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.
Highlights
Placentalia is the crown clade of eutherian mammals and includes 18–19 different orders with living representatives plus other major groups that are entirely extinct (e.g., Meridiungulata, Creodonta, Dinocerata, Mesonychia, Embrithopoda, Desmostylia, and Leptictida)
(1) we review the supporting arguments and shortcomings of each of the five models of placental diversification, including the identification of general problems that can negatively impact divergence time estimates; (2) examine the pros and cons of different timetree methods that may be applied to estimate the timing of the placental radiation; and (3) discuss the complexities of timetree estimation when the genetic signal for speciation times is complicated by the coalescence process and hybridization (Hallström and Janke, 2008)
The reconstruction of a reliable timetree for placental mammals is fundamentally important for understanding the potential role of the KPg extinction and other events in Earth history in promoting mammalian diversification
Summary
Placentalia is the crown clade of eutherian mammals and includes 18–19 different orders with living representatives plus other major groups that are entirely extinct (e.g., Meridiungulata, Creodonta, Dinocerata, Mesonychia, Embrithopoda, Desmostylia, and Leptictida). Like the Explosive Model, the Long Fuse Model suggests an important role for the KPg boundary event, but restricts its impact to intraordinal splitting and ecological/phenotypic diversification, which exploded after the KPg mass extinction event in response to newly available niche space (Meredith et al, 2011) This hypothesis is most strongly favored by analyses of molecular datasets comprising multiple gene fragments for small and large numbers of taxa (Kumar and Hedges, 1998; Eizirik et al, 2001; Murphy et al, 2001a; Murphy et al, 2001b; Springer et al, 2003; Springer et al, 2005; Murphy et al, 2007; Meredith et al, 2011; Lartillot and Delsuc, 2012; Emerling et al, 2015; Hedges et al, 2015; Foley et al, 2016; Springer et al, 2017) and genome wide data (Wildman et al, 2007; dos Reis et al, 2012; dos Reis et al, 2014; Tarver et al, 2016; Wu et al, 2017). One area of interest is to determine whether any of the previously supported models for mammalian evolution based on molecular studies are biased because of the distorting effects of combining loci from regions of the genome with highly variable or elevated recombination rates
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