Evolutionary Models for the Diversification of Placental Mammals Across the KPg Boundary

Abstract

Deciphering the timing of the placental mammal radiation is a longstanding problem in evolutionary biology, but consensus on the tempo and mode of placental diversification remains elusive. Nevertheless, an accurate timetree is essential for understanding the role of important events in Earth history (e.g., Cretaceous Terrestrial Revolution, KPg mass extinction) in promoting the taxonomic and ecomorphological diversification of Placentalia. Archibald and Deutschman described three competing models for the diversification of placental mammals, which are the Explosive, Long Fuse, and Short Fuse Models. More recently, the Soft Explosive Model and Trans-KPg Model have emerged as additional hypotheses for the placental radiation. Here, we review molecular and paleontological evidence for each of these five models including the identification of general problems that can negatively impact divergence time estimates. The Long Fuse Model has received more support from relaxed clock studies than any of the other models, but this model is not supported by morphological cladistic studies that position Cretaceous eutherians outside of crown Placentalia. At the same time, morphological cladistics has a poor track record of reconstructing higher-level relationships among the orders of placental mammals including the results of new pseudoextinction analyses that we performed on the largest available morphological data set for mammals (4,541 characters). We also examine the strengths and weaknesses of different timetree methods (node dating, tip dating, and fossilized birth-death dating) that may now be applied to estimate the timing of the placental radiation. While new methods such as tip dating are promising, they also have problems that must be addressed if these methods are to effectively discriminate among competing hypotheses for placental diversification. Finally, we discuss the complexities of timetree estimation when the signal of speciation times is impacted by incomplete lineage sorting (ILS) and hybridization. Not accounting for ILS results in dates that are older than speciation events. Hybridization, in turn, can result in dates than are younger or older than speciation dates. Disregarding this potential variation in "gene" history across the genome can distort phylogenetic branch lengths and divergence estimates when multiple unlinked genomic loci are combined together in a timetree analysis.

Keywords: KPg boundary; placental radiation; relaxed clocks; timetrees; tip dating.

Figure 1

Graphical summary of the five competing models of diversification for placental mammals. Approximate dates that were used to illustrate each model are derived from representative studies as indicated in the figure. (A) Explosive Model. (B) Soft Explosive Model. (C) Trans-KPg Model. (D) Long Fuse Model. (E) Short Fuse Model. For the Short Fuse Model, some molecular estimates for the base of Placentalia are older than the date obtained by Bininda-Emonds et al. (2007), e.g., Kumar and Hedges (1998) obtained a date of ∼129 Ma.

Figure 2

Example of a homology problem from Chen et al.’s (2017) phylogenomic data set for Laurasiatheria and outgroups. Partial ETV1 gene alignment (top) and gene tree for the full ETV1 alignment are shown. Protein-coding sequences for 15 taxa (green lettering) are for exon 1 and begin on the start codon ATG, but the first eight taxa in the alignment (red lettering) instead are represented by sequence from intron 1 of ETV1. Faulty annotation and subsequent misalignment of protein-coding sequence to non-coding sequence results in 20 ‘pseudo-synapomorphies’ for a clade that contradicts five well-established mammalian clades. The long internal branch that subtends this clade, 0.0328 substitutions per site, is indicated. Nucleotides that differ from the majority nucleotide at each position in the alignment are highlighted in colored boxes.

Figure 3

Example of ‘zombie’ whale lineages implied by the timetree for mammals of Liu et al. (2017a). Due to inadequate density of fossil calibrations in this molecular clock study, the slowly evolving cetacean clade shows extremely shallow divergences (A) relative to previous molecular clock analyses such as McGowen et al. (2009) (B). Numerous extinct sperm whales (Physeteroidea) and baleen whales (Mysticeti) are found in strata that are much older than the divergence time estimate between Physeter (giant sperm whale) and Balaenoptera (rorqual baleen whale) in (A) but not in(B). Geological range estimates for extinct mysticetes (green bars) and physeteroids (brown bars) are from Marx and Fordyce (2015) and Lambert et al. (2017a; 2017b). Paintings are by C. Buell.

