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Reconsidering the Loss of Evolutionary History: How Does Non-random Extinction Prune the Tree-of-Life?

Kowiyou Yessoufou and T. Jonathan Davies

Abstract Analysing extinction within a phylogenetic framework may seem counter-intuitive because extinction is a priori a non-heritable trait. However, extinction risk is correlated with other traits, such as body size, that show a strong phylogenetic signal. Further, there has been much effort in identifying key traits important for diversification, and recent evidence has demonstrated that the processes of speciation and extinction may be inextricably linked. A phylogenetic approach also allows us to quantify the impact of extinction, for example, as the loss of branches from the tree-of-life. Early work suggested that extinctions might result in little loss of evolutionary history, but subsequent studies indicated that nonrandom extinctions might prune more of the evolutionary tree. Loss of phylogenetic diversity might have ecosystem consequences because functional differences between species tend to be correlated with the evolutionary distances between them. Here we explore how extinction prunes the tree-of-life. Our review indicates that the loss of evolutionary history under non-random extinction (the emerging pattern in extinction biology) might be less pronounced than some previous studies have suggested. However, the loss of functional diversity might still be large, depending on the evolutionary model of trait change. Under a punctuated model of evolution, in which trait differences accrue in bursts at speciation, the number of branches lost is more important than their summed lengths. We suggest that evolutionary models need to be incorporated more explicitly into measures of phylogenetic diversity if we are to use phylogeny as a proxy for functional diversity.

Keywords Extinction risk • Phylogenetic comparative methods • Punctuated evolution • Phylogenetic diversity • Feature diversity

Introduction

There is mounting evidence that we are entering a sixth mass extinction (Millennium Ecosystem Assessment 2005), and the future of biodiversity is at risk due to the high rates at which biological diversity – species, habitats, evolutionary diversity – is being eroded. Species are experiencing unprecedented pressures across their ranges owing to global change, including increased invasion success of aliens (Winter et al. 2009), habitat destruction (Vitousek et al. 1997; Haberl et al. 2007), climate change and climate variability (Willis et al. 2008, 2010). Consequently, approximately 30 % of assessed species are currently categorised as threatened by the IUCN, and a greater proportion may be committed to extinction in the near future (Thomas et al. 2004). Current rates of species loss might be 1,000–10,000 times greater than past extinction rates (Pimm et al. 1995; Millennium Ecosystem Assessment 2005) with particularly elevated rates in tropical biomes (Vamosi and Vamosi 2008), known for their unique life-form diversity. At the ecosystem level, with the loss of species, we also lose their contributions to overall ecosystem functioning and services. The loss of ecosystem services is of particular concern because human survival relies strongly on key services such as food production, plant pollination, medicinal plants, clean water, clean air, nutrient cycling, carbon sequestration, climate stability, recreation, tourism, etc. – which are provided by a well functioning system of biological diversity.

It is well established that human activities can drive extinctions within a short period of time (Baillie et al. 2004; Mace et al. 2005a). Because human population has increased exponentially over the last centuries, and is expected to reach nine billion by 2050 (un.org/esa/population/publications/longrange2/2004worldpo p2300reportfinalc.pdf), pressure on natural ecosystems is also predicted to increase, yet at the same time there will be an even greater demand for the ecosystem services provided by biologically diverse natural systems. As a result, the rate of species extinction is projected to rise by at least a further order of magnitude over the next few hundred years (Mace et al. 2005b), potentially decreasing the provisioning of ecosystem services at a time when demand is growing. Understanding how the ongoing extinction crisis will impact the provisioning of critical ecosystem services is therefore a matter of urgency.

Quantifying the ecosystem contributions of individual species is a major challenge. Current estimates of global diversity vary by over an order of magnitude (see e.g. May 2010), with the vast majority of species (86 % and 91 % of terrestrial and oceanic diversity, respectively) remaining unknown to science (Mora et al. 2011). An in-depth understanding of species ecologies is therefore impractical for most of life; at best, we might be able to infer their placement on the tree-of-life. Whilst there is now a general consensus on the positive link between biodiversity and ecosystem function (Hooper et al. 2012), there has been growing evidence suggesting that evolutionary history provides a more informative measure of biological diversity than traditional metrics based upon richness and abundance (e.g. Faith 1992; Faith et al. 2010; Davies and Cadotte 2011; see also Srivastava et al. 2012 for a comprehensive review). It is suggested that evolutionary history might better capture functional diversity including unmeasured or hard-to-measure traits (Crozier 1997; Faith 2002). As such, phylogeny provides a unique framework that captures both known (Forest et al. 2007; Saslis-Lagoudakis et al. 2011) and unknown ecosystem services (Faith et al. 2010). Understanding how the current extinction crisis will prune the tree-of-life is therefore critical for ensuring a continued provisioning of the ecosystem services upon which we rely, but for which we might lack detailed ecological knowledge of underlying process or mechanism (Faith et al. 2010).

There has been growing effort to incorporate species evolutionary histories into conservation decision-making (e.g. Purvis et al. 2000a, 2005; Isaac et al. 2007, 2012; Faith 2008). This effort has been facilitated by the rapid rise in analytical tools, and the availability of large comprehensive phylogenetic trees for well studied taxonomic groups such as mammals (Bininda-Edmonds et al. 2007), birds (McCormack et al. 2013), amphibians (Pyron and Wiens 2013), and flowering plants (e.g. Davies et al. 2004). Here, we review recent insights from phylogenetic studies of extinction risk, and re-examine how extinctions impact the tree-of-life.

 
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