CHAPTER 14 Holocene extinctions and the loss of feature diversity Arne Ø. Mooers, Simon J. Goring, Samuel T. Turvey, and Tyler S. Kuhn mouse 2}, because, on the tree, species {mouse 1} 14.1 Introduction preserves much of the feature diversity represented Species are hard to de/ ne, but under all de/ nitions by {beaver, mouse 2}. We can say that each of {bea- they are unique. Each species can be considered to ver, mouse 1, mouse 2} are redundant with respect possess a set of unique characters which comprise to the features represented by the rodent lineage its feature diversity, the diversity that would be lost that gave rise to them. when that species goes extinct. However, because The mouse/aardvark comparison and Fig. 14.1 species differentiate via evolution from other spe- allow us to consider a set of interesting observa- cies, they also share features as a function of degree tions about how feature diversity is distributed of relationship. So, within placental mammals, all across biodiversity, and what the impacts of his- mice share all the characteristics that allow us to torically and prehistorically recent (i.e. Holocene) call something a mouse, whereas the sole living extinctions have been on this distribution. First, species of aardvark shares very few basic mam- it is now well known that biodiversity is very mal characteristics with anything: it must be true unevenly distributed across the tree of life: the fact that the Earth loses less diversity when any single that at the ordinal level the mammals are approxi- mouse species goes extinct than when the last liv- mately 50% rodents (Rodentia) and 0.02% aard- ing aardvark shuf7 es off its mortal coil. This is one vark (Tubulidentata) is typical (reviewed in Purvis well-established way in which species are not cre- and Hector 2000). The few living monotremes are ated equal (Vane-Wright et al. 1991; Faith 1992). another obvious case within mammals, being only We can start to formalize this simple idea with distantly related to the remaining approximately the help of Fig. 14.1. It depicts the common pattern 5500 known Holocene species. In phylogenetic of a diversifying phylogenetic tree, but also can terms, the tree of life is very imbalanced, because represent the pattern of shared feature diversity, clades differ greatly in the net diversi/ cation with branch lengths representing the number of they have experienced. Interestingly, the simplest unique features that have evolved along that lin- null models of diversi/ cation also lead to imbal- eage. Pruning the tree illustrates how species and ance, although they are usually not as extreme groups of species may differ in the number of as those observed in nature (reviewed in Mooers unique features they have: if we prune distinct- et al. 2007). ive species (such as the aardvark in Fig. 14.1) we The second observation, made most clearly by will lose more of the tree (more unique features) Nee and May (1997), is that, at least under sim- than if we prune less distinctive species (e.g. the ple null models of diversi/ cation, random loss of cat). Likewise, if we prune species {dog, cat}, we species has a mild impact on the total loss of the will lose more of the tree than if we prune {beaver, tree. This is easy to intuit: if loss is random, more 263 114-Turvey-Chap14.indd4-Turvey-Chap14.indd 226363 112/5/20082/5/2008 112:31:032:31:03 PPMM 264 HOLOCENE EXTINCTIONS concentrated within slowly diversifying groups could lead to very large losses. AardvarkBeaver Mouse 1 Mouse 2 Dog Cat The Nee and May (1997) result spurred a ser- ies of empirical investigations into how much of the tree of life would be lost if current extinction risk projections were predictive: von Euler (2001) considered birds of the world, Purvis et al. (2000a) considered both the world’s birds and the world’s carnivores and primates, Sechrest et al. (2002) looked at these latter two groups in the world’s biodiversity hotspots, Johnson et al. (2002) studied marsupials in Australia, Russell et al. (1998) looked at historical and projected extinctions for all mam- mals and birds (using taxonomies), and Mooers and Figure 14.1 Schematic diagram demonstrating clumping of Atkins (2003) considered at-risk birds in Indonesia. extinction on a phylogenetic tree. Branch lengths represent the All these studies agreed that projected losses are number of unique features. The loss of the aardvark would lead to signi/ cantly greater than if extinctions were ran- the greatest loss of feature diversity. If both dog and cat go extinct, their shared feature diversity (dashed branch) would also be lost. dom, because projected losses are clumped and/or Extinction of beaver and mouse 2 would lead to less loss, because concentrated in species-poor groups. In addition, mouse 1 would represent the shared features of the set (dotted von Euler (2001) offered evidence that projected branches). extinctions will make the future bird tree