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, 17 (4), 413-21

Using Genomic Data to Unravel the Root of the Placental Mammal Phylogeny

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Using Genomic Data to Unravel the Root of the Placental Mammal Phylogeny

William J Murphy et al. Genome Res.

Abstract

The phylogeny of placental mammals is a critical framework for choosing future genome sequencing targets and for resolving the ancestral mammalian genome at the nucleotide level. Despite considerable recent progress defining superordinal relationships, several branches remain poorly resolved, including the root of the placental tree. Here we analyzed the genome sequence assemblies of human, armadillo, elephant, and opossum to identify informative coding indels that would serve as rare genomic changes to infer early events in placental mammal phylogeny. We also expanded our species sampling by including sequence data from >30 ongoing genome projects, followed by PCR and sequencing validation of each indel in additional taxa. Our data provide support for a sister-group relationship between Afrotheria and Xenarthra (the Atlantogenata hypothesis), which is in turn the sister-taxon to Boreoeutheria. We failed to recover any indels in support of a basal position for Xenarthra (Epitheria), which is suggested by morphology and a recent retroposon analysis, or a hypothesis with Afrotheria basal (Exafricoplacentalia), which is favored by phylogenetic analysis of large nuclear gene data sets. In addition, we identified two retroposon insertions that also support Atlantogenata and none for the alternative hypotheses. A revised molecular timescale based on these phylogenetic inferences suggests Afrotheria and Xenarthra diverged from other placental mammals approximately 103 (95-114) million years ago. We discuss the impacts of this topology on earlier phylogenetic reconstructions and repeat-based inferences of phylogeny.

Figures

Figure 1.
Figure 1.
Three hypotheses for the basal relationships among placental mammal superordinal clades. The name for each hypothesis refers to the ingroup taxa.
Figure 2.
Figure 2.
Alignment of PTPRB exon 9 sequences from 49 vertebrate species. A single amino acid deletion shared by all xenarthrans and afrotherians is highlighted with a box. Full-length amino acid sequences are derived from draft genome sequences or traces. Sequences with truncated ends were generated by PCR using conserved primers in the exon flanking the indel. Asterisks indicate gaps in the sequence assemblies or traces.
Figure 3.
Figure 3.
Alignment of ZNF367 exon 5 sequences from 46 mammals. A single amino acid insertion shared by all xenarthrans and afrotherians is highlighted with a box. Full-length amino acid sequences are derived from full genome sequences or traces. Sequences with truncated ends were generated by PCR using conserved primers in the exon flanking the indel.
Figure 4.
Figure 4.
Alignment of C14orf121 exon 35 sequences from 34 mammals (upper panel), and LAMC2 exon 13 sequences from 28 mammals (lower panel). The indels shared by xenarthrans and afrotherians are highlighted with boxes. Full-length amino acid sequences are derived from draft genome sequences or traces. Sequences with truncated ends were generated by PCR using conserved primers in the exon flanking the indel.
Figure 5.
Figure 5.
(A) L1MB5 insertion in an intron of the OTC gene. The upper gel image shows PCR products obtained by amplifying different mammalian genomic DNAs with conserved primers flanking the retroposon insertion site. Below is a partial alignment of the exonic (underlined)/intronic sequences flanking the L1MB5 insertion from 26 placental mammals. The central portion of the inserted sequence has been edited, as shown by the double slash marks. (B) A multispecies alignment showing the second L1MB5 insertion in an intron of the RABGAP1L gene from 23 placental mammals. Direct repeats are highlighted in gray.
Figure 6.
Figure 6.
A molecular timescale for placental mammals based on the data set from Roca et al. (2004), 13 fossil constraints (Springer et al. 2003), and a mean prior of 105 Mya for the placental root. Divergence estimates are shown for several key superordinal clades (for a full list of divergence times and confidence intervals, see Supplemental Table 2).

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