Periodic Reporting for period 5 - ADaPTIVE (Analysing Diversity with a Phenomic approach: Trends in Vertebrate Evolution)
Reporting period: 2021-06-01 to 2022-11-30
What processes have shaped the evolution of animal diversity through deep time? Approaches to this question can focus on many different factors, from life history and ecology to large-scale environmental change and extinction, and measure diversity in many ways. To date, the majority of studies on the evolution of diversity across large groups have focused on relatively simple metrics, specifically taxon counts or body size. However, three-dimensional descriptors of organismal shape better capture their diversity and provide a more complete picture of evolutionary change. Morphological data can also bridge deep-time palaeobiological analyses, which are ideal for understanding macro-scale environmental influences on evolution, with studies of the genetic and developmental factors that shape variation within species and must also influence large-scale patterns of evolutionary change. Thus, accurately reconstructing the patterns and processes underlying evolution, including understanding how and why species respond differently to environmental change, requires an approach that can robustly represent multiple aspects of an organism’s form, or their phenome, the sum total of their observable traits.
Recent advances in imaging have made mass 3D scanning of organisms possible, but quantifying and analysing phenomes across diverse clades remained challenging. In this project, we pioneered a new approach for capturing the evolution of 3D shape and reconstructing its evolution through deep time, applying it to the remarkable diversity of tetrapods (amphibians, reptiles, birds, and mammals). Using both empirical results and simulation, we assessed intrinsic and extrinsinc factors shaping vertebrate evolution and also developed and tested novel models of morphological evolution, This project thus combines the deep data from the fossil record with our understanding of genomic and developmental processes into a unified model of phenomic evolution, identifying novel patterns that lay the foundation for targeted developmental analysis and for informing predictions of species response to climate change.
Recent advances in imaging have made mass 3D scanning of organisms possible, but quantifying and analysing phenomes across diverse clades remained challenging. In this project, we pioneered a new approach for capturing the evolution of 3D shape and reconstructing its evolution through deep time, applying it to the remarkable diversity of tetrapods (amphibians, reptiles, birds, and mammals). Using both empirical results and simulation, we assessed intrinsic and extrinsinc factors shaping vertebrate evolution and also developed and tested novel models of morphological evolution, This project thus combines the deep data from the fossil record with our understanding of genomic and developmental processes into a unified model of phenomic evolution, identifying novel patterns that lay the foundation for targeted developmental analysis and for informing predictions of species response to climate change.
The first half of the project was focused on two major objectives: data collection and development and testing of surface morphometric approaches and analysis of modularity. To accomplish the first task, we purchased three portable scanning systems and travelled to over 50 international collections to scan >2500 specimens representing over 1800 species, of which approximately 500 are extinct. During the first three years of this project, we spent extensive time trialing and comparing different approaches to dense morphometric data collection and analysis, ultimately selecting surface semilandmark analysis. Our work included comparisons with standard approaches for morphometric data capture and analysis of modularity, including development of the first likelihood based method for evaluating modularity, and use of morphometric data for estimating divergences, which we published in a series of papers. We also conducted theoretical work, simulating the effect of integration on macroevolutionary patterns, resulting in the development of the Fly-in-the-Tube model of the evolution of integrated phenotypes. While our work relied on already collected material, there are large gaps in the fossil record, so we also conducted fieldwork in poorly studied regions to discover new species and specimens relevant to this work. Our fieldwork during this project focused on the Cretaceous and Paleogene of India and Argentina, as well as the Neogene of Kenya, and resulted in the naming of new vertebrates including dinosaurs.
