The soft explosive model of placental mammal evolution

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 Howev...

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Main Authors: Matthew J. Phillips, Carmelo Fruciano
Format: Article
Language:English
Published: BMC 2018-07-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12862-018-1218-x
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author Matthew J. Phillips
Carmelo Fruciano
author_facet Matthew J. Phillips
Carmelo Fruciano
author_sort Matthew J. Phillips
collection DOAJ
description 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.
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spelling doaj.art-1c00ec554fbc4d75a887a28fc215fb1a2022-12-21T21:45:56ZengBMCBMC Evolutionary Biology1471-21482018-07-0118111310.1186/s12862-018-1218-xThe soft explosive model of placental mammal evolutionMatthew J. Phillips0Carmelo Fruciano1School of Earth, Environmental and Biological Sciences, Queensland University of TechnologySchool of Earth, Environmental and Biological Sciences, Queensland University of TechnologyAbstract 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.http://link.springer.com/article/10.1186/s12862-018-1218-xCretaceous-Paleogene boundaryFossil calibrationLife historyMolecular datingPlacentalia
spellingShingle Matthew J. Phillips
Carmelo Fruciano
The soft explosive model of placental mammal evolution
BMC Evolutionary Biology
Cretaceous-Paleogene boundary
Fossil calibration
Life history
Molecular dating
Placentalia
title The soft explosive model of placental mammal evolution
title_full The soft explosive model of placental mammal evolution
title_fullStr The soft explosive model of placental mammal evolution
title_full_unstemmed The soft explosive model of placental mammal evolution
title_short The soft explosive model of placental mammal evolution
title_sort soft explosive model of placental mammal evolution
topic Cretaceous-Paleogene boundary
Fossil calibration
Life history
Molecular dating
Placentalia
url http://link.springer.com/article/10.1186/s12862-018-1218-x
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