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Of mice and rats: a new molecular palaeobiological approach and best practice in divergence time estimation

Final Report Summary - MURINEVOL (Of mice and rats: a new molecular palaeobiological approach and best practice in divergence time estimation)

The extinct organisms can provide crucial information about the origin and time of origination of extant groups. Development of phylogenetic methods for the study of evolutionary processes through time have revolutionized the field of evolutionary biology and resulted in an unprecedented expansion of our knowledge about the tree of life. These methods have shed light on the macroevolution of many taxonomic groups. Despite an increase of the number of studies addressing the diversification patterns of organisms, no synthesis has addressed the case of the most diversified mammalian clade: the Rodentia. The most important subfamily of rodents is the Murinae (Old World mice and rats). Their outstanding diversity, combined with the richness of their fossil record, makes them the most suitable model to study the factors that promote morphological diversity and trigger evolutionary radiations, which are key components of the tree of life. An essential question in evolutionary biology is to understand the processes that drive the high diversity of some clades. Are they linked to the appearance of key innovations or to environmental and biogeographic changes?
This project unravels for the first time the relationships of this important group of rodents based on new numerical comparative phylogenetic methods. This provides not only the key means of clock calibration but also the knowledge of the mechanism underlying the origin of novelties in this group.
We establish the phylogenetic relationships of extant and extinct murines by combining morphological and molecular data, compile a dataset of characterization of phenotypes of extinct and extant murines in terms of continuous variable characters, calibrate the phylogenetic tree, evaluate the performance of phenotypic data characterized in terms of discrete variable characters (the phenotypic dataset used in the phylogenetic analysis that constitutes Objective 1) and continuous variable characters (Objective 2), to establish maximal first occurrences, and the age of all the constituent fossil record (Objective 3), to infer the best practise approach to the use of fossil data in the tip-calibration of the molecular clock (Objective 4), and to test macroevolutionary hypothesis (Objective 5).
The results demonstrate the importance of including both extant and extinct members of a clade in cladistic analyses in order to accurately calibrate phylogenies and to explore the correlation between phenotypic innovations, biogeographic events, climatic changes, and diversification.
1) The matrix including morphological continuous and discrete and molecular data of more than 100 extinct and extant murine taxa has been achieved. This work had not been done by anyone before (Figs 1-3).
2) Fossil taxa have been included as terminal tips within a molecular clock analysis (tip-calibration) using the supermatrix already constructed for phylogenetic analysis (objective 1), alternately employing the discrete character (objective 1) and continuous variable character (objective 2) phenotypic data to evaluate the performance of these alternate approaches to characterising morphology.
3) For the first time the murine fossil record has been accurately classified on the basis of morphological discrete and continuous characters into the different tribe resultant from molecular analyses (Arvicanthini, Otomyini, Millardini, Apodemini, Malacomyini, Praomyini, Murini, Hydromyini, Rattini).
4) The maximal first occurrences, and also the age of all the constituent fossil record of murines has been established.
5) The first fossil murine from Lebanon has been identified (Figure 4).

6) The application of numerical comparative phylogenetic methods has clarified the role that extrinsic and intrinsic factors and the mechanisms underlying the origin of novelties had during the evolution of some group of rodents. The evolutionary history of some group of rodents seems to have been mainly triggered by abiotic phenomena. For instance, gundis show accelerated evolutionary rates and greater disparity at 13.7 8 and 2.5 Ma, which correlate with important environmental events (Figure 5). Likewise, the study of rhizomyine rodents demonstrated a linkage of monsoon variations and their tempo and mode in evolution (figure 6).
7) Patterns of diversification rates and the impact of biotic (“key innovations”) and/or abiotic factors in a phylogenetic context have been documented. The results do not show an evident linkage between radiation and ecological opportunities in murines.
8) An exceptionally preserved murine specimen has been CT-scanned twice. The first time for reconstructing the whole skeleton and the second so as to get a 3D reconstruction of the mandible and cranial fragment at higher resolution (Figure 7).
9) Synchrotron X-ray fluorescence and absorption spectroscopy as well as infrared spectroscopy has been applied to the same exceptionally preserved specimen and confirmed the preservation of soft tissue in the body, such as viscera and hairs (Figure 8).
Impact: Integration of these data has led to the establishment of a state of the art approach to divergence time estimation, linking this to phenotypic evolution, as well as to extrinsic phenomena including causal agents of evolutionary change like global climate evolution. Several SCI papers as well as book chapters have been already published or are being in press and more will follow.

