The soft explosive model of placental mammal evolution

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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.

Electronic supplementary material

The online version of this article (10.1186/s12862-018-1218-x) contains supplementary material, which is available to authorized users.

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Most cited references 58

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The delayed rise of present-day mammals.

Olaf Bininda-Emonds, Marcel Cardillo, Kate E. Jones … (2007)

Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals.

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The placental mammal ancestor and the post-K-Pg radiation of placentals.

Maureen A. O'Leary, Jonathan I. Bloch, John J. Flynn … (2013)

To discover interordinal relationships of living and fossil placental mammals and the time of origin of placentals relative to the Cretaceous-Paleogene (K-Pg) boundary, we scored 4541 phenomic characters de novo for 86 fossil and living species. Combining these data with molecular sequences, we obtained a phylogenetic tree that, when calibrated with fossils, shows that crown clade Placentalia and placental orders originated after the K-Pg boundary. Many nodes discovered using molecular data are upheld, but phenomic signals overturn molecular signals to show Sundatheria (Dermoptera + Scandentia) as the sister taxon of Primates, a close link between Proboscidea (elephants) and Sirenia (sea cows), and the monophyly of echolocating Chiroptera (bats). Our tree suggests that Placentalia first split into Xenarthra and Epitheria; extinct New World species are the oldest members of Afrotheria.

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Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds.

Ziheng Yang, Bruce Rannala (2006)

We implement a Bayesian Markov chain Monte Carlo algorithm for estimating species divergence times that uses heterogeneous data from multiple gene loci and accommodates multiple fossil calibration nodes. A birth-death process with species sampling is used to specify a prior for divergence times, which allows easy assessment of the effects of that prior on posterior time estimates. We propose a new approach for specifying calibration points on the phylogeny, which allows the use of arbitrary and flexible statistical distributions to describe uncertainties in fossil dates. In particular, we use soft bounds, so that the probability that the true divergence time is outside the bounds is small but nonzero. A strict molecular clock is assumed in the current implementation, although this assumption may be relaxed. We apply our new algorithm to two data sets concerning divergences of several primate species, to examine the effects of the substitution model and of the prior for divergence times on Bayesian time estimation. We also conduct computer simulation to examine the differences between soft and hard bounds. We demonstrate that divergence time estimation is intrinsically hampered by uncertainties in fossil calibrations, and the error in Bayesian time estimates will not go to zero with increased amounts of sequence data. Our analyses of both real and simulated data demonstrate potentially large differences between divergence time estimates obtained using soft versus hard bounds and a general superiority of soft bounds. Our main findings are as follows. (1) When the fossils are consistent with each other and with the molecular data, and the posterior time estimates are well within the prior bounds, soft and hard bounds produce similar results. (2) When the fossils are in conflict with each other or with the molecules, soft and hard bounds behave very differently; soft bounds allow sequence data to correct poor calibrations, while poor hard bounds are impossible to overcome by any amount of data. (3) Soft bounds eliminate the need for "safe" but unrealistically high upper bounds, which may bias posterior time estimates. (4) Soft bounds allow more reliable assessment of estimation errors, while hard bounds generate misleadingly high precisions when fossils and molecules are in conflict.

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Author and article information

Contributors

Matthew J. Phillips:

ORCID: http://orcid.org/0000-0003-1532-449X

m9.phillips@qut.edu.au

Carmelo Fruciano: carmelofruciano@yahoo.it

Journal

Journal ID (nlm-ta): BMC Evol Biol

Journal ID (iso-abbrev): BMC Evol. Biol

Title: BMC Evolutionary Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2148

Publication date (Electronic): 3 July 2018

Publication date PMC-release: 3 July 2018

Publication date Collection: 2018

Volume: 18

Electronic Location Identifier: 104

Affiliations

ISNI 0000000089150953, GRID grid.1024.7, School of Earth, Environmental and Biological Sciences, , Queensland University of Technology, ; Brisbane, Australia

Author information

Matthew J. Phillips http://orcid.org/0000-0003-1532-449X

Article

Publisher ID: 1218

DOI: 10.1186/s12862-018-1218-x

PMC ID: 6029115

PubMed ID: 29969980

SO-VID: 8184e0ff-749f-496b-9336-b8dd8988aff7

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 17 October 2017

Date accepted : 19 June 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100000923, Australian Research Council;

Award ID: DP150104659

Custom metadata

ScienceOpen disciplines: Evolutionary Biology

Keywords: cretaceous-paleogene boundary,fossil calibration,life history,molecular dating,placentalia

Data availability:

ScienceOpen disciplines: Evolutionary Biology

Keywords: cretaceous-paleogene boundary, fossil calibration, life history, molecular dating, placentalia

The soft explosive model of placental mammal evolution

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Most cited references 58

The delayed rise of present-day mammals.

The placental mammal ancestor and the post-K-Pg radiation of placentals.

Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds.

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