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

Abstract

AbstractPhylogenetic metrics are essential tools in 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 branches of phylogenetic trees. 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 through causes other than extinction, for example through natural selection. We introduce ‘EvoHeritage’, a generalisation of PD that is founded on the joint processes of accumulation and attrition of features, and can be applied to phylogenetic trees or more complex networks. Whilst PD measures evolutionary history, EvoHeritage is required to capture a more pertinent subset of evolutionary history including only features that have survived attrition. We show that EvoHeritage is not the same as PD on a tree with scaled branches; instead, accumulation and attrition interact in a more complex non-monphyletic way that cannot be captured by branch lengths alone. This leads us to speculate that existing phylogenetic trees and networks may be insufficiently flexible objects to capture the nuances of evolutionary processes. We derive a dimensionless measure of EvoHeritage that reproduces species richness and PD at opposite ends of a continuum based on the intensity of attrition. We suggest how the existing calculus of PD-based metrics and other phylogenetic biodiversity metrics could be recast in terms of EvoHeritage accumulation and attrition. We give three empirical applications that all rely on our new approach. The first is in ecology, evaluating EvoHeritage as a predictor of community productivity against species richness and PD. The second is in evolution, quantifying living fossils and resolving their associated controversy. The third is in conservation, using a partitioning of EvoHeritage to re-balance priorities at the broad scale of the complete tree of life.