Mammal Extinctions and the Increasing Isolation of Humans on the Tree of Life Sandrine Pavoine, Michael Bonsall, T
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Mammal extinctions and the increasing isolation of humans on the tree of life Sandrine Pavoine, Michael Bonsall, T. Jonathan Davies, Shelly Masi To cite this version: Sandrine Pavoine, Michael Bonsall, T. Jonathan Davies, Shelly Masi. Mammal extinctions and the increasing isolation of humans on the tree of life. Ecology and Evolution, Wiley Open Access, 2019, 9 (3), pp.914-924. 10.1002/ece3.4630. hal-02084469 HAL Id: hal-02084469 https://hal.sorbonne-universite.fr/hal-02084469 Submitted on 29 Mar 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Received: 20 June 2018 | Revised: 23 September 2018 | Accepted: 24 September 2018 DOI: 10.1002/ece3.4630 ORIGINAL RESEARCH Mammal extinctions and the increasing isolation of humans on the tree of life Sandrine Pavoine1 | Michael B. Bonsall2,3 | T. Jonathan Davies4,5,6 | Shelly Masi7 1Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum national Abstract d'Histoire naturelle (MNHN), Centre A sixth great mass extinction is ongoing due to the direct and indirect effects of National de la Recherche Scientifique (CNRS), Sorbonne Université, Paris, France human pressures. However, not all lineages are affected equally. From an anthropo‐ 2Mathematical Ecology Research centric perspective, it is often purported that humans hold a unique place on Earth. Group, Department of Zoology, University Here, we show that our current impacts on the natural world risk realizing that ex‐ of Oxford, Oxford, UK pectation. We simulated species loss on the mammalian phylogenetic tree, informed 3St Peter's College, Oxford, UK 4Department of Biology, McGill University, by species current extinction risks. We explored how Homo sapiens could become Montreal, Quebec, Canada isolated in the tree if species currently threatened with extinction disappeared. We 5 African Centre for DNA analyzed correlates of mammal extinctions risks that may drive this isolation pattern. Barcoding, University of Johannesburg, Johannesburg, South Africa We show that, within mammals, and more particularly within primates, extinction 6Departments of Botany, Forest & risks increase with the number of known threat types, and decrease with geographic Conservation Sciences, Biodiversity range size. Extinctions increase with species body mass, trophic level, and the median Research Centre, University of British Columbia, Vancouver, British Columbia, longitudinal extent of each species range in mammals but not within primates. The Canada risks of extinction are frequently high among H. sapiens close relatives. Pruning 7Unité Eco‐anthropologie et Ethnobiologie (EAE), Muséum National d'Histoire Naturelle threatened primates, including apes (Hominidae, Hylobatidae), from the tree of life (MNHN), Centre National de la Recherche will lead to our species being among those with the fewest close relatives. If no ac‐ Scientifique (CNRS), Université Paris Diderot, Paris, France tion is taken, we will thus not only lose crucial biodiversity for the preservation of Earth ecosystems, but also a key living reference to what makes us human. Correspondence Sandrine Pavoine, Centre d'Ecologie et KEYWORDS des Sciences de la Conservation (CESCO), Muséum national d'Histoire naturelle evolutionary history, extinction risks, phylogenetic originality, primates, threats (MNHN), 61 rue Buffon, 75005 Paris, France. Email: [email protected] 1 | INTRODUCTION with extinction (Hoffmann et al., 2010). Yet, species are not equiva‐ lent, and not all lineages are affected equally. Earth is experiencing a major extinction crisis (Barnosky et al., 2011). For a conservation purpose, assigning species different conser‐ Marine and terrestrial ecosystems are undergoing profound changes vation values might seem controversial. Giving all species, the same as a result of human activities. Indeed, if primary causes for past value equates biodiversity to the number of species (=species rich‐ mass extinction events still remain unclear, the anthropogenic cause ness). However, we can simply reframe this problem by consider‐ of the current biodiversity crisis is widely understood (Novacek & ing other hierarchies of biodiversity. For example, if we value each Cleland, 2001). To evaluate the extent of this crisis, the loss of biodi‐ individual equally, we must value species differently as species are versity is usually estimated in terms of number of species driven ex‐ represented by different numbers of individuals (abundance‐based tinct. Notably, about one‐fifth of vertebrate species are threatened species diversity). Evaluating character states also naturally values This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 914 | www.ecolevol.org Ecology and Evolution. 