2016. A transitional gundi (Rodentia: Ctenodactylidae) from the Miocene of Israel [PLoS One]
2016 The family Petromuridae (in press.) [Handbook of Mammals of the World]
2016 The family Thryonomyidae (in press.) [Handbook of Mammals of the World]
2016 The family Ctenodactylidae (in press.) [Handbook of Mammals of the World]
2016 The family Pedetidae (in press.) [Handbook of Mammals of the World]
2015 Miocene rodent from Lebanon provides the "missing link" between Asian and African gundis (Rodentia: Ctenodactylidae) [Scientific Reports]
2015 Causal evidence between monsoon and evolution of rhizomyine rodents. [Scientific Reports]
2015 Palaeodiversity of Cricetodontini during the late Aragonian (Middle Miocene) from the European basins [Palaeobiodiversity and Palaeoenvironments]

Training activities
I have been trained by Prof. P. Donoghue, Prof. Z. Yang and M. do Reis in the use of Bayesian phylogenetic analyses using MrBayes, in the alignment of molecular sequences using PRANK and in evaluating the impact of analysing the data using JModelTest (nucleotides) and ProtTest (amino acids).
I have attended lectures and workshops offered by the School of Earth Sciences, which covered topics and skills relevant to the project, particularly:
- workshop on Bayesian Methods to Estimate Species Divergence Times;
- a suite of courses within the module "Evolution of the Biosphere" (EASC30008_2014) given by Prof. M. Benton, which included a suite of training in the handling of the statistical software R and its applications in plotting palaeodiversity charts and palaeomaps, as well as phylogenetic comparative methods in macroevolution.
- a suite of courses entitled “Methods for Visualizing Fossils in 3D”, which was a unique opportunity to receive a one-to-one training by experts in a variety of cutting-edge methods and approaches. The following topics were covered “Avizo – licensed software for 3-D visualization” (demonstrated by S. Lautenschlager), “SPIERS – free software for 3-D visualization” (demonstrated by R. Garwood and M. Sutton), “Blender – free software for 3-D animation and creation” (demonstrated by S. Lautenschlager and R. Garwood), “NextEngine laser scanner & Scanstudio – capturing surface features of fossils in 3D” (demonstrated by T. Davies) and “Makerbot 3-D printing – printing scalable 3-D models of fossils” (demonstrated by T. Davies).
Finally, I attended the workshop: "How to prepare a good research bid for Science and Engineering" offered by the University of Bristol on complementary skills.

Transfer of knowledge activities
-I have been referee of the following doctoral dissertations:
- "Evolución de la biodiversidad en micromamíferos del Neógeno de la Cuenca de Madrid: relaciones entre patrones morfométricos, ecológicos y ambientales" submitted for the degree of Doctor of Philosophy in Physics and defended on April the 22nd of 2016 by Verónica Hernández Ballarín at the Complutense University of Madrid (Madrid, Spain);
- "Estudio del Protictitherium crassum del Cerro de los Batallones (Torrejón de Velasco, Madrid): Aportación a la filogenia y evolución de la familia Hyaenidae" submitted for the degree of Doctor of Philosophy in Physics and defended on January the 26th of 2016 by Susana Fraile Gracia at the Complutense University of Madrid (Madrid, Spain)
-I have been tutor of two students within the MSc Palaeobiology program of the School of Earth Sciences at the University of Bristol: Giuseppe Mennella and Shay Mullineaux.
- I have presented project results at large international meetings:
- Communication at the 74th Annual Meeting of the Society of Vertebrate Paleontology, held in Berlin, Germany, in November 5-8, 2014;
- Communication at the 75th Annual Meeting of the Society of Vertebrate Paleontology, held in Dallas, USA, in October 14-17, 2015;
- Communication at the 76th Annual Meeting of the Society of Vertebrate Paleontology, which will be held in Salt Lake City, USA, in October 26-29, 2016.
- I have taken part to the community service by:
- co-hosting and guiding visitors of the temporary exhibit “Telling the Color of Dinosaurs”, at the Bristol Museum & Art Gallery, Bristol;
- having a stand at the event "Bristol Bright Night" held in "At Bristol", Bristol;
- showcasing my research at University of Bristol open days.