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Ranked Tree Shapes, Non-Random Extinctions and the Loss Of bioRxiv preprint doi: https://doi.org/10.1101/224295; this version posted November 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Version dated: November 23, 2017 2 NON-RANDOM EXTINCTIONS AND PHYLOGENETIC DIVERSITY 3 Ranked tree shapes, non-random extinctions and the loss of 4 phylogenetic diversity 1;2;3;y 1;2;3 1;4 5 Odile Maliet , Fanny Gascuel , and Amaury Lambert 1 6 Center for Interdisciplinary Research in Biology (CIRB), College de France, CNRS, INSERM, 7 PSL Research University, Paris, France; 2 8 Institut de Biologie de l'Ecole´ Normale Sup´erieure (IBENS), Ecole´ Normale Sup´erieure, CNRS, 9 INSERM, PSL Research University, Paris, France; 3 10 Sorbonne Universit´es,UPMC Univ Paris 06, ED 227, Paris, France; 4 11 Sorbonne Universit´es,UPMC Univ Paris 06, CNRS, Laboratoire Probabilit´eset Mod`eles 12 Al´eatoires, Paris, France; y 13 Corresponding author: Odile Maliet, Institut de Biologie de l'Ecole´ Normale Sup´erieure, 14 ´equipe `Mod´elisationde la biodiversit´e', Ecole´ Normale Sup´erieure, 46 rue d'Ulm, 75005 Paris, 15 France; E-mail: [email protected]. 16 Abstract.| 17 Phylogenetic diversity (PD) is a measure of the evolutionary legacy of a group of 18 species, which can be used to define conservation priorities. It has been shown that an 19 important loss of species diversity can sometimes lead to a much less important loss of PD, 20 depending on the topology of the species tree and on the distribution of its branch lengths. bioRxiv preprint doi: https://doi.org/10.1101/224295; this version posted November 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 21 However, the rate of decrease of PD strongly depends on the relative depths of the nodes in 22 the tree and on the order in which species become extinct. We introduce a new, 23 sampling-consistent, three-parameter model generating random trees with covarying 24 topology, clade relative depths and clade relative extinction risks. This model can be seen 25 as an extension to Aldous' one parameter splitting model (β, which controls for tree 26 balance) with two additional parameters: a new parameter α quantifying the correlation 27 between the richness of a clade and its relative depth, and a parameter η quantifying the 28 correlation between the richness of a clade and its frequency (relative abundance or range), 29 taken herein as a proxy for its overall extinction risk. We show on simulated phylogenies 30 that loss of PD depends on the combined effect of all three parameters, β, α and η. In 31 particular, PD may decrease as fast as species diversity when high extinction risks are 32 clustered within small, old clades, corresponding to a parameter range that we term the 33 `thin ice zone' (β < −1 or α < 0; η > 1). Besides, when high extinction risks are clustered 34 within large clades, the loss of PD can be higher in trees that are more balanced (β > 0), 35 in contrast to the predictions of earlier studies based on simpler models. We propose a 36 Monte-Carlo algorithm, tested on simulated data, to infer all three parameters. Applying it 37 to a real dataset comprising 120 bird clades (class Aves) with known range sizes , we show 38 that parameter estimates precisely fall close to close to a 'thin ice zone': the combination of 39 their ranking tree shape and non-random extinctions risks makes them prone to a sudden 40 collapse of PD. 41 (Keywords: Phylogenetic tree, macroevolution, Beta-splitting model, field of bullets model, 42 broken stick, self-similar fragmentation, sampling distribution, rarefaction, biodiversity) bioRxiv preprint doi: https://doi.org/10.1101/224295; this version posted November 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 43 Introduction 44 As it becomes increasingly clear that human activities are causing a major 45 extinction crisis (Leakey and Lewin 1995; Glavin 2007; Wake and Vredenburg 2008; 46 Barnosky et al. 2011), several theoretical studies have aimed at characterizing how the 47 evolutionary legacy of parts of the Tree of Life, and hence also the genetic diversity able to 48 drive future evolution, will decrease in the face of forthcoming extinctions. This 49 evolutionary component of biodiversity can be measured by the phylogenetic diversity 50 (PD), defined as the sum of the branch lengths of the phylogeny spanned by a given set of 51 taxa (Faith 1992). This metric is increasingly being used to measure biodiversity and to 52 identify conservation strategies (Veron et al. 2015). 