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Phylogenetic Biodiversity Metrics Should Account for Both Accumulation and Attrition of Evolutionary Heritage

View ORCID ProfileJames Rosindell, Kerry Manson, Rikki Gumbs, William D. Pearse, View ORCID ProfileMike Steel
doi: https://doi.org/10.1101/2022.07.16.499419
James Rosindell
1Department of Life Sciences, Silwood Park Campus, Imperial College London, Buckhurst Road, Ascot, Berkshire, SL5 7PY, United Kingdom
2Biomathematics Research Centre, University of Canterbury, Christchurch, New Zealand
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  • For correspondence: j.rosindell@imperial.ac.uk
Kerry Manson
2Biomathematics Research Centre, University of Canterbury, Christchurch, New Zealand
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Rikki Gumbs
3EDGE of Existence Programme, Zoological Society of London, Regent’s Park, London NW1 4RY, UK
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William D. Pearse
1Department of Life Sciences, Silwood Park Campus, Imperial College London, Buckhurst Road, Ascot, Berkshire, SL5 7PY, United Kingdom
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Mike Steel
2Biomathematics Research Centre, University of Canterbury, Christchurch, New Zealand
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Abstract

Phylogenetic metrics are essential tools used in the study of ecology, evolution and conservation. Phylogenetic diversity (PD) in particular is one of the most prominent measures of biodiversity, and is based on the idea that biological features accumulate along the edges of phylogenetic trees that are summed. We argue that PD and many other phylogenetic biodiversity metrics fail to capture an essential process that we term attrition. Attrition is the gradual loss of features and other sources of variety through causes other than extinction. Here we introduce ‘EvoHeritage’, a generalisation of PD that is founded on the joint processes of accumulation and attrition of features. We argue that whilst PD measures evolutionary history, EvoHeritage is required to capture a more pertinent subset of evolutionary history including only components that have survived attrition. We show that EvoHeritage is not the same as PD on a tree with scaled edges; instead, accumulation and attrition interact in a more complex non-monophyletic way that cannot be captured by edge lengths alone. This leads us to speculate that the one dimensional edge lengths of classic trees may be insufficiently flexible to capture the nuances of evolutionary processes. We derive a measure of EvoHeritage and show that it elegantly reproduces species richness and PD at opposite ends of a continuum based on the intensity of attrition. We demonstrate the utility of EvoHeritage in ecology as a predictor of community productivity compared with species richness and PD. We also show how EvoHeritage can quantify living fossils and resolve their associated controversy. We suggest how the existing calculus of PD-based metrics and other phylogenetic biodiversity metrics can and should be recast in terms of EvoHeritage accumulation and attrition.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Following comments from reviewers and others we have made the following revisions. 1.) simplified the distinction between stochastic and deterministic cases of our EvoHeritage model to illustrate that there is no fundamental difference between them. Relatedly, we have revised the maths to make it clearer how the species richness and phylogenetic diversity ends of the EvoHeritage spectrum represent an emergent finding more than being special cases by design. 2.) revised all the figures for clarity of key concepts, this includes a.) replacing the need for a glossary in the main text (the glossary remains as separate supplementary information), b.) a new figure to explain the living fossils conceptual advance, and workflow for the application to living fossils. c.) a new figure to explain the workflow for the community productivity example 3.) To further simplify the main text we largely remove any mention of phylogenetic networks and focus instead on trees (we retain more on networks in the supplementary material only). We have similarly removed the multiple forms of EvoHeritage from all the formulas as we agree they add little except complexity 4.) We have removed the conservation applications from the revised manuscript. We felt that these applications required a lot more work to be convincing and are thus better suited to a separate manuscript 5.) We have removed the section related to Hill numbers, this was another source of complexity that did not add to the main message of the manuscript or to the applications that remain the focus. 6.) We have strengthened the remaining applications to living fossils and primary productivity - conducting new analyses for both. We have improved clarity of presentation around these applications as well.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted May 23, 2023.
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Phylogenetic Biodiversity Metrics Should Account for Both Accumulation and Attrition of Evolutionary Heritage
James Rosindell, Kerry Manson, Rikki Gumbs, William D. Pearse, Mike Steel
bioRxiv 2022.07.16.499419; doi: https://doi.org/10.1101/2022.07.16.499419
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Phylogenetic Biodiversity Metrics Should Account for Both Accumulation and Attrition of Evolutionary Heritage
James Rosindell, Kerry Manson, Rikki Gumbs, William D. Pearse, Mike Steel
bioRxiv 2022.07.16.499419; doi: https://doi.org/10.1101/2022.07.16.499419

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