Mammal diversity will take millions of years to recover from the current biodiversity crisis Matt Davisa,b,1, Søren Faurbyc,d, and Jens-Christian Svenninga,b aCenter for Biodiversity Dynamics in a Changing World (BIOCHANGE), Aarhus University, 8000 Aarhus C, Denmark; bSection for Ecoinformatics and Biodiversity, Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark; cDepartment of Biological and Environmental Sciences, University of Gothenburg, SE 405 30 Gothenburg, Sweden; and dGothenburg Global Biodiversity Centre, University of Gothenburg, SE-405 30 Gothenburg, Sweden Edited by Gene Hunt, Smithsonian Institution, Washington, DC, and accepted by Editorial Board Member Douglas Futuyma September 6, 2018 (received for review March 26, 2018) The incipient sixth mass extinction that started in the Late PD can only be restored by time as species evolve and create new Pleistocene has already erased over 300 mammal species and, evolutionary history. For example, although as few as 500 indi- with them, more than 2.5 billion y of unique evolutionary history. viduals of the critically endangered (CR) pygmy sloth (Bradypus At the global scale, this lost phylogenetic diversity (PD) can only be pygmaeus) remain (13), global PD would recover from the ex- restored with time as lineages evolve and create new evolutionary tinction of this species in less than 2 y (11). This is not to say that history. Given the increasing rate of extinctions however, can a new species of pygmy sloth would evolve within this time or mammals evolve fast enough to recover their lost PD on a human that the sloth’s ecological functions would be restored, but that time scale? We use a birth–death tree framework to show that the 8,900-y loss in unique evolutionary history brought about by even if extinction rates slow to preanthropogenic background lev- the sloth’s extinction could be countered simply by all 5,418 els, recovery of lost PD will likely take millions of years. These remaining mammal species existing, and hence evolving, for an findings emphasize the severity of the potential sixth mass extinc- additional 1.64 y. The pygmy sloth, however, is one of the tion and the need to avoid the loss of unique evolutionary youngest mammal species, splitting from its congener during a history now. vicariance event in the Holocene. The extinction of the aardvark (Orycteropus afer) would cause a much larger drop in PD, over 75 phylogenetic diversity | mammals | mass extinction | diversification rate | My, because the aardvark is the sole representative of an entire evolutionary distinctiveness order. Such deep cuts into the mammal tree are increasingly likely, given that over one-fifth of current mammal species are s we enter a potential sixth mass extinction (1), triaging threatened with extinction (14). How much PD will mammals Aspecies and prioritizing limited conservation funds grow lose during the ongoing sixth mass extinction, and can they re- increasingly urgent if we wish to preserve biodiversity (2). cover this lost biodiversity? However, taxonomic species richness (SR), the most used metric for measuring biodiversity among researchers, governments, and Massive Losses of Evolutionary History managers, is insufficient for these purposes because it implicitly We randomly sampled 30 phylogenies from the posterior distri- treats all species equally (3). Functional diversity (FD), a richer bution reported by Faurby (15), which includes all extant and metric that captures species’ ecological adaptations and contri- extinct Late Quaternary mammal species. Combining these trees butions to ecosystem function is growing in popularity, but it is difficult to measure and hard to compare between different Significance taxonomic groups (2–4). Phylogenetic diversity (PD), the amount of independent evolution within a phylogeny (5), is a comple- Biodiversity is more than the number of species on Earth. It is mentary metric that measures lineage history and may be cor- also the amount of unique evolutionary history in the tree of related to functional trait diversity and evolutionary potential (4, life. We find that losses of this phylogenetic diversity (PD) are 6, 7, but cf. ref. 8). PD is generally considered a better metric of disproportionally large in mammals compared with the num- biodiversity than SR because it incorporates both SR and phy- ber of species that have recently gone extinct. This lost PD can logeny, is less influenced by arbitrary taxonomic decisions, and only be restored with time as lineages evolve and create new provides a powerful metaphor of “national heritage” for con- evolutionary history. Without coordinated conservation, it will servationists (5, 9). Furthermore, unlike FD index values, which likely take millions of years for mammals to naturally recover are relative to each idiosyncratic analysis, PD is typically mea- from the biodiversity losses they are predicted to endure over sured in millions of years of independent evolution (the sum of the next 50 y. However, by prioritizing PD in conservation, we all branch lengths connecting a set of species to the root of their could potentially save billions of years of unique evolutionary phylogenetic tree), a meaningful common currency that allows history and the important ecological functions they may comparisons across a wide range of taxa and studies (2, 5). It is represent. difficult to understand and measure the FD contribution of every Author contributions: M.D. and J.