, supervised PhD projects are expanding knowledge on cricetid evolution. These studies aim to clarify phylogenetic relationships, divergence times, and the environmental factors influencing cricetid diversification and adaptation.

An innovative aspect of the research involves incorporating continuous morphological characters alongside traditionally used discrete traits. Continuous traits provide insights into gradual evolutionary changes and complement phylogenetic data. Collaborations with ANR researchers like Sabrina Renaud and Tiago Simões enrich these analyses, enabling a more nuanced understanding of morphological evolution across rodent lineages.

Another critical perspective is estimating ancestral states to link morphological evolution with environmental and ecological shifts. Advanced probabilistic models like BAMM and PyRate will estimate diversification rates using time-calibrated phylogenies and fossil occurrence data.

These methods will reveal the tempo and mode of diversification, identifying periods of rapid evolutionary change and their drivers.

This work has the potential to uncover the complex interplay between ecological factors, evolutionary mechanisms, and biodiversity patterns, providing a holistic view of how life evolves.

The Miocene is characterized by important tectonic activity that drove sea level changes and orogeny, in turn significantly altering
the climate. About 20 million years ago the contact between Afro-Arabia and Eurasia created a land-bridge that enabled faunal
exchanges between these two continents. The aim of this project is to unravel the evolutionary response of the most speciose group
of mammals, the rodents, in this unique context of overwhelming biotic and abiotic perturbations. Cutting-edge methodologies
together with a combination of morphological and molecular approaches with time-calibrated phylogenetic trees will allow inferring
the dynamics of speciation and extinction and the variation of diversity among lineages. Long-standing questions in evolutionary
biology will be addressed: why certain clades are highly diversified while others are not? Is this due to the appearance of key
innovations or related to extrinsic factors?