A genomic timescale for placental mammal evolution

Abstract

The precise pattern and timing of speciation events that gave rise to all living placental mammals remain controversial. We provide a comprehensive phylogenetic analysis of genetic variation across an alignment of 241 placental mammal genome assemblies, addressing prior concerns regarding limited genomic sampling across species. We compared neutral genome-wide phylogenomic signals using concatenation and coalescent-based approaches, interrogated phylogenetic variation across chromosomes, and analyzed extensive catalogs of structural variants. Interordinal relationships exhibit relatively low rates of phylogenomic conflict across diverse datasets and analytical methods. Conversely, X-chromosome versus autosome conflicts characterize multiple independent clades that radiated during the Cenozoic. Genomic time trees reveal an accumulation of cladogenic events before and immediately after the Cretaceous-Paleogene (K-Pg) boundary, implying important roles for Cretaceous continental vicariance and the K-Pg extinction in the placental radiation.

Fig. 1.. Placental mammal phylogeny based on coalescent analysis of nearly neutral sites.

(A) Fifty-percent Majority-rule consensus tree from a SVDquartets analysis of 411,110 genome-wide, nearly neutral sites from the human-referenced alignment of 241 species. Bootstrap support is 100% for all nodes. Superordinal clades are labeled and identified in four colors. Nodes corresponding to Boreoeutheria and Atlantogenata are indicated with black circles. (B) The frequency at which eight superordinal clades [numbered 1 to 8 in (A)] were recovered as monophyletic in 2164 window-based maximum likelihood trees from representative autosomes (Chr1, Chr21 and Chr22) and ChrX. Dotted lines indicate relationships that differ from the concatenated maximum likelihood analysis.

Fig. 2.. Contrasting patterns of phylogenomic discordance.

(A) Distribution of phylogenomic signal from select clades (table S5), visualized by using TreeHouseExplorer (23) in 100-kb alignment windows along human Chr1, Chr21, Chr22, and ChrX. Vertical bars along each chromosome are color-coded to indicate the distribution of the topology—t1, blue; t2, red; or t3, green, corresponding to topologies shown at left—that was recovered in the locus window. Black ovals indicate approximate positions of centromeres, and white boxes indicate heterochromatic regions. (B) Frequency of each topology on the representative autosomes, ChrX, and the low-recombining region of the X (4). (C) Relative topology frequencies in regions of high GC content (>55%) and low GC content (<35%). There are topological differences between ChrX and the autosomes, and corresponding GC content changes, for the primary intraordinal rodent clades, arctoid carnivorans, and cricetid rodents. Support for Zooamata was obtained by summing support for this clade across all three topologies at top. An alternately colored version of this figure is also available (fig. S8).

Fig. 3.. Rare genomic changes.

(A) Number of deletions recovered in the HRA, RRA, in both the HRA and RRA, and on the HRA ChrX in support of all potential laurasiatherian hypotheses. Within Euarchontoglires, hundreds of raw deletions were recovered for Euarchonta, a subset of which were further validated (table S7). Glires + Primatomorpha and Glires + Scandentia were unsupported by the deletion analysis. (B) The topology inferred from the Kuritzin-Kischka-Schmitz-Churakov (KKSC) analysis (50) of deletions for Cetartiodactyla, Perissodactyla, and Ferae (Carnivora + Pholidota) from the HRA, RRA, and HRA/RRA overlap datasets. In all cases, the corresponding KKSC bifurcation test was significant, indicating that a polytomy at this node was rejected. This topology was also recovered in an ASTRAL-BP analysis of the overlapping set of deletions (fig. S9). Bootstrap support values are shown for 500 replicates. (C) High-confidence chromosome breakpoints supporting the monophyly of select superordinal clades. No conflicting breakpoints were found for these nodes.

Fig. 4.. Genomic timescale for placental mammal diversification.

Divergence times estimated with 37 fossil calibrations for interordinal and intraordinal diversification events in mammals. (A) A representative topology from ChrX showing divergence times and CIs for 65 species, estimated by using the Benton2009 root constraint and the independent rate model (IRM) clock model. (B) Genomic estimates for major placental mammal clades based on 316 100-kb windows by using the Benton2009 + IRM analysis, distributed across Chr1, Chr21, Chr22, and ChrX. The box plots summarize the mean and variation around the mean. The corresponding upper 95% CI and lower 95% CI are displayed as blue and orange circles, respectively, for each of the 316 estimates. The related minimum, maximum, mean, and median 95% CIs are listed in table S10. (C) Paleomaps (38) illustrate the extent of continental fragmentation and sea level rise at a series of time points during the Cretaceous.

Fig. 5.. Divergence time sensitivity analyses.

For analyses in which 316 trees were used, point divergence time estimates for all 316 time trees are displayed. The overlaid box plots show the mean of 316 point estimates. The corresponding minimum, maximum, mean, and median 95% CIs are listed in table S10. (A) Variation in node ages when the root constraint, stratigraphic bounds (correcting for body size), and missingness are varied. (B) Comparison of point estimates when the tree is fully calibrated by using a combination of “cladistic” (fossils assigned to a node based on a formal cladistic analysis) and “opinion” fossil constraints relative to point estimates calibrated only with cladistic fossils (table S9). (Bottom) Comparison of divergence time estimates using the IRM) or autocorrelated rate model (ARM). The effective joint prior (No DNA) is compared with divergence times estimated when only the root of Placentalia is calibrated by using the Benton 2009 soft bound upper constraint. (C) Comparison of point estimates and 95% CIs for single-tree datasets in which selective pressure, genome alignment reference species, and the number of species are varied (table S10). (D) The inferred ages of select interordinal (x axis, blue dots) and intraordinal divergences (x axis, yellow dots) across the range of sensitivity analyses are listed in table S10.