Losing history: how extinctions prune features from the tree of life

Abstract

Biodiversity provides many valuable services to humanity; however, rapid expansion of the human population has placed increasing pressure on natural systems, and it has been suggested that we may be entering a sixth mass extinction. There is an urgent need, therefore, to prioritize conservation efforts if we are to maintain the provisioning of such service in the future. Phylogenetic diversity (PD), the summed branch lengths that connect species on the tree-of-life, might provide a valuable metric for conservation prioritization because it has been argued to capture feature diversity. Frequently, PD is estimated in millions of years, and therefore implicitly assumes an evolutionary model in which features diverge gradually over time. Here, I explore the expected loss of feature diversity when this assumption is violated. If evolution tends to slow down over time, as might be the case following adaptive radiations, losses of feature diversity might be relatively small. However, if evolution occurs in rapid bursts, following a punctuated model, impacts of extinctions might be much greater. PD captures many important properties, but if we use it as a proxy for feature diversity, we first need to ensure that we have the correct evolutionary model.

Keywords: ecosystem services; feature diversity; phylogenetic diversity; phylogeny; punctuated evolution.

Figure 1.

Simulated trait evolution under alternative evolutionary models. Illustration of accumulating trait variance assuming a model of phyletic gradualism (Brownian motion) (a) and a speciational model of punctuated evolution (b), in which trait change occurs in rapid bursts at speciation. Evolutionary time is on the x-axis and trait values on the y-axis. Lineages are represented by black lines and speciation events are indicated where a lineage splits in two. At origination, the ancestral lineage is assumed to have a trait value of 0. Lineages tend to diverge over time, following the assumed evolutionary model. However, because trait evolution is non-directional, the expected mean trait value at any point in time is that of the ancestor, but variance increases proportionally with time. Evolutionary convergences are illustrated when lineages cross on the y-axis; this can occur instantaneously at speciation for the model of punctuated evolution. Code for simulations kindly provided by T. Ingram (see also [72]).

Figure 2.

Predicted losses of PD (vertical grey bar) for projected extinctions using IUCN Red List data (categories Critically Endangered (CR), Endangered (EN) and Vulnerable (VU)) under three alternative evolutionary models: phyletic gradualism (a,d,g), evolutionary slowdown with a delta tree transformation [71] of 0.1 (b,e,h) and punctuated evolution (c,f,i), compared to expected losses assuming random extinctions (frequency histograms). Results are shown for Primates (a–c), Artiodactyla (d–f) and Carnivora (g–i).

Figure 3.

Simulated tree topologies (n = 128) assuming a coalescent model (a) following Nee & May [53], a birth–death (b = 1, d = 0.2) model (b) and the delta transformation (δ = 0.1) of the same birth–death tree (c).