Genomics, biogeography, and the diversification of placental mammals

Abstract

Previous molecular analyses of mammalian evolutionary relationships involving a wide range of placental mammalian taxa have been restricted in size from one to two dozen gene loci and have not decisively resolved the basal branching order within Placentalia. Here, on extracting from thousands of gene loci both their coding nucleotide sequences and translated amino acid sequences, we attempt to resolve key uncertainties about the ancient branching pattern of crown placental mammals. Focusing on approximately 1,700 conserved gene loci, those that have the more slowly evolving coding sequences, and using maximum-likelihood, Bayesian inference, maximum parsimony, and neighbor-joining (NJ) phylogenetic tree reconstruction methods, we find from almost all results that a clade (the southern Atlantogenata) composed of Afrotheria and Xenarthra is the sister group of all other (the northern Boreoeutheria) crown placental mammals, among boreoeutherians Rodentia groups with Lagomorpha, and the resultant Glires is close to Primates. Only the NJ tree for nucleotide sequences separates Rodentia (murids) first and then Lagomorpha (rabbit) from the other placental mammals. However, this nucleotide NJ tree still depicts Atlantogenata and Boreoeutheria but minus Rodentia and Lagomorpha. Moreover, the NJ tree for amino acid sequences does depict the basal separation to be between Atlantogenata and a Boreoeutheria that includes Rodentia and Lagomorpha. Crown placental mammalian diversification appears to be largely the result of ancient plate tectonic events that allowed time for convergent phenotypes to evolve in the descendant clades.

Fig. 1.

Alternative hypotheses regarding the branching order among placental mammals. (A) Afrotheria as sister taxon to the other placental mammalian clades. (B) Xenarthra as sister taxon to the other placental mammalian clades. (C) Xenarthra and Afrotheria group together to the exclusion of the other clades. (D) Murid rodents as sister taxon to the other placental mammalian clades; Glires is disrupted by the joining of Lagomorpha to the remaining placental clades.

Fig. 2.

Phylogenetic relationships among major placental groups. Optimal tree topology obtained by MP using first and second codon positions (267,158 steps), PAUP* ML (-ln L = 7,238,023.807), PhyML ML (-ln L = 7,240,210.130) and Bayesian approaches, based on the 1,443,825-bp alignment. PhyML bootstrap supports equal 100% for all nodes. Bayesian posterior probabilities equal 1.0 for all nodes. MP bootstrap supports equal 100% for all nodes with the exception of a 95% value at one node. Branch lengths reflect the likelihood distances calculated by PAUP* Ver. 4.0b10 using the GTR + I + Γ model chosen by ModelTest.

Fig. 3.

NJ analyses of amino acid and nucleotide data sets. Optimal tree topology and branch lengths obtained by NJ analyses of nucleotides (Left) using the maximum composite likelihood distance and amino acid (Right) using the JTT distance. Bootstrap values of all nodes were 100% for 1,000 replicates, except when indicated by * (=97%). An identical tree topology to that shown for amino acids was obtained when only first and second codon positions were used.

Fig. 4.

Plate tectonics explain the diversification of the major placental clades. The most parsimonious reconstruction of placental mammalian diversification, given the phylogenetic findings (i.e., Fig. 2), is depicted. The four major clades of placental mammals are Afrotheria (represented by elephant), Xenarthra (represented by armadillo), Laurasiatheria (represented by cow), and Euarchontoglires (represented by monkey). (A) Eutheria originated on the supercontinent of Pangaea during the Jurassic. At this time, the four placental clades had not diverged from each other. (B) The initial split between placental clades occurred during the Creataceous when Gondwana and the northern continent of Laurasia became widely divided. This separated the southern mammalian clade Atlantogenata (Afrotheria and Xenarthra) from the northern clade Boreoeutheria (Laurasiatheria and Euarchontoglires). (C) In the south, the late Cretaceous separation of Africa and South America is coincident with the divergence of Afrotheria and Xenarthra. The separation of Laurasiatheria and Euarchontoglires also occurred in the north, and diversification among placental mammalian orders was complete by the early Cenozoic. Maps are adapted from ref. .