-C.S. designed research; M.D. performed research; M.D. species in a community, but with the rapid advancement of en- and S.F. contributed new reagents/analytic tools; M.D., S.F., and J.-C.S. analyzed data; and vironmental DNA methods and computational capabilities, we M.D., S.F., and J.-C.S. wrote the paper. could potentially place all those species on the tree of life to The authors declare no conflict of interest. measure their contribution to PD (6, 10). This article is a PNAS Direct Submission. G.H. is a guest editor invited by the Editorial The incipient sixth mass extinction that started during the Late Board. Pleistocene has been diagnosed by extremely elevated modern Published under the PNAS license. extinction rates compared with background levels (1). However, Data deposition: All data and code for the analysis are archived at Zenodo doi.org/10.5281/ one can also put our current biodiversity crisis in perspective by zenodo.1286876. estimating the time necessary for global diversity to recover to a 1To whom correspondence should be addressed. Email: [email protected]. preanthropogenic state (11). Although regional losses in bio- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. diversity might be lessened by restoration activities such as spe- 1073/pnas.1804906115/-/DCSupplemental. cies reintroductions and rewilding (12), at the global scale, lost Published online October 15, 2018. 11262–11267 | PNAS | October 30, 2018 | vol. 115 | no. 44 www.pnas.org/cgi/doi/10.1073/pnas.1804906115 Downloaded by guest on October 2, 2021 and ranked threat statuses from the International Union for the than expected, given null expectations of random extinctions Conservation of Nature (IUCN), we calculated the loss of PD (Fig. 2 and SI Appendix, Table S1). This is partly because pre- since the Last Interglacial (∼130,000 y ago) and the expected loss historic and historic extinctions were highly size-biased (19), of PD, given probabilities that currently threatened species will devastating large mammals (SI Appendix, Fig. S2), a group go extinct in the near future (16). Unlike most previous studies, shouldering a disproportionate share of PD. Evolutionary history here, we use the Last Interglacial as a baseline instead of the has its own intrinsic value (20), but these lost years also represent present day because it better represents the typical, megafauna- a loss of instrumental value in the extinction of unique functional rich state that existed through much of the Cenozoic (17). traits (2, 10). Human-linked extinctions have already left the Leaving prehistoric extinctions out of analyses undercounts world in an atypical state: depauperate of large animals and the biodiversity loss and ignores the many large impacts these ex- important ecosystem functions and services they provide (17). tinctions have had on modern ecology (17). To put global PD If current lineages simply persisted without any new speciation losses in perspective compared with species losses, we randomly or extinction, it would take nearly 500,000 y for the ∼5,400 shuffled species’ IUCN statuses 250 times so that taxonomic current mammal species to evolve enough new history to restore losses during simulated extinctions were of the same severity but net PD to preanthropogenic levels. But there will be new ex- random with respect to phylogeny (SI Appendix). tinctions. The IUCN’s own definitions for ranks predict the loss Several unique mammal lineages (notably the endemic South of 99.9% of CR species and 67% of endangered species within American orders Litopterna and Notoungulata) were completely the next 100 y (16), eliminating even more ecosystem functions lost during the likely human-linked extinctions of the terminal and services and further increasing mammals’ already large PD Pleistocene and early Holocene (18). These extinctions also debt. At the same time, mammals will also continue to diversify; decimated the sloth and anteater, armadillo, odd-toed ungulate, if every lineage speciated into two distinct lineages, PD could be and elephant lineages, all disproportionately rich in PD (Fig. 1 restored in half the time. The larger the speciation rate (λ)is and SI Appendix, Fig. S1). Human-linked prehistoric extinctions compared with the extinction rate (μ), the shorter the amount of saddled global mammal diversity with a PD loss of 2 billion y of time (t) that it will take for mammals to naturally evolve back unique evolutionary history. Historic extinctions since 1500 CE their lost PD. Given realistic background speciation and extinc- caused an additional 500 My of loss, leaving PD levels far worse tion rates, how long would it take mammals to regain this ECOLOGY A B Expected % contribution to PD is..