even less balanced than it is today. This means that feature diversity will be even less uniformly distributed species will be chosen from the most speciose parts among living species than at present, increasing of the tree, which are those parts that contain the the distinctiveness of some remaining lineages. most redundancy. From the point of view of con- It might help to contextualize the main observa- serving the products of evolution in the face of cur- tion (non-random loss of feature diversity) by com- rent extinctions, this observation is often cited with parison with past extinctions, and this is the focus of some relief (see e.g. Avise 2005). Importantly, Nee this / nal chapter. For this we must move from time- and May (1997) highlighted that the actual amount based model trees to primarily morphology-based of evolutionary history lost depends strongly on taxonomies, and this presents several interesting the shape of the tree: the more imbalanced the issues. Phylogenetic trees are often depicted with tree, and the shorter the branches near the root, the all the species an equal distance from their com- more that can be lost (Vazquez and Gittleman 1998; mon root, so that we can think of branch lengths Heard and Mooers 2000). Interestingly, Rauch and as equal to time. Elapsed time must be correlated Bar-Yam (2004) applied diversi/ cation models simi- with feature diversity (Crozier 1997). However, we lar to Nee and May’s to make a very different claim: know of no good quantitative test of the strength the distribution of genetic redundancy (for them, of this correlation, partly because the very notion within species) is highly skewed, such that some of feature diversity is vague. Williams and Gaston lineages (individuals) would be genetically much (1994) argue clearly that the correlation may be low, more distinct than others; that is, non-random loss and indeed there is no theoretical reason to expect of these lineages would have a large effect on total that morphological evolution should proceed at genetic diversity. This perspective of non-random a constant rate (this is the reason why molecu- loss is very important, and the question of the fail- lar clocks based on neutral genetic mutations are safe of phylogenetic redundancy becomes largely used instead of cumulative phenotypic character- empirical. Heard and Mooers (2000) documented state changes to estimate phylogenetic divergence that (1) although non-random loss alone may con- dates). So, for example, Amborella trichopoda seems tribute little to loss overall, (2) non-random loss to be the sister group to all other living 7 owering 114-Turvey-Chap14.indd4-Turvey-Chap14.indd 226464 112/5/20082/5/2008 112:31:032:31:03 PPMM THE LOSS OF FEATURE DIVERSITY 265 plants (Mathews and Donoghue 1999). As such it is recently published supertree for all mammals a monotypic lineage on a very long branch of the (Bininda-Emonds et al. 2007), to examine how tree of life. However, it is presented in textbooks as Holocene extinctions were distributed among classically ‘primitive’, representing a suite of ‘basal’ taxa. We begin by examining taxonomies, a classi- characters rather than a suite of novel ones: time / cation system based primarily on morphological seems to have stood still for this particular lineage. differences. Taxonomies may offer a crude com- The tuatara Sphenodon punctatus is another case. pound measure of feature diversity and time, in so Recent genetic studies (Hay et al. 2008) suggest that far as they can often be interpreted as re7 ections although morphologically unchanged since the of underlying phylogeny (especially following the Cretaceous, S. punctatus may in fact possess one of incorporation of cladistic methodology into tax- the fastest rates of molecular evolution for the mito- onomy from the mid twentieth century onwards). chondrial DNA control region ever observed, mak- New taxa are probably more likely to be recognized ing a strong case that although morphologically when groups of individuals or species are pheno- ‘primitive’ it might be inappropriate to label S. punc- typically distinct (Scotland and Sanderson 2003), tatus as primitive in a phylogenetic context. A. tri- and so a taxonomy must contain at least some chopoda and S. punctatus are only two examples of information about how feature diversity is shared many such small-taxon number lineages, and con- among its members. We recognize, however, that siderable quantitative work still needs to be done until we have a better concept of feature diversity, to de/ ne and understand the relationships between this argument is weak (e.g. A. trichopoda had already feature diversity and phylogenetic diversity. been assigned to its own order before phylogenetic Furthermore, it is important to bear in mind work was conducted, and it is ‘different’ because it that there are two different hypotheses to explain is primitive, not because it is derived).