Waking the undead: Implications of a soft explosive model for the timing of placental mammal diversification

Abstract

The explosive, long fuse, and short fuse models represent competing hypotheses for the timing of placental mammal diversification. Support for the explosive model, which posits both interordinal and intraordinal diversification after the KPg mass extinction, derives from morphological cladistic studies that place Cretaceous eutherians outside of crown Placentalia. By contrast, most molecular studies favor the long fuse model wherein interordinal cladogenesis occurred in the Cretaceous followed by intraordinal cladogenesis after the KPg boundary. Phillips (2016) proposed a soft explosive model that allows for the emergence of a few lineages (Xenarthra, Afrotheria, Euarchontoglires, Laurasiatheria) in the Cretaceous, but otherwise agrees with the explosive model in positing the majority of interordinal diversification after the KPg mass extinction. Phillips (2016) argues that rate transference errors associated with large body size and long lifespan have inflated previous estimates of interordinal divergence times, and further suggests that most interordinal divergences are positioned after the KPg boundary when rate transference errors are avoided through the elimination of calibrations in large-bodied and/or long lifespan clades. Here, we show that rate transference errors can also occur in the opposite direction and drag forward estimated divergence dates when calibrations in large-bodied/long lifespan clades are omitted. This dragging forward effect results in the occurrence of more than half a billion years of 'zombie lineages' on Phillips' preferred timetree. By contrast with ghost lineages, which are a logical byproduct of an incomplete fossil record, zombie lineages occur when estimated divergence dates are younger than the minimum age of the oldest crown fossils. We also present the results of new timetree analyses that address the rate transference problem highlighted by Phillips (2016) by deleting taxa that exceed thresholds for body size and lifespan. These analyses recover all interordinal divergence times in the Cretaceous and are consistent with the long fuse model of placental diversification. Finally, we outline potential problems with morphological cladistic analyses of higher-level relationships among placental mammals that may account for the perceived discrepancies between molecular and paleontological estimates of placental divergence times.

Mammal madness: is the mammal tree of life not yet resolved?

“…An alternate explanation is that Phillips' [105] interordinal divergence dates are too young because they are dragged forward by divergence dates in clades with large body size and long lifespan that are also too young. Indeed, Phillip's preferred timetree, which is based on calibrations at only 27 nodes (contra 82 in Meredith et al [4]), has estimated dates at 62 of 136 internal nodes in Placentalia that are younger than minimum ages implied by the fossil record [106]. Included among these nodes are numerous interordinal divergences as well as some divergences in clades that are characterized by smaller body sizes (e.g.…”

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

“…Liu et al's preferred time tree includes 12 nodes (e.g., Paenungulata, Anthropoidea, Caniformia) where molecular divergence dates are more recent than ages implied by fossils (4,8,9), so-called "zombie lineages" (9). The most striking example is for sperm whale versus minke whale (∼2.9 Ma).…”

“…"Unreliability surrounding the fossil record" (1) is, therefore, an unreasonable explanation for this shallow split or for the extremely recent basal divergence in Cetacea (∼11.4 Ma). Widespread zombie lineages in a time tree pull remaining divergence dates toward the present (9). Denser sampling of fossil calibrations and imposition of hard-bounded minima can offset such distortions (2), but these tactics were not utilized.…”

“…Denser sampling of fossil calibrations and imposition of hard-bounded minima can offset such distortions (2), but these tactics were not utilized. Rather than generating "a hypothesis of mammalian divergence timing that is more consistent with the fossil record" (1), widespread homology errors and methodological glitches generated a pattern of diversification that strictly counters extensive systematic work on Mammalia (2-5) and robust paleontological patterns (4,8,9) (The Paleobiology Database; paleodb.org).…”

Recombination-aware phylogenomics unravels the complex divergence of hybridizing species.

“…This raises the prospect that some described 'star-like' phylogenies might be artifacts resulting from combined effects of selecting phylogenetic markers from regions of elevated recombination rate that contained mixed histories derived from historical/contemporary gene flow. Accounting for this bias may play a central role in resolving conflicts between molecular divergence times and paleontological estimates for taxon originations (Meredith et al 2011;dos Reis et al 2012;Liu et al 2017;Springer et al 2017), thus contributing to a substantially more accurate reconstruction of the history of life.…”