2019;9:914–924. PAVOINE ET AL. | 915 species differently (character‐based diversity). An extension of this explore a range of potential correlates of extinction risks: species’ reasoning underlies Faith’s (1992a,b) framework of phylogenetic di‐ phylogenetic distance to H. sapiens, their phylogenetic originality, versity, where the “richness” of a species set is calculated by count‐ intrinsic factors linked to species biology, and extrinsic factors linked ing units of branch lengths in a phylogenetic tree, where branch to the threats that species face within their environment (e.g., urban‐ lengths are assumed to capture changes in character states. ization, hunting) and across their species geographic distribution. In Phylogenetic diversity thus provides an alternative but equally our analyses, we ask the following questions: How will extinctions robust measure of biodiversity that encapsulates the shared evolu‐ impact the position of H. sapiens on the mammalian phylogenetic tionary histories of a set of species. The growing use of phylogenies tree? Which factors correlate with species extinction risks? in ecology and conservation biology recognizes that the branching pattern on a phylogenetic tree reflects the accumulation of some 2 | METHODS feature differences (e.g., morphological, behavioral, life history, and/ or ecological differences) between evolutionary lineages (Harvey & 2.1 | Mammalian extinction risk status Pagel, 1991; Tucker et al., 2017). These features are assumed (and sometimes proven to) display what is called a phylogenetic signal: We used the IUCN Red List (IUCN 2016) to classify each mammal spe‐ Related species tend to resemble each other in their features, more cies into one of the following categories: least concern (LC), near threat‐ than they resemble species drawn at random from a phylogenetic ened (NT), vulnerable (VU), endangered (EN), critically endangered tree (e.g., Kamilar & Cooper, 2013). Thus, phylogenetic measures (CR), data deficient (DD). We excluded extinct species and those ex‐ could be more effective than species‐based measures at preserving tinct in the wild. We obtained classifications for 5451 mammal species feature diversity (Faith, 1992a,b). Yet, current conservation prac‐ of which 435 were primates. The IUCN Red List assessments rely on tices may often poorly protect phylogenetic diversity as they target published data and expert inputs and may be subject to bias that might species‐rich areas with high endemism, but ignore species related‐ vary across taxonomic groups (Trull, Böhm, & Carr, 2018); however, the ness (Veron, Davies, Cadotte, Clergeau, & Pavoine, 2017). standardization of the data compiled enhances taxonomic comparisons The extinction risks of mammals have been particularly well (Rodrigues, Pilgrim, Lamoreux, Hoffmann, & Brooks, 2006). studied compared to other groups, especially in a phylogenetic context (Veron et al., 2017). Including more than 5000 species, 2.2 | Taxonomy and phylogeny mammals are charismatic and essential key species for ecosystem functions. About a quarter of mammals are threatened with extinc‐ We used the Wilson and Reeder (2005) taxonomy following the IUCN tion (International Union for Conservation of Nature [IUCN] 2016). Red List (IUCN 2016). For mammals, we used the Bininda‐Emonds Losing even a single mammal species may represent the loss of mil‐ et al. (2007) timetree improved by Fritz et al. (2009), referred to as lions of years of unique evolutionary history. For example, losing the the “Fritz et al. phylogeny” (4854 species had both a IUCN category near threatened Monito del Monte (Dromiciops gliroides, sole extant and a position in this phylogeny). We also considered the phylogenetic member of the Microbiotheria; IUCN, 2016) could represent a loss tree published by Rolland et al. (2014) who resolved the Fritz et al.’s of about 63 MY of evolution (according to Fritz, Bininda‐Emonds, & tree and redated it with dates from Meredith et al. (2011) (same spe‐ Purvis, 2009 and Rolland, Condamine, Jiguet, & Morlon, 2014 phy‐ cies as in Fritz et al. phylogeny). We refer to the resulting timetree as logenetic