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Innovation and opportunity in the evolution of life

Periodic Reporting for period 4 - INNOVATION (Innovation and opportunity in the evolution of life)

Berichtszeitraum: 2023-04-01 bis 2024-09-30

The project addresses key aspects of macroevolution, the large-scale evolution of life as measured on geological time scales of millions of years. These key questions explore how morphology, the external appearance of organisms, evolves and why some groups such as birds become so successful, when their closest relatives, crocodiles, did not? Further, to what extent do successful groups like birds owe their success to remarkable innovations (flight, feathers) or to changing environmental circumstances, including external crises?

We explore these questions using the fossil record of tetrapods, the amphibians, reptiles, birds and mammals. There are 30,000 living species of tetrapods, and they have a rich fossil record spanning some 400 million years. Further, the phylogenetic tree of living and fossil tetrapods is relatively well understood, and with dates from key fossils, we can draw a reasonably reliable time tree. This is a phylogenetic tree, showing the relationships of species, but with key branching points reasonably reliably dated. Methods now exist to analyse patterns and rates of evolution across such time trees, with proper expression of multiple uncertainties (relationships, dating, incompleteness of the fossil record). Knowing when rates of evolution accelerated points to times of expansion that can be matched to external environmental events or the emergence of particular functional novelties.

The first aim of the ‘Innovation’ project was to produce a complete phylogenetic tree of tetrapods (30,000 living species; 10,000 extinct species) and use this to explore a core question in macroevolution: are three outputs: (1) the complete evolutionary tree of tetrapods; (2) a table of morphological characters across all tetrapod groups; and (3) many case studies of macroevolution among tetrapods (e.g. amphibians, early reptiles, dinosaurs, birds, mammals) in leading scientific journals. In sum, these will provide the largest-ever geologically dated morphological evolutionary tree and character set, so enabling a thorough exploration of key evolutionary drivers and models across a single important clade.
We highlight five major themes of the ‘Innovation’ project.

(1) We defined a new concept, the ‘Angiosperm terrestrial revolution’, encompassing key steps in the evolution of life on land in the mid Cretaceous and Paleogene. The establishment of flowering plants (angiosperms) in the Cretaceous and the explosion of tropical rain forests in the Paleogene revolutionised terrestrial ecosystems, triggering explosive evolution of insects, spiders, lizards, birds, and mammals.

(2) We also highlighted the huge importance of the Triassic as a key time in the evolution of life, terming this the ‘Triassic Revolution.’ On land, ongoing competition between synapsids and archosauromorphs through the Triassic was marked by a posture shift from sprawling to erect, and a shift in physiology to warm-bloodedness, with insulating skin coverings of hair and feathers.

(3) The launch of AVONET in 2022 was a contribution to open access data sharing, providing a resource on bird evolution, ecology, and behaviour. ‘Innovation’ PDRA Catherine Sheard led this and used data she had gathered for her studies under the grant, but also assembling data from many others. The database lists all 11,009 living bird species, with information on key ecological and morphological features. The launch paper has been cited >1000 times, showing the impact of the project.

(4) One of our early studies showed that feathers, long been regarded as the innovation that drove the success of birds, originated much earlier, some 100 million years before the origin of birds. Hair and feathers likely evolved in the Early Triassic ancestors of mammals and birds, at a time when synapsids and archosaurs show independent evidence of higher metabolic rates (erect gait and endothermy), as part of a major resetting of terrestrial ecosystems following the devastating end-Permian mass extinction.

(5) We also made several macroevolutionary studies of squamates (lizards, snakes and relatives) through time. We confirmed that the major expansion of dietary functional morphology happened in the mid-Cretaceous. Until that time, squamates had relatively uniform tooth types, which then diversified substantially and ecomorphospace expanded to modern levels. Our continuing work on squamate phylogeny included a further publication, in Nature in 2025, where we presented Agriodontosaurus, the world’s oldest squamate, which leads to substantial re-dating of the whole evolutionary tree of early lizards and their relatives.
Our work has shown how combined methods from palaeontology, genomics, phylogenetics, and functional biology can allow novel approaches in understanding key events in the evolution of life, but also some fundamental aspects of evolution such as the relative importance of innovation (= the emergence of new anatomical and physiological solutions to evolutionary pressures) and environmental change in driving the big patterns of evolution. Life has gone through major phases in its long history, and certain groups of plants and animals have had times of great success and times of less significance; these patterns of rise and fall have causes, and we have shown some of the ways to tackle these large questions.

We are fortunate that tetrapods, including dinosaurs, have great public appeal, as do mass extinctions and other ‘events’ of the past history of the Earth. Therefore, many of our discoveries have been widely appealing, and they lead our audiences, including school children, to ask questions like: ’how do you know that?’ Even the methodological improvements have been appealing, allowing us to address basic questions about how we know the ages of particular fossils, or how we know birds evolved from among dinosaurs, or even that a particular group of dinosaurs or other extinct forms owed their success to efficient shearing dentition, or a change in vegetation, or an improvement in flight efficiency, makes people re-evaluate what can be known and tested, or not known.

These studies have improved interdisciplinarity among researchers. At one point, palaeontologists would rarely address large-scale evolutionary questions with rigorously analysed data, and it was rare for genomic experts to engage with palaeontologists. Now, there is a common language in discussion and in methods, including the ecological and morphological data, the phylogenetic trees, and the modes of analysis.

We have contributed to the free exchange of data and methods by engaging with open access data bases such as AVONET and providing work packages of code within the framework of the R programming language.
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