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A New Estimate of Afrotherian Phylogeny Based on Simultaneous Analysis of Genomic, Morphological, and Fossil Evidence

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A New Estimate of Afrotherian Phylogeny Based on Simultaneous Analysis of Genomic, Morphological, and Fossil Evidence

Erik R Seiffert. BMC Evol Biol.

Abstract

Background: The placental mammalian clade Afrotheria is now supported by diverse forms of genomic data, but interordinal relationships within, and morphological support for, the group remains elusive. As a means for addressing these outstanding problems, competing hypotheses of afrotherian interordinal relationships were tested through simultaneous parsimony analysis of a large data set (> 4,590 parsimony informative characters) containing genomic data (> 17 kb of nucleotide data, chromosomal associations, and retroposons) and 400 morphological characters scored across 16 extant and 35 extinct afrotherians.

Results: Parsimony analysis of extant taxa alone recovered the interordinal topology (Afrosoricida, ((Macroscelidea, Tubulidentata), (Hyracoidea, (Proboscidea, Sirenia)))). Analysis following addition of extinct taxa instead supported Afroinsectivora (Afrosoricida + Macroscelidea) and Pseudoungulata (Tubulidentata + Paenungulata), as well as Tethytheria (Proboscidea + Sirenia). This latter topology is, however, sensitive to taxon deletion and different placements of the placental root, and numerous alternative interordinal arrangements within Afrotheria could not be statistically rejected. Relationships among extinct stem members of each afrotherian clade were more stable, but one alleged stem macroscelidean (Herodotius) never grouped with that clade and instead consistently joined pseudoungulates or paenungulates. When character transformations were optimized onto a less resolved afrotherian tree that reflects uncertainty about the group's interordinal phylogeny, a total of 21 morphological features were identified as possible synapomorphies of crown Afrotheria, 9 of which optimized unambiguously across all character treatments and optimization methods.

Conclusion: Instability in afrotherian interordinal phylogeny presumably reflects rapid divergences during two pulses of cladogenesis - the first in the Late Cretaceous, at and just after the origin of crown Afrotheria, and the second in the early Cenozoic, with the origin of crown Paenungulata. Morphological evidence for divergences during these two pulses either never existed or has largely been "erased" by subsequent evolution along long ordinal branches. There may, nevertheless, be more morphological character support for crown Afrotheria than is currently assumed; the features identified here as possible afrotherian synapomorphies can be further scrutinized through future phylogenetic analyses with broader taxon sampling, as well as recovery of primitive fossil afrotherians from the Afro-Arabian landmass, where the group is likely to have first diversified.

Figures

Figure 1
Figure 1
Estimate of afrotherian interordinal phylogeny based on data from extant taxa alone. Strict consensus of results from parsimony analyses of extant taxa only with all characters unordered (1 most parsimonious tree (MPT), tree length (TL) = 18428, consistency index (CI) = 0.52, retention index (RI) = 0.39, rescaled consistency index (RCI) = 0.26) and with some multistate characters ordered and scaled (1 MPT, TL = 18068, CI = 0.52, RI = 0.39, RCI = 0.26). Intraordinal relationships are not shown, but in both trees are as in Fig. 2. Numbers above and below branches are bootstrap support values (1000 replicates) from analysis of the matrix with some multistate characters ordered and scaled (above) and with all multistate characters unordered (below).
Figure 2
Figure 2
Phylogenetic relationships of living and extinct afrotherians. Adams consensus tree summarizing results from parsimony analyses with all characters unordered (12 MPTs, TL = 19478, CI = 0.50, RI = 0.44, RCI = 0.28) and with some morphological characters ordered and scaled (1 MPT, TL = 18689.54, CI = 0.50, RI = 0.44, RCI = 0.28). Branches depicted with dashes break down in the strict consensus of all 13 trees. Values above and below branches are bootstrap support (1000 replicates) from analysis of the matrix with some multistate characters ordered and scaled (above) and with all multistate characters unordered (below). Herodotiine taxa (alleged stem macroscelideans) are in bold face; asterisks identify "wild card" taxa whose variable positions given different character treatments lead to decreased resolution in the strict consensus tree.

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