Inferring the mammal tree: Species-level sets of phylogenies for questions in ecology, evolution, and conservation

Abstract

Big, time-scaled phylogenies are fundamental to connecting evolutionary processes to modern biodiversity patterns. Yet inferring reliable phylogenetic trees for thousands of species involves numerous trade-offs that have limited their utility to comparative biologists. To establish a robust evolutionary timescale for all approximately 6,000 living species of mammals, we developed credible sets of trees that capture root-to-tip uncertainty in topology and divergence times. Our "backbone-and-patch" approach to tree building applies a newly assembled 31-gene supermatrix to two levels of Bayesian inference: (1) backbone relationships and ages among major lineages, using fossil node or tip dating, and (2) species-level "patch" phylogenies with nonoverlapping in-groups that each correspond to one representative lineage in the backbone. Species unsampled for DNA are either excluded ("DNA-only" trees) or imputed within taxonomic constraints using branch lengths drawn from local birth-death models ("completed" trees). Joining time-scaled patches to backbones results in species-level trees of extant Mammalia with all branches estimated under the same modeling framework, thereby facilitating rate comparisons among lineages as disparate as marsupials and placentals. We compare our phylogenetic trees to previous estimates of mammal-wide phylogeny and divergence times, finding that (1) node ages are broadly concordant among studies, and (2) recent (tip-level) rates of speciation are estimated more accurately in our study than in previous "supertree" approaches, in which unresolved nodes led to branch-length artifacts. Credible sets of mammalian phylogenetic history are now available for download at http://vertlife.org/phylosubsets, enabling investigations of long-standing questions in comparative biology.

Fig 1. Species-level relationships and tempo of diversification across mammals.

The node-dated molecular phylogeny of 5,911 extant and recently extinct species shows branches colored with tip-level speciation rates (tip DR metric; interior branches reconstructed using Brownian motion for visual purposes only). Zoom in to the branch tips to see species labels (gray branches of 1,813 species are included via taxonomic constraints rather than DNA). The maximum clade credibility topology of 10,000 trees is shown, and numbered clade labels correspond to orders and subclades listed in the plot periphery: scale in Ma. Dryad data: https://doi.org/10.5061/dryad.tb03d03; phylogeny subsets: http://vertlife.org/phylosubsets. Afro, Afrotheria; Euar, Euarchontoglires; Lago, Lagomorpha; Laur, Laurasiatheria; Ma, millions of years; Mars, Marsupialia; tip DR, tip-level pure-birth diversification rate; X, Xenarthra. Artwork from phylopic.org and open source fonts (see S1 Text, section 9 for detailed credits).

Fig 2. Building the backbone-and-patch Mammalia phylogenies.

(a) Schematic overview of DNA sequence gathering from NCBI, taxonomic matchup, iterative error checking, and estimating a global ML tree from the resulting supermatrix (31 genes by 4,098 species [49]). Patch phylogenies were then delimited, estimated using Bayesian inference [50], and joined to fossil-calibrated backbone trees (node- or tip-dated). The resulting posterior samples of 10,000 fully dated phylogenies either had the global ML tree topology constrained (completed trees of 5,911 species, “TopoCons”) or no topology constraints (DNA-only trees, “TopoFree”). (b, c) Comparison of results from the time-calibrated backbones as pruned to the 28 patch clade representatives. The tip-dated analysis uses fossil taxa as extinct tips in the tree (left side) and then pruned (right side), whereas the node-dated approach uses exponential priors from minimum to soft-max ages. Trees are maximum clade credibility summaries of 10,000 trees. Circles at nodes indicate PP values according to the legend. (d) Topological and age uncertainty in the backbones included the unresolved base of Placentalia, which slightly favors the Atlantogenata hypothesis (blue) versus Exafroplacentalia (red; shown for the node-dated backbone). (e) Bayesian phylogenies of 28 patch clades were separately estimated in relative-time units for rescaling to representative divergence times on the backbone. Combining sets of backbones and patch clades yielded four posterior distributions for analysis. Dryad data: https://doi.org/10.5061/dryad.tb03d03; phylogeny subsets: http://vertlife.org/phylosubsets. Carbonif., Carboniferous; Cisu., Cisuralian; FBD, fossilized birth–death; Guad., Guadalupian; Lopi., Lopingian; Marsup., Marsupialia; mis-ID, misidentification; Miss., Mississippian; ML, maximum-likelihood; Monotr., Monotremata; NCBI, National Center for Biotechnology Information; Nioge., Neogene; PASTIS, Phylogenetic Assembly with Soft Taxonomic Inferences; Penn., Pennsylvanian; PP, posterior probability; RAxML, Randomized Axelerated Maximum Likelihood. Artwork from phylopic.org and open source fonts (see S1 Text, section 9 for detailed credits).

