When Placental Mammals Evolved

Dating Placentalia: Morphological clocks fail to close the molecular-fossil gap

Authors:

Puttick et al

Abstract:

Dating the origin of Placentalia has been a contentious issue for biologists and paleontologists. While it is likely that crown-group placentals originated in the Late Cretaceous, nearly all molecular clock estimates point to a deeper Cretaceous origin. An approach with the potential to reconcile this discrepancy could be the application of a morphological clock. This would permit the direct incorporation of fossil data in node dating, and would break long internal branches of the tree, so leading to improved estimates of node ages. Here, we use a large morphological dataset and the tip-calibration approach of MrBayes. We find that the estimated date for the origin of crown mammals is much older (∼130–145 Ma) than fossil and molecular clock data (∼80–90 Ma). Our results suggest that tip-calibration may result in estimated dates that are more ancient than those obtained from other sources of data. This can be partially overcome by constraining the ages of internal nodes on the tree; however, when this was applied to our dataset, the estimated dates were still substantially more ancient than expected. We recommend that results obtained using tip-calibration, and possibly morphological dating more generally, should be treated with caution.

Did Placentals and Marsupials Diverge 170 Million Years ago Starting at the Aalenian/Bajocian Jurassic?

The Interrelationships of Placental Mammals and the Limits of Phylogenetic Inference

Authors:

Tarver et al

Abstract:

Placental mammals comprise three principal clades: Afrotheria (e.g. elephants and tenrecs), Xenarthra (e.g. armadillos and sloths) and Boreoeutheria (all other placental mammals), the relationships among which are the subject of controversy and a touchstone for debate on the limits of phylogenetic inference. Previous analyses have found support for all three hypotheses, leading some to conclude that this phylogenetic problem might be impossible to resolve, due to the compounded effects of Incomplete Lineage Sorting (ILS) and a rapid radiation. Here we show, using a genome scale nucleotide dataset, microRNAs, and the reanalysis of the three largest previously published amino-acid datasets, that the root of Placentalia lies between Atlantogenata and Boreoeutheria. Although we found evidence for ILS in early placental evolution, we are able to reject previous conclusions that the placental root is a hard polytomy that cannot be resolved. Reanalyses of previous datasets recover Atlantogenata + Boreoeutheria and show that contradictory results are a consequence of poorly fitting evolutionary models; instead, when the evolutionary process is better-modelled, all datasets converge on Atlantogenata. Our Bayesian molecular clock analysis estimates that marsupials diverged from placentals 157-170 Ma, crown Placentalia diverged 86-100 Ma, and crown Atlantogenata diverged 84-97 Ma. Our results are compatible with placental diversification being driven by dispersal rather than vicariance mechanisms, postdating early phases in the protracted opening of the Atlantic Ocean.

Uncertainty in the Timing of Animal (Metazoan) Origins Strongly Suggest Molecular Clock Dating is Premature for use

Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales

Authors:

dos Reis et al

Abstract:

The timing of divergences among metazoan lineages is integral to understanding the processes of animal evolution, placing the biological events of species divergences into the correct geological timeframe. Recent fossil discoveries and molecular clock dating studies have suggested a divergence of bilaterian phyla greater than 100 million years before the Cambrian, when the first definite crown-bilaterian fossils occur. Most previous molecular clock dating studies, however, have suffered from limited data and biases in methodologies, and virtually all have failed to acknowledge the large uncertainties associated with the fossil record of early animals, leading to inconsistent estimates among studies. Here we use an unprecedented amount of molecular data, combined with four fossil calibration strategies (reflecting disparate and controversial interpretations of the metazoan fossil record) to obtain Bayesian estimates of metazoan divergence times. Our results indicate that the uncertain nature of ancient fossils and violations of the molecular clock impose a limit on the precision that can be achieved in estimates of ancient molecular timescales. For example, although we can assert that crown Metazoa originated during the Cryogenian (with most crown-bilaterian phyla diversifying during the Ediacaran), it is not possible with current data to pinpoint the divergence events with sufficient accuracy to test for correlations between geological and biological events in the history of animals. Although a Cryogenian origin of crown Metazoa agrees with current geological interpretations, the divergence dates of the bilaterians remain controversial. Thus, attempts to build evolutionary narratives of early animal evolution based on molecular clock timescales appear to be premature.

Molecular Clock Suggests Angiosperms Diverged in the Middle to Late Jurassic

Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times

Authors:

Zeng et al

Abstract:

Angiosperms are the most successful plants and support human livelihood and ecosystems. Angiosperm phylogeny is the foundation of studies of gene function and phenotypic evolution, divergence time estimation and biogeography. The relationship of the five divergent groups of the Mesangiospermae (~99.95% of extant angiosperms) remains uncertain, with multiple hypotheses reported in the literature. Here transcriptome data sets are obtained from 26 species lacking sequenced genomes, representing each of the five groups: eudicots, monocots, magnoliids, Chloranthaceae and Ceratophyllaceae. Phylogenetic analyses using 59 carefully selected low-copy nuclear genes resulted in highly supported relationships: sisterhood of eudicots and a clade containing Chloranthaceae and Ceratophyllaceae, with magnoliids being the next sister group, followed by monocots. Our topology allows a re-examination of the evolutionary patterns of 110 morphological characters. The molecular clock estimates of Mesangiospermae diversification during the late to middle Jurassic correspond well to the origins of some insects, which may have been a factor facilitating early angiosperm radiation.

When *DID* Placental Mammals Really Evolve?

Ancient dates or accelerated rates? Morphological clocks and the antiquity of placental mammals

Authors:

Beck et al

Abstract:

Analyses of a comprehensive morphological character matrix of mammals using ‘relaxed’ clock models (which simultaneously estimate topology, divergence dates and evolutionary rates), either alone or in combination with an 8.5 kb nuclear sequence dataset, retrieve implausibly ancient, Late Jurassic–Early Cretaceous estimates for the initial diversification of Placentalia (crown-group Eutheria). These dates are much older than all recent molecular and palaeontological estimates. They are recovered using two very different clock models, and regardless of whether the tree topology is freely estimated or constrained using scaffolds to match the current consensus placental phylogeny. This raises the possibility that divergence dates have been overestimated in previous analyses that have applied such clock models to morphological and total evidence datasets. Enforcing additional age constraints on selected internal divergences results in only a slight reduction of the age of Placentalia. Constraining Placentalia to less than 93.8 Ma, congruent with recent molecular estimates, does not require major changes in morphological or molecular evolutionary rates. Even constraining Placentalia to less than 66 Ma to match the ‘explosive’ palaeontological model results in only a 10- to 20-fold increase in maximum evolutionary rate for morphology, and fivefold for molecules. The large discrepancies between clock- and fossil-based estimates for divergence dates might therefore be attributable to relatively small changes in evolutionary rates through time, although other explanations (such as overly simplistic models of morphological evolution) need to be investigated. Conversely, dates inferred using relaxed clock models (especially with discrete morphological data and MrBayes) should be treated cautiously, as relatively minor deviations in rate patterns can generate large effects on estimated divergence dates.

Rocks vs Genes: Timing the Evolution of Birds

Flying rocks and flying clocks: disparity in fossil and molecular dates for birds

Authors:

Ksepka et al

Abstract:

Major disparities are recognized between molecular divergence dates and fossil ages for critical nodes in the Tree of Life, but broad patterns and underlying drivers remain elusive. We harvested 458 molecular age estimates for the stem and crown divergences of 67 avian clades to explore empirical patterns between these alternate sources of temporal information. These divergence estimates were, on average, over twice the age of the oldest fossil in these clades. Mitochondrial studies yielded older ages than nuclear studies for the vast majority of clades. Unexpectedly, disparity between molecular estimates and the fossil record was higher for divergences within major clades (crown divergences) than divergences between major clades (stem divergences). Comparisons of dates from studies classed by analytical methods revealed few significant differences. Because true divergence ages can never be known with certainty, our study does not answer the question of whether fossil gaps or molecular dating error account for a greater proportion of observed disparity. However, empirical patterns observed here suggest systemic overestimates for shallow nodes in existing molecular divergence dates for birds. We discuss underlying biases that may drive these patterns.

Academic Bun Fight: Evolution of Placental Mammals Since the KT/K-Pg Event

This is one of those topics I wish Darren Naish would give an opinion on.   I normally like to start the day with a precambrian paper of some kind, but I don't see one I'm, uh, digging.  However, this bun fight is sticky and interesting.

O'Leary et al published a paper on the evolution of placental mammals across the KT/K-Pg boundary (The Placental Mammal Ancestor and the Post–K-Pg Radiation of Placentals). They used both genomic and phenomic data to create a supermatrix to produce a phylogeny of placental mammals using 86 different critters and over 4500 characters.  They used far, far more data than any study before, from what I gather.  One of the radical arguments is there was one (*1*) ancestor to modern placentals.

There has now been a critique of the paper (Technical Comment on “The Placental Mammal Ancestor and the Post–K-Pg Radiation of Placentals".  The basic theme is O'Leary et al probably overreached with their analysis.  One of the cautions stated is similar lifestyles will cause convergent evolution.   

The reply from the original authors is here (Response to Comment on “The Placental Mammal Ancestor and the Post–K-Pg Radiation of Placentals”) where they offer their counter arguments. I am not so sure I buy into the comment of "Accumulated negative evidence indicates that [placental] fossils are absent."  That comment strikes me as very wrong. 

But then, I am not an expert and this is why I wish Darren would comment. 

Exploring the Potential Triggers for the Cambrian Explosion

Triggers for the Cambrian explosion: Hypotheses and problems

Authors:

1. Xingliang Zhang (a)
2. Degan Shu (a)
3. Jian Han (a)
4. Zhifei Zhang (a)
5. Jianni Liu (a)
6. Dongjing Fu (a)

Affiliations:

a. Early Life Institute and State Key Laboratory for Continental Dynamics, Department of Geology, Northwest University, Xian 710069, China

Abstract:

Abrupt appearance of major bilaterian clades in the fossil record during the first three stages of the Cambrian Period has puzzled the scientific world since 1830s. Many proposed causes including environmental, developmental, and ecological hypotheses, are reviewed. Nutrient availability, oxygenation, and change of seawater composition are commonly supposed to be environmental triggers. The nutrient input, e.g. the enrichment of phosphorus in an environment, would cause excess primary production, but it is neither directly linked with diversity nor disparity. Fluctuating abiotic conditions during the Snowball Earth and the associated oxygenation event may have stimulated the diversification of complex multicellular organisms including diverse of macroscopic and morphologically differentiated algae in the early Ediacaran, but did not lead to the ecological success of metazoan or bilaterian lineages. Further increase of oxygen level and change of seawater composition just before and during early Cambrian are suggested by the high weathering rate of the trans-Gondwana mountains, Great Unconformity, and decline of oceanic salinity. These are potential candidates of environmental triggers for the Cambrian explosion but require future more detailed geochemical studies to confirm. The molecular phylogeny calibrated with the molecular clock data suggested that the developmental system of bilaterians was established before their divergence. This, in turn, suggests that the Cambrian explosion require environmental triggers. However, there still exists the contention between deep or shallow divergence of bilaterian clades, which remains to be solved in the future. The deep divergence model is supported by a majority of molecular clock studies, but is challenged by the paucity of bilaterian fossils before and during the Ediacaran Period. The shallow model is generally consistent with the fossil record, but has to explain the rapidity of increase in diversity, disparity, morphological complexity, acquisition of biomineralized shells, etc. Regardless of deep or shallow model, the conservation of lineage-specific kernels within the gene regulatory networks (GRNs) provides an explanation for the long-term stability of body plans after the Cambrian explosion, and continuous addition of microRNAs into the GRNs seems to correspond well to the increase in morphological complexity. As for ecological causes, some hypotheses (e.g. adaptive radiation after mass extinction, cropping, and geosphere-biosphere feedbacks) can not explain the uniqueness of the event, some others (such as Cambrian substrate revolution, predator–prey pressure, evolution of zooplankton, and roughening of fitness landscapes) fall into the trap of chicken-and-egg problem because of considering the consequence as a cause. Expansion of ecosystem engineering in the early Cambrian might also be caused by the Cambrian explosion. However, ecosystem engineering associated with Ediacaran ecosystems is likely a pivotal ecological prerequisite for the later ecological success of bilaterian clades, particularly the engineering effect by Ediacaran sponges that ventilated seawater by sponge pumping and removing organic material from the water column. However, the ecological abundance of Ediacaran sponges needs to be further investigated. Finally, a working plan is proposed for future research. For paleontologists, searching for ancestors of early Cambrian faunas is crucial to testify the earlier divergence of bilaterian lineages. Environmentally, precise values on the oxygen level and seawater composition are required during the Ediacaran-Cambrian transition.

A Simple Method for Reconciling Molecular and Fossil Divergence Dates

A Simple Method for Estimating Informative Node Age Priors for the Fossil Calibration of Molecular Divergence Time Analyses

Authors:

1. Michael D. Nowak (a)
2. Andrew B. Smith (b)
3. Carl Simpson (c)
4. Derrick J. Zwickl

Affiliations:

a. Institute of Systematic Botany, University of Zürich, Zürich, Switzerland

b. Department of Palaeontology, The Natural History Museum, London, United Kingdom

c. Museum für Naturkunde der Humboldt-Universität zu Berlin, Berlin, Germany

d. Department of Ecology and Evolution, University of Kansas, Lawrence, Kansas, United States of America

Abstract:

Molecular divergence time analyses often rely on the age of fossil lineages to calibrate node age estimates. Most divergence time analyses are now performed in a Bayesian framework, where fossil calibrations are incorporated as parametric prior probabilities on node ages. It is widely accepted that an ideal parameterization of such node age prior probabilities should be based on a comprehensive analysis of the fossil record of the clade of interest, but there is currently no generally applicable approach for calculating such informative priors. We provide here a simple and easily implemented method that employs fossil data to estimate the likely amount of missing history prior to the oldest fossil occurrence of a clade, which can be used to fit an informative parametric prior probability distribution on a node age. Specifically, our method uses the extant diversity and the stratigraphic distribution of fossil lineages confidently assigned to a clade to fit a branching model of lineage diversification. Conditioning this on a simple model of fossil preservation, we estimate the likely amount of missing history prior to the oldest fossil occurrence of a clade. The likelihood surface of missing history can then be translated into a parametric prior probability distribution on the age of the clade of interest. We show that the method performs well with simulated fossil distribution data, but that the likelihood surface of missing history can at times be too complex for the distribution-fitting algorithm employed by our software tool. An empirical example of the application of our method is performed to estimate echinoid node ages. A simulation-based sensitivity analysis using the echinoid data set shows that node age prior distributions estimated under poor preservation rates are significantly less informative than those estimated under high preservation rates.

Estimating Divergence Times in Large Molecular Phylogenies

Estimating divergence times in large molecular phylogenies

Authors:

1. Koichiro Tamura (a)
2. Fabia Ursula Battistuzzi (b,c)
3. Paul Billing-Ross (b)
4. Oscar Murillo (b)
5. Alan Filipski (b)
6. Sudhir Kumar (b,d,*)

Author Affiliations:

a. Department of Biological Sciences, Tokyo Metropolitan University, Tokyo 192-0397, Japan

b. Center for Evolutionary Medicine and Informatics, Biodesign Institute, Arizona State University, Tempe, AZ 85287-5301

c. Department of Biological Sciences, Oakland University, Rochester, MI 48309

d. School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501

*. To whom correspondence should be addressed. E-mail: s.kumar@asu.edu.

Abstract:

Molecular dating of species divergences has become an important means to add a temporal dimension to the Tree of Life. Increasingly larger datasets encompassing greater taxonomic diversity are becoming available to generate molecular timetrees by using sophisticated methods that model rate variation among lineages. However, the practical application of these methods is challenging because of the exorbitant calculation times required by current methods for contemporary data sizes, the difficulty in correctly modeling the rate heterogeneity in highly diverse taxonomic groups, and the lack of reliable clock calibrations and their uncertainty distributions for most groups of species. Here, we present a method that estimates relative times of divergences for all branching points (nodes) in very large phylogenetic trees without assuming a specific model for lineage rate variation or specifying any clock calibrations. The method (RelTime) performed better than existing methods when applied to very large computer simulated datasets where evolutionary rates were varied extensively among lineages by following autocorrelated and uncorrelated models. On average, RelTime completed calculations 1,000 times faster than the fastest Bayesian method, with even greater speed difference for larger number of sequences. This speed and accuracy will enable molecular dating analysis of very large datasets. Relative time estimates will be useful for determining the relative ordering and spacing of speciation events, identifying lineages with significantly slower or faster evolutionary rates, diagnosing the effect of selected calibrations on absolute divergence times, and estimating absolute times of divergence when highly reliable calibration points are available.