Early History of Mammals Is Elucidated with the ENCODE Multiple Species Sequencing Data

Abstract

Understanding the early evolution of placental mammals is one of the most challenging issues in mammalian phylogeny. Here, we addressed this question by using the sequence data of the ENCODE consortium, which include 1% of mammalian genomes in 18 species belonging to all main mammalian lineages. Phylogenetic reconstructions based on an unprecedented amount of coding sequences taken from 218 genes resulted in a highly supported tree placing the root of Placentalia between Afrotheria and Exafroplacentalia (Afrotheria hypothesis). This topology was validated by the phylogenetic analysis of a new class of genomic phylogenetic markers, the conserved noncoding sequences. Applying the tests of alternative topologies on the coding sequence dataset resulted in the rejection of the Atlantogenata hypothesis (Xenarthra grouping with Afrotheria), while this test rejected the second alternative scenario, the Epitheria hypothesis (Xenarthra at the base), when using the noncoding sequence dataset. Thus, the two datasets support the Afrotheria hypothesis; however, none can reject both of the remaining topological alternatives. Application of molecular phylogenetic methods drastically changed the conception of relationships within mammals. Recent molecular phylogenetic studies have shown that living placental mammals belong to one of the three subgroups: Boreoeutheria, Afrotheria, or Xenarthra, but the relations between these are still unknown. In a previous analysis using 16 genes, Boreoeutheria and Xenarthra grouped together. However, a study based on LINE insertions supported the grouping of Boreoeutheria and Afrotheria. To resolve this discrepancy, we applied sequence data from 1% of a genome in a subset of 18 mammalian species. We used concatenated coding sequence data from 218 genes encompassing 205 kilobases of DNA sequence. Phylogenetic analyses have shown Afrotheria as a basal group of Placentalia with high statistical support. To further validate these results, we analyzed a new phylogenetic marker: conserved noncoding sequence alignments (430 kilobases), which resulted in the same position of the placental root. Topological tests rejected the possibility of Afrotheria-Xenarthra grouping with the coding sequence dataset and Boreoeutheria-Afrotheria grouping with the noncoding sequence dataset. Ascertaining the relationships between mammals is of great importance for the investigation of evolutionary behavior of the different functional genomic elements.