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. 2018 Jul 3;18(1):104.
doi: 10.1186/s12862-018-1218-x.

The Soft Explosive Model of Placental Mammal Evolution

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Free PMC article

The Soft Explosive Model of Placental Mammal Evolution

Matthew J Phillips et al. BMC Evol Biol. .
Free PMC article

Abstract

Background: Recent molecular dating estimates for placental mammals echo fossil inferences for an explosive interordinal diversification, but typically place this event some 10-20 million years earlier than the Paleocene fossils, among apparently more "primitive" mammal faunas.

Results: However, current models of molecular evolution do not adequately account for parallel rate changes, and result in dramatic divergence underestimates for large, long-lived mammals such as whales and hominids. Calibrating among these taxa shifts the rate model errors deeper in the tree, inflating interordinal divergence estimates. We employ simulations based on empirical rate variation, which show that this "error-shift inflation" can explain previous molecular dating overestimates relative to fossil inferences. Molecular dating accuracy is substantially improved in the simulations by focusing on calibrations for taxa that retain plesiomorphic life-history characteristics. Applying this strategy to the empirical data favours the soft explosive model of placental evolution, in line with traditional palaeontological interpretations - a few Cretaceous placental lineages give rise to a rapid interordinal diversification following the 66 Ma Cretaceous-Paleogene boundary mass extinction.

Conclusions: Our soft explosive model for the diversification of placental mammals brings into agreement previously incongruous molecular, fossil, and ancestral life history estimates, and closely aligns with a growing consensus for a similar model for bird evolution. We show that recent criticism of the soft explosive model relies on ignoring both experimental controls and statistical confidence, as well as misrepresentation, and inconsistent interpretations of morphological phylogeny. More generally, we suggest that the evolutionary properties of adaptive radiations may leave current molecular dating methods susceptible to overestimating the timing of major diversification events.

Keywords: Cretaceous-Paleogene boundary; Fossil calibration; Life history; Molecular dating; Placentalia.

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Figures

Fig. 1
Fig. 1
Eutherian fossil record species diversification rate. Data points are calculated as new appearances/Ma (scaled by species richness in the previous time bin, a proxy for starting species richness). Barremian-Aptian provides the previous time bin for Albian-Cenomanian. The green-blue colour shading indicates the proportion of eutherians among mammal first appearances for each time bin. Referenced arrows indicate molecular dating estimates for the temporal midpoint of the placental interordinal diversification, including for Laurasiatheria, Euarchontoglires and Afrotheria (See Additional file 2: Table S2). The KPg boundary is shown as red dashes. Tur-San, Turonian to Santonian; Maa, Maastrichtian [–3], [–12] [–69]
Fig. 2
Fig. 2
Simulating error-shift inflation of deep placental divergences, and amelioration by excluding calibrations among large, long-lived clades. a. Dated tree on which 20,000 bp DNA sequences were simulated under two rate schemes, “ancestral rates” with all branch rates drawn from a single lognormal distribution (see Methods) and “mixed rates” with the rate drawn from that same distribution, except divided by 5 for the daughter lineages of nodes I and III. b. Soft bound calibrations on nodes I-VI under alternative MCMCtree reconstructions. Date estimates and 95% CIs for simulated clades c “Placentalia” d “Laurasiatheria” and e “Sirenia” are shown for the “ancestral rates” simulation (light grey), and for the “mixed rates” simulation with either full calibration (black) or calibration only on ancestral rates clades (dark grey). Corresponding date estimates from Phillips ([11], Fig. 4c,d) on the empirical data are shown for f Placentalia, g Laurasiatheria and h Sirenia, with full calibration (black) and largely focusing on ancestral rates clades (dark grey)
Fig. 3
Fig. 3
Placental mammal ordinal-level timetrees on the 122-taxon dataset for which large, long-lived taxa are excluded. Node heights are averaged over MCMCtree independent and autocorrelated rates analyses, with 95% CIs shown for analyses under independent rates (purple bars) and autocorrelated rates (grey bars). a. using our dR40 calibration set. b. Adding additional poorly-vetted calibrations for Lorisiformes, Lagomorpha, Emballonuroidea and Erinaceidae-Soricidae, and with maximum bounds for basal Primates, Rodentia and Chiroptera increased, following Springer et al. [10]. Substituting in these “dR40Springer” calibrations inflates the midpoint for the primary placental interordinal diversification from 64.5 Ma to 72.2 Ma
Fig. 4
Fig. 4
Comparison of the dR40 and dR40Springer calibration bounds, joint marginal priors, and posterior divergence estimates for seven key clades. For each clade the calibration bounds and 95% CIs for marginal priors and posterior estimates are shown (above) for our preferred dR40 calibration set, and (below) for the dR40Springer calibration set with calibration bounds substituted in from Springer et al. [10]. Posterior estimates are shown separately for the autocorrelated and independent rates models, however, the marginal priors under these two rates models are effectively the same, and here for clarity we average over the slight, primarily stochastic differences between them. (marginal priors and posterior estimates are provided in Additional file 2). Erinaceidae-Soricidae is further discussed in Additional file 1 (“Incorrect or poorly supported fossil placements”, 7)

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