Fig 3. Tempo of mammalian divergences recovered in the two dating analyses of the present study.

Tip-dated (fossilized birth–death) and node-dated (exponential priors) analyses yielded broadly similar results. (a) Among major clades, mean divergence times and 95% highest posterior density intervals are shown for the 28 backbone lineages present in the full trees. (b) Species-specific rates of speciation were compared using the tip DR metric, as calculated upon 10,000 trees as harmonic mean estimates (colored dots by higher taxon) and 95% CIs (Spearman’s r = 0.93 of tip- to node-dated harmonic means). Dryad data: https://doi.org/10.5061/dryad.tb03d03; phylogeny subsets: http://vertlife.org/phylosubsets. CI, confidence interval; tip DR, tip-level pure-birth diversification rate.

Fig 4. Mammalian backbone-level divergence times in our study (node-dated analysis) versus previous studies and the fossil record.

The right-side phylogeny depicts relationships among the 27 extant orders (labeled in capital letters and nested in a hierarchical list), and the dotted line represents the K-Pg extinction event, 66 Ma. Divergence times are colored per study as mean ages and 95% confidence intervals. Fossil-calibrated molecular ages are compared with min and max ages for the oldest crown fossil according to Foley and colleagues [63] and oldest stem fossil according to the Paleobiology Database. Asterisks (*) on taxon names denote three instances of “zombie lineage” disagreement of our study with previous interpretations of the fossil record (see Discussion). Note that extant Microbiotheria and Tubulidentata are monotypic, and so they lack crown ages. Dryad data: https://doi.org/10.5061/dryad.tb03d03; phylogeny subsets: http://vertlife.org/phylosubsets. K-Pg, Cretaceous–Paleogene; Ma, million years ago; max, maximum; min, minimum. Artwork from phylopic.org and open source fonts (see S1 Text, section 9 for detailed credits).

Fig 5. Accumulation of lineages through time for living mammal species as reconstructed in our study versus previous studies.

(a) The shape of Mammalia-wide phylogenies is compared among studies using the natural log of lineage accumulation (see legend colors). Some studies produced one consensus tree (single line), whereas other studies produced sets of 1,000 or 10,000 trees (many lines), in which case 100 trees were randomly sampled. (b) Each of the main species-level Mammalia studies is compared for three major placental orders: Rodentia (purple), Chiroptera (red), and Primates (orange). The degrees of phylogenetic uncertainty present in the tree sets is represented by the width of the lineage accumulation curves. The gray lines in the lower-right-side plot pertain to the MRP supertree with polytomies, whereas the colored lines result from randomly resolving those polytomies into a set of 1,000 trees, of which 100 trees are plotted here. Dryad data: https://doi.org/10.5061/dryad.tb03d03; phylogeny subsets: http://vertlife.org/phylosubsets. Ma, million years ago; MCC, maximum clade credibility; MRP, matrix representation parsimony. Artwork from phylopic.org and open source fonts (see S1 Text, section 9 for detailed credits).

Fig 6. Tip-level speciation rates (tip DR metric) from this study versus previous Mammalia-wide phylogenies.

Comparisons (a) as plotted on trees with relative color scales calibrated per data set so that the top 1% of the tip rate harmonic means correspond to the bright red color of each tree and (b) on a pairwise basis for all species with taxon names matching directly between data sets (n = 4,670, 5,329, and 5,033 species, respectively). Note that the x-axes differ but correspond to the range of tip DR values (95% CI) of each data set. Dryad data: https://doi.org/10.5061/dryad.tb03d03; phylogeny subsets: http://vertlife.org/phylosubsets. CI, confidence interval; tip DR, tip-level pure-birth diversification rate.