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375 Million Years of the Diversification of Life on Land: Shifting the Paradigm?

Periodic Reporting for period 4 - TERRA (375 Million Years of the Diversification of Life on Land: Shifting the Paradigm?)

Reporting period: 2020-01-01 to 2020-06-30

Life on land today is spectacularly diverse, representing 75–95% of all species on Earth. However, it has been unclear how this extraordinary diversity has been acquired across deep geological time. Is diversity on land today truly much higher than at any point in the geological past? This research project addressed this major knowledge gap by reassessing the dominant paradigm of terrestrial diversification, an exponential increase in diversity over the last 375 million years, primarily using the rich and well-studied fossil record of tetrapods (four-limbed vertebrates) as an exemplar group. Previous analyses of tetrapod diversification were based on outdated datasets and methods that were likely to artificially inflate apparent diversity towards the present day, and did not take into account variation in the sampling of the tetrapod fossil record through time. In this project we compiled major new datasets on the spatial and temporal distribution of terrestrial tetrapods across their entire fossil record, and quantified spatial and temporal variation in fossil sampling and completeness. We developed innovative new statistical approaches to account for major fossil record biases when estimating diversity - in particular major but previously largely overlooked variation in how fossils have been sampled spatially. These approaches were used to reassess the long term patterns of local and regional scale tetrapod diversity through time, as well as around key mass extinction events, and to reassess patterns of marine animal diversity over similar timescales. Our results have helped to overturn the dominant paradigm of terrestrial diversification: rather than sustained, exponential diversification we find overwhelming evidence for constraints on diversity over tens to hundreds of millions of years, punctuated by severe ecological disruptions such as the Cretaceous-Paleogene mass extinction. We recover similar patterns for marine animals, suggesting common mechanisms in marine and terrestrial ecosystems. Our results also demonstrate the role played by environmental change (e.g. climate change, sea level) in driving diversification patterns both on land and in the sea.
The project has achieved all major goals and answered key research questions. Project dissemination has mainly taken place through publication (21 publications to date; one manuscript in press; one in review; eight further manuscripts in advanced stages of preparation) and presentations at international conferences. The key results are:

- Contribution of a significant volume of new data, and improvement of existing data, on the stratigraphic and geographic distribution and taxonomy of terrestrial tetrapods within the Paleobiology Database.

- Compilation and analysis of datasets on fossil record completeness through time for major vertebrate groups. Data were collected for 12 major tetrapod groups. Analyses have demonstrated different patterns of fossil record completeness between marine and terrestrial realms, between different body size and taphonomic classes, and across major extinction events (e.g. Brown et al. 2019, Palaeontology; Cashmore et al. 2019, 2020, Palaeontology). We generated new methods for assessing taxonomic 'diagnosability' of preserved fossil remains - i.e. how useful taxonomic and phylogenetic information is distributed through the vertebrate skeleton (Cashmore 2019, PhD thesis).

- Development of improved methods for estimating diversity change in deep time. Our results clearly demonstrate that diversity estimators that interpolate based on coverage of the underlying species-abundance distribution are the best methods available for estimating relative changes in diversity through time (Close et al. 2018, Methods in Ecology & Evolution). Based on these insights, we developed a new approach that allows fossil diversity to be estimated while holding the geographic spread of sampled localities constant (Close et al. 2017, Nature Communications; Close et al. 2020, Proceedings of the Royal Society B; Close et al. 2020, Science).

- Analyses of local and regional scale richness of tetrapod communities do not support the paradigm of exponential or unconstrained diversification on land (Close et al. 2017, Nature Communications; Close et al. 2019, Nature Ecology & Evolution; Close et al. 2020, Proceedings of the Royal Society B). Instead, diversity appears to be strongly constrained, implying biotic controls such as competition for resources are important in limiting diversification. Similar results for the marine realm are obtained when classic data for marine animals are re-analysed (Close et al. 2020, Science), suggesting similar processes operating on land and in the sea. The Cretaceous-Paleogene mass extinction played a dramatic role in structuring the evolution of diversity, with diversity on land and in the sea reaching a new higher equilibrium in the aftermath of the extinction. This suggests that mass extinctions play a key role in restructuring ecosystems and resetting limits to diversification (Close et al. 2019, Nature Ecology & Evolution; Close et al. 2020, Proceedings of the Royal Society B; Close et al. 2020, Science).

- Results suggest large-scale environmental changes play an important role in driving long-term patterns of diversity change for individual groups. For example, the 'Carboniferous Rainforest Collapse', driven by climate changes, appears to have led to reduced diversity but more cosmopolitan faunas in its aftermath (Dunne et al. 2018, Proceedings of the Royal Society B). Climate change was also a key driver of the evolution of pseudosuchian archosaurs (Mannion et al. 2015, Nature Communications) and early dinosaurs (Dunne 2019, PhD thesis; Dunne et al. in press).

- The large increase in terrestrial tetrapod diversity following the Cretaceous-Paleogene mass extinction results from the diversification of mammals (Close et al. 2019, Nature Ecology & Evolution; Close et al. 2020, Proceedings of the Royal Society B). Critically, however, diversity increased across all body size classes, suggesting an ability of eutherian mammals to more finely partition ecological space than their Mesozoic predecessors (Benevento et al. in review).
The project results have significantly advanced the field beyond the state of the art. Our work overturns hypotheses of unconstrained, exponential diversification of terrestrial biodiversity through geological time, suggesting instead that ecosystem diversity may have been constrained at regional level over long geological periods, and then fundamentally restructured by major extinction events, and suggests that this pattern is shared between marine and terrestrial realms. These results have significant implications for understanding major macroevolutionary and macroecological patterns today and in the past. We have developed innovative new methods that refine our ability to reliably test changes in diversity in the fossil record. These methods are broadly applicable and can be extended to address a broad series of questions about the spatial and temporal framework of diversity.
Changes in local richness of land tetrapods across the Phanerozoic (from Close et al. 2019)