The Interrelationships of Placental Mammals and the Limits of Phylogenetic Inference

Abstract

Placental mammals comprise three principal clades: Afrotheria (e.g., elephants and tenrecs), Xenarthra (e.g., armadillos and sloths), and Boreoeutheria (all other placental mammals), the relationships among which are the subject of controversy and a touchstone for debate on the limits of phylogenetic inference. Previous analyses have found support for all three hypotheses, leading some to conclude that this phylogenetic problem might be impossible to resolve due to the compounded effects of incomplete lineage sorting (ILS) and a rapid radiation. Here we show, using a genome scale nucleotide data set, microRNAs, and the reanalysis of the three largest previously published amino acid data sets, that the root of Placentalia lies between Atlantogenata and Boreoeutheria. Although we found evidence for ILS in early placental evolution, we are able to reject previous conclusions that the placental root is a hard polytomy that cannot be resolved. Reanalyses of previous data sets recover Atlantogenata + Boreoeutheria and show that contradictory results are a consequence of poorly fitting evolutionary models; instead, when the evolutionary process is better-modeled, all data sets converge on Atlantogenata. Our Bayesian molecular clock analysis estimates that marsupials diverged from placentals 157-170 Ma, crown Placentalia diverged 86-100 Ma, and crown Atlantogenata diverged 84-97 Ma. Our results are compatible with placental diversification being driven by dispersal rather than vicariance mechanisms, postdating early phases in the protracted opening of the Atlantic Ocean.

Keywords: genome; mammalian; microRNA; palaeontology; phylogeny; placental.

Fig. 1.

The three principal competing hypotheses for the higher-level relationships among placental mammals, with either (a) Afrotheria, (b) Xenarthra, or (c) Atlantogenata being the sister taxon to all other placentals.

Fig. 2.

Results from four of the phylogenetic analyses with each one providing support for Atlantogenata as the sister taxon to all other eutherians. (a) The 21.4 million whole-genome nucleotide alignment analyzed using Phylobayes (CAT–GTR+G), RAxML and ASTRAL with support values for almost all nodes being either 1 or 100. (b) The single concatenated nucleotide alignment for the pre-mir sequences analyzed under GTR+G in Phylobayes. Laurasiatheria is shown collapsed as the interrelationships among the constituent taxa vary between data sets.

Fig. 3

Results from the discordance analysis of the unbinned gene trees with a threshold bootstrap support value of 50% (“left”) and 75% (“right”). These results clearly show that Atlantogenata is the preferred topology, and that much of the incongruence observed across gene trees is due to stochastic errors and not ILS.

Fig. 4.

Results from the molecular clock analysis showing the divergence times for placental lineages with all posterior probabilities shown in “green” and overlaid on the joint prior shown in “red,” with both shaded to show values of highest likelihood (see table 6 for the 95% HPD values). Current biogeographic reconstructions for the breakup of Pangea at 180, 120, and 90 Ma, from “left to right,” respectively, with hotter colors (“red”) indicating faster rates of sea floor formation than colder colors (“blue”) based on Seton et al. (2012) and downloadable from http://www.earthbyte.org/Resources/global_plate_model_ESR12.html. Both the Northern and Southern hemisphere continents have separated by 90 Ma, highlighting the role of dispersal, rather than vicariance, for the biogeographic distribution of crown placentals as the breakup of Pangaea predates current molecular clock estimates for the divergence of crown placentals.