53 Nee and May (1997) were the first to formally investigate the expected loss of PD in 54 the face of species extinctions, by simulating species trees using the Kingman coalescent. 55 They found that 80% of the phylogenetic diversity can be conserved even when 95% of 56 species are lost. Further studies showed that the loss of PD is in fact much higher when 57 trees are generated through other models of species diversification, such as the Yule or the 58 birth-death models (Mooers et al. 2012; Lambert and Steel 2013). These models indeed 59 generate longer pendant edges (i.e., branches that lead to the tips), hence lower 60 phylogenetic redundancy, than in the standard Kingman coalescent (used by Nee and May 61 1997). However, Nee and May (1997) also showed that phylogenetic diversity is very 62 sensitive to the shape of the species tree (also called its `topology'), with extremely 63 unbalanced trees (`comb trees') losing much more phylogenetic diversity than balanced 64 trees (`bush trees'), due to a lack of phylogenetic redundancy (i.e., the presence of recently 65 diverged sister species). Overall, these results highlighted the sensitivity of the loss of 66 phylogenetic diversity in response to species extinctions to both edge lengths and tree 67 shape. bioRxiv preprint doi: https://doi.org/10.1101/224295; this version posted November 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 68 In this line, we also expect the correlation between the species richness of clades and 69 their relative ages to have a significant impact on the loss of PD (`clade' standing here for 70 any subtree within the full phylogeny). Here the age of a clade, also called `stem age', 71 denotes the depth (measured from the present) of its root node (i.e., the node where this 72 clade is tied to the rest of the tree). Under random extinction, since smaller clades are 73 more likely to become extinct first, the consequence of their total extinction on PD will 74 depend on the lengths of pendant edges in these clades compared to those in larger clades. 75 The effect of such correlation on the loss of PD has not yet been explored, but should be 76 particularly important in unbalanced phylogenetic trees (exhibiting large variation in the 77 species richness of clades), which dominate empirical data (e.g., Guyer and Slowinski 1991; 78 Heard 1992; Guyer and Slowinski 1993; Slowinski and Guyer 1993; Mooers 1995; Purvis 79 1996; Mooers and Heard 1997; Blum and Fran¸cois2006). 80 Besides, the loss of PD was shown to be influenced by the distribution of extinction 81 risks within species trees. Several studies showed that accounting for realistic scenarios of 82 species extinctions (considering that species with higher extinction risk{as per the IUCN 83 Red List status{are more likely to go extinct first) predicts proportionately higher losses in 84 PD than scenarios with random extinction risks (e.g. and review, Purvis et al. 2000a; von 85 Euler 2001; Purvis 2008; Veron et al. 2015). Extinctions may for example be clustered 86 within certain clades (Bennett and Owens 1997; McKinney 1997; Russell et al. 1998; Purvis 87 et al. 2000a; Baillie et al. 2004; Bielby et al. 2006; Fritz and Purvis 2010), correlated to the 88 age of clades (von Euler 2001; Johnson et al. 2002; Redding and Mooers 2006), or to the 89 species richness of clades (Russell et al. 1998; Hughes 1999; Purvis et al. 2000a; Schwartz 90 and Simberloff 2001; von Euler 2001; Johnson et al. 2002; Lozano and Schwartz 2005, 91 assuming in some studies a correlation between rarity and extinction risks). In contrast, 92 theoretical analyses of predictions based on model trees (Nee and May 1997; Mooers et al. 93 2012; Lambert and Steel 2013) have all been based so far on the field of bullets model, bioRxiv preprint doi: https://doi.org/10.1101/224295; this version posted November 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 94 which considers equal extinction probabilities across species (Raup et al.
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