With the establishment of our data collection and analytical pipeline, we shifted focus to analysis of empirical datasets in the second half of the project, again with each team member focusing on a specific group. To date, this work has benn published over 30 papers and further disseminated through numerous international presentations for scientific and public audiences, through open sharing of our 3D data via Phenome10k.org and via articles in mainstream press and popular science journals, including Scientific American, the Guardian, and BBC. Our published works focus on both the species level and macroevolutionary scale, with papers focusing on every major clade of tetrapods. Our results have produced transformative new understanding of the processes underlying cranial evolution across tetrapods, including identifying a novel model of attenuated evolution, describing a likely common pattern of deep time clade evoution in response to major shifts in ecosystems and climate. Both ecology and life history are primary influences on evolutionary tempo, with nectivorous birds, social mammals, and paedomorphic salamanders show particularly high rates of evolution. Different cranial regions, e.g. feeding structures vs the braincase, also show divergent evolutionary trajectories, epitomising mosaic evolution, which also reflects developmental associations of traits. One of the most surprising results is that there is a clear dichotomy in where variation in the skull is concentrated - in the rostrum of birds and mammals, but in the suspensorium of amphibians and non-avian reptiles. Why this divergent pattern exists is an open question for a future project, but it likely reflects fundamental developmental processes associated with neural crest migration. We have also demonstrated that, in some groups, high integration of traits limits the evolution of structures and that cranial integration is highly conserved within vertebrate classes, but shifts between them, with the biggest differences observed between amphibians and amniotes. The final phase of our project involved unifying all of the datasets into a single cross-tetrapod analysis. This work demonstrates that birds are extremely unusual compared to all other tetrapods, but that this distinctiveness is not associated with a higher rate of evolution, demonstrating the remarkable complexity of evolutionary processes.
With the establishment of our data collection and analytical pipeline, we shifted focus to analysis of empirical datasets in the second half of the project, again with each team member focusing on a specific group. To date, this work has benn published over 30 papers and further disseminated through numerous international presentations for scientific and public audiences, through open sharing of our 3D data via Phenome10k.org and via articles in mainstream press and popular science journals, including Scientific American, the Guardian, and BBC. Our published works focus on both the species level and macroevolutionary scale, with papers focusing on every major clade of tetrapods. Our results have produced transformative new understanding of the processes underlying cranial evolution across tetrapods, including identifying a novel model of attenuated evolution, describing a likely common pattern of deep time clade evoution in response to major shifts in ecosystems and climate. Both ecology and life history are primary influences on evolutionary tempo, with nectivorous birds, social mammals, and paedomorphic salamanders show particularly high rates of evolution. Different cranial regions, e.g. feeding structures vs the braincase, also show divergent evolutionary trajectories, epitomising mosaic evolution, which also reflects developmental associations of traits. One of the most surprising results is that there is a clear dichotomy in where variation in the skull is concentrated - in the rostrum of birds and mammals, but in the suspensorium of amphibians and non-avian reptiles. Why this divergent pattern exists is an open question for a future project, but it likely reflects fundamental developmental processes associated with neural crest migration. We have also demonstrated that, in some groups, high integration of traits limits the evolution of structures and that cranial integration is highly conserved within vertebrate classes, but shifts between them, with the biggest differences observed between amphibians and amniotes. The final phase of our project involved unifying all of the datasets into a single cross-tetrapod analysis. This work demonstrates that birds are extremely unusual compared to all other tetrapods, but that this distinctiveness is not associated with a higher rate of evolution, demonstrating the remarkable complexity of evolutionary processes.
This project has set a new standard for macroevolutionary study and phenomics. We have gathered an unprecedented, rich, comparative dataset on phenotype and developed and refined several new methods for gathering and analysing dense 3D data from 3D images. We have analysed macroevolutionary patterns of morphological evolution and modularity on a far larger scale than previously achieved, hailed as "the vanguard of comparative evolutionary morphology" in a commentary piece. We have used our rich data and understanding of evolutionary history of these groups to reconstruct their evolutionry history and the primary factors influencing it, identifying new models of evolution along the way. We have identified a fundamental divide across vertebrates in where they concentrate changes in their skulls and we have proposed novel hypotheses on how these differences arise during development. In the final phase of the project, we combined our analyses across all of our different clades and conducted the first study of skull morphology across the whole of tetrapods. In the size of our dataset, the density and quality of our phenomic data, and the depth and rigour of our analyses, we have broken new ground for the study of phenomics and the understanding of skull evolution and diversity, with ramifications for understanding how species can, or cannot, respond to changes in their environment.