Genomic evidence reveals a radiation of placental mammals uninterrupted by the KPg boundary

Abstract

The timing of the diversification of placental mammals relative to the Cretaceous-Paleogene (KPg) boundary mass extinction remains highly controversial. In particular, there have been seemingly irreconcilable differences in the dating of the early placental radiation not only between fossil-based and molecular datasets but also among molecular datasets. To help resolve this discrepancy, we performed genome-scale analyses using 4,388 loci from 90 taxa, including representatives of all extant placental orders and transcriptome data from flying lemurs (Dermoptera) and pangolins (Pholidota). Depending on the gene partitioning scheme, molecular clock model, and genic deviation from molecular clock assumptions, extensive sensitivity analyses recovered widely varying diversification scenarios for placental mammals from a given gene set, ranging from a deep Cretaceous origin and diversification to a scenario spanning the KPg boundary, suggesting that the use of suboptimal molecular clock markers and methodologies is a major cause of controversies regarding placental diversification timing. We demonstrate that reconciliation between molecular and paleontological estimates of placental divergence times can be achieved using the appropriate clock model and gene partitioning scheme while accounting for the degree to which individual genes violate molecular clock assumptions. A birth-death-shift analysis suggests that placental mammals underwent a continuous radiation across the KPg boundary without apparent interruption by the mass extinction, paralleling a genus-level radiation of multituberculates and ecomorphological diversification of both multituberculates and therians. These findings suggest that the KPg catastrophe evidently played a limited role in placental diversification, which, instead, was likely a delayed response to the slightly earlier radiation of angiosperms.

An ABBA-BABA Test for Introgression Using Retroposon Insertion Data

“…6D). Importantly, our comparisons of observed and expected retroposons are not complicated by non-biological sources of gene tree heterogeneity that plague similar comparisons for gene trees that are based on sequence alignments (Song et al 2012;Zhong et al 2013;Jarvis et al 2014;Liu et al 2017).…”

“…5D; Meredith et al 2011;dos Reis et al 2012;Emerling et al 2015;Foley et al 2016;Tarver et al 2016). Previous investigations of this systematic problem have employed both genome-scale DNA sequence data and retroposon insertions, yielding highly incongruent results (Nishihara et al 2006;Hallström et al 2011;Meredith et al 2011;Song et al 2012;Tarver et al 2016;Chen et al 2017;Doronina et al 2017a;Feijoo and Parada, 2017;Liu et al 2017). Some of these analyses are further complicated by homology problems with the underlying data (see Gatesy 2016, 2017;Gatesy and Springer 2017).…”

Virtual endocranial and inner ear endocasts of the Paleocene ‘condylarth’ Chriacus: new insight into the neurosensory system and evolution of early placental mammals

“…Placentals, which give live-birth to well-developed young, can be found all around the world in a plethora of ecological niches and display a wide range of body masses (Nowak, 1999). This clade probably started to diversify during the Late Cretaceous when dinosaurs were still the dominant animals on Earth (Murphy et al, 2001;dos Reis et al, 2012dos Reis et al, , 2014Liu et al, 2017). The end-Cretaceous cataclysm that killed off non-avian dinosaurs and many other vertebrates about 66 million years ago provided placental mammals with a unique opportunity to thrive (Wible et al, 2007;O'Leary et al, 2013).…”

Phylogenomic red flags: Homology errors and zombie lineages in the evolutionary diversification of placental mammals

“…Liu et al (1) construct a species tree for Mammalia based on 4,388 proteincoding genes from 90 taxa to derive a novel model for the placental radiation, but their coalescence time tree shows multiple "red flags" that suggest underlying problems. Three well-validated clades (2-5), Odontoceti (toothed whales), Lemuriformes (lemurs, aye-aye), and Afrosoricida (tenrecs, golden moles) are robustly contradicted (100% bootstrap) in their preferred STAR species tree (1).…”

“…Given these red flags, we examined alignments and gene trees for a subsample of the 400 genes that Liu et al spot-checked and determined were "clean and devoid of the salient irregularities that characterize rogue loci" (1). Detailed visual inspection of the first 50 genes in this "clean" set shows clear-cut homology errors (paralogy, exons aligned to introns, different exons aligned to each other, editing mistakes) in 50 of 50 alignments (100%).…”