Figure 4

Summary of pseudoextinction results for the reanalysis of morphological data from Morphobank Project 773 (O’Leary et al., 2013). Analyses were performed with a molecular scaffold that was based on robustly supported clades (>95% bootstrap support) from Meredith et al.’s (2011) phylogenetic analysis of 26 nuclear loci. The molecular scaffold included several polytomies that are not yet confidently resolved by molecular data: trichotomy at root of Placentalia (Afrotheria, Boreoeutheria, Xenarthra), paenungulate trichotomy (Hyracoidea, Proboscidea, Sirenia), Euarchontoglires trichotomy (Primatomorpha, Glires, Scandentia), and Laurasiatheria polytomy (Carnivora+Pholidota, Chiroptera, Cetartiodactyla, Perissodactyla). Pseudoextinct taxa were made pseudoextinct by recoding soft tissue characters as missing and deleting the pseudoextinct taxon from the molecular scaffold. Maximum parsimony analyses of 19 ordinal level taxa were individually executed with PAUP 4.0a165 (Swofford, 2002) and compared to the master scaffold. Parsimony analyses for each pseudoextinct clade were performed with 1000 random input orders of taxa and tree-bisection and reconnection branch swapping. Mammalian orders that showed shifts in phylogenetic position in these analyses are indicated by arrows that show the movements of entire clades as well as the repositioning of subtaxa within or among orders. Only four orders (Lagomorpha, Hyracoidea, Proboscidea, Sirenia) did not show changes to phylogenetic relationships in these analyses. Monotreme outgroups were included in the original analysis but were pruned from the tree shown here. Paintings are by C. Buell.

Figure 5

Examples of the effects of coalescence for individual genes on divergence time estimation relative to speciation times (i.e., incipient cladogenesis with cessation of gene flow), T1 and T2. Gene tree lineages are thin and black and are contained within thick and yellow species tree lineages. (A) Coalescence of a gene in the most recent common ancestor of X and Y and in the most recent common ancestor of X+Y and W. The topology of the species tree and the topology of the gene tree are congruent. Coalescence times for this gene exceed species divergence times, but by less than one internal branch. (B) Deep coalescence of a gene in the common ancestor of W, X, and Y in which the gene tree topology agrees with the species tree topology. (C) Deep coalescence of a gene in the common ancestor of W, X, and Y in which the gene tree topology conflicts with the species tree topology. All coalescences of genes in this figure are deeper than speciation times, so molecular clock estimates from these gene trees would be older than the true speciation times (T1 and T2).

Figure 6

Examples of the effects of introgression/hybridization on divergence time estimation relative to speciation (incipient cladogenesis) times for individual gene segments that each have a single evolutionary history. (A) Introgression of a gene from the ancestor of Y to the ancestor of X. This gene flow pathway will decrease the estimated divergence time between X and Y relative to the actual speciation time (T2), but have no effect on the estimated divergence time between W and X+Y. (B) Introgression of a gene from the ancestor of W to the ancestor of X. This gene flow pathway will increase the amount of divergence between X and Y relative to the speciation time T2, and decrease the divergence between W and X+Y relative to the speciation time T1. If this gene flow pattern is pervasive through the genome, then the democratic vote (i.e., count of different genes supporting each topology) of traditional concatenation and coalescence methods will flip the topology to [(W,X),Y]. (C) Introgression of a gene from the ancestor of X to the ancestor of W. This gene flow pathway will have no effect on the estimated divergence between X and Y relative to the speciation time T2, but will decrease the estimated divergence between W and X+Y relative to the speciation time T1. If this gene flow pattern is pervasive through the genome, then the democratic vote will flip the topology to [(W,X),Y]. (D) Introgression of a gene from an extinct relative of W to the ancestor of X. Introgressed genes of this type will increase the estimated divergence between X and Y relative to the speciation time T2, and decrease the estimated divergence between W and X+Y relative to the speciation time T1. If this gene flow pattern is pervasive through the genome, then the democratic vote will flip the topology to [(W,X),Y]. (E) Introgression of a gene from an extinct relative of X+Y to the ancestor of X. Introgressed genes of this type will increase the estimated divergence between X and Y relative to the speciation time T2, but have no effect on the estimated divergence between W and X + Y relative to the speciation time T1. (F) Hybridization between the ancestors of X and Y results in a new species, (H), that coexists with the parental lineages that terminate in species X and Y. If the majority of the genome of H is derived from the ancestral lineage to X, then the democratic vote across the genome will favor the topology ((H,X),Y). Conversely, if the majority of the genome of H is derived from the ancestral lineage to Y, then the democratic vote across the genome will favor the topology [(H,Y),X].