scholarly journals Investigating the reliability of molecular estimates of evolutionary time when substitution rates and speciation rates vary

2021 ◽  
Author(s):  
Andrew M Ritchie ◽  
Xia Hua ◽  
Lindell Bromham

Background An accurate timescale of evolutionary history is essential to testing hypotheses about the influence of historical events and processes, and the timescale for evolution is increasingly derived from analysis of DNA sequences. But variation in the rate of molecular evolution complicates the inference of time from DNA. Evidence is growing for numerous factors, such as life history and habitat, that are linked both to the molecular processes of mutation and fixation and to rates of macroevolutionary diversification. However, the most widely used models of molecular rate variation, such as the uncorrelated and autocorrelated lognormal clocks, rely on idealised models of rate variation and molecular dating methods are rarely tested against complex models of rate change. One relationship that is not accounted for in molecular dating is the potential for interaction between molecular substitution rates and speciation, a relationship that has been supported by empirical studies in a growing number of taxa. If these relationships are as widespread as evidence indicates, they may have a significant influence on molecular dates. Results We simulate phylogenies and molecular sequences under three different realistic rate variation models - one in which speciation rates and substitution rates both vary but are unlinked, one in which they covary continuously and one punctuated model in which molecular change is concentrated in speciation events, using empirical case studies to parameterise realistic simulations. We test two commonly used "relaxed clock" molecular dating methods against these realistic simulations to explore the degree of error in molecular dates under each model. We find average divergence time inference errors ranging from 12% of node age for the unlinked model when reconstructed under an uncorrelated rate prior, to up to 93% when punctuated simulations are reconstructed under an autocorrelated prior. Conclusions We demonstrate the potential for substantial errors in molecular dates when both speciation rates and substitution rates vary between lineages. This study highlights the need for tests of molecular dating methods against realistic models of rate variation generated from empirical parameters and known relationships.

2019 ◽  
Author(s):  
Qiqing Tao ◽  
Koichiro Tamura ◽  
Beatriz Mello ◽  
Sudhir Kumar

AbstractConfidence intervals (CIs) depict the statistical uncertainty surrounding evolutionary divergence time estimates. They capture variance contributed by the finite number of sequences and sites used in the alignment, deviations of evolutionary rates from a strict molecular clock in a phylogeny, and uncertainty associated with clock calibrations. Reliable tests of biological hypotheses demand reliable CIs. However, current non-Bayesian methods may produce unreliable CIs because they do not incorporate rate variation among lineages and interactions among clock calibrations properly. Here, we present a new analytical method to calculate CIs of divergence times estimated using the RelTime method, along with an approach to utilize multiple calibration uncertainty densities in these analyses. Empirical data analyses showed that the new methods produce CIs that overlap with Bayesian highest posterior density (HPD) intervals. In the analysis of computer-simulated data, we found that RelTime CIs show excellent average coverage probabilities, i.e., the true time is contained within the CIs with a 95% probability. These developments will encourage broader use of computationally-efficient RelTime approach in molecular dating analyses and biological hypothesis testing.


2010 ◽  
Vol 277 (1700) ◽  
pp. 3587-3592 ◽  
Author(s):  
Soo Hyung Eo ◽  
J. Andrew DeWoody

Rates of biological diversification should ultimately correspond to rates of genome evolution. Recent studies have compared diversification rates with phylogenetic branch lengths, but incomplete phylogenies hamper such analyses for many taxa. Herein, we use pairwise comparisons of confamilial sauropsid (bird and reptile) mitochondrial DNA (mtDNA) genome sequences to estimate substitution rates. These molecular evolutionary rates are considered in light of the age and species richness of each taxonomic family, using a random-walk speciation–extinction process to estimate rates of diversification. We find the molecular clock ticks at disparate rates in different families and at different genes. For example, evolutionary rates are relatively fast in snakes and lizards, intermediate in crocodilians and slow in turtles and birds. There was also rate variation across genes, where non-synonymous substitution rates were fastest at ATP8 and slowest at CO 3. Family-by-gene interactions were significant, indicating that local clocks vary substantially among sauropsids. Most importantly, we find evidence that mitochondrial genome evolutionary rates are positively correlated with speciation rates and with contemporary species richness. Nuclear sequences are poorly represented among reptiles, but the correlation between rates of molecular evolution and species diversification also extends to 18 avian nuclear genes we tested. Thus, the nuclear data buttress our mtDNA findings.


2019 ◽  
Vol 37 (1) ◽  
pp. 280-290 ◽  
Author(s):  
Qiqing Tao ◽  
Koichiro Tamura ◽  
Beatriz Mello ◽  
Sudhir Kumar

Abstract Confidence intervals (CIs) depict the statistical uncertainty surrounding evolutionary divergence time estimates. They capture variance contributed by the finite number of sequences and sites used in the alignment, deviations of evolutionary rates from a strict molecular clock in a phylogeny, and uncertainty associated with clock calibrations. Reliable tests of biological hypotheses demand reliable CIs. However, current non-Bayesian methods may produce unreliable CIs because they do not incorporate rate variation among lineages and interactions among clock calibrations properly. Here, we present a new analytical method to calculate CIs of divergence times estimated using the RelTime method, along with an approach to utilize multiple calibration uncertainty densities in dating analyses. Empirical data analyses showed that the new methods produce CIs that overlap with Bayesian highest posterior density intervals. In the analysis of computer-simulated data, we found that RelTime CIs show excellent average coverage probabilities, that is, the actual time is contained within the CIs with a 94% probability. These developments will encourage broader use of computationally efficient RelTime approaches in molecular dating analyses and biological hypothesis testing.


2021 ◽  
Vol 21 (1) ◽  
Author(s):  
De Chen ◽  
Peter A. Hosner ◽  
Donna L. Dittmann ◽  
John P. O’Neill ◽  
Sharon M. Birks ◽  
...  

Abstract Background Divergence time estimation is fundamental to understanding many aspects of the evolution of organisms, such as character evolution, diversification, and biogeography. With the development of sequence technology, improved analytical methods, and knowledge of fossils for calibration, it is possible to obtain robust molecular dating results. However, while phylogenomic datasets show great promise in phylogenetic estimation, the best ways to leverage the large amounts of data for divergence time estimation has not been well explored. A potential solution is to focus on a subset of data for divergence time estimation, which can significantly reduce the computational burdens and avoid problems with data heterogeneity that may bias results. Results In this study, we obtained thousands of ultraconserved elements (UCEs) from 130 extant galliform taxa, including representatives of all genera, to determine the divergence times throughout galliform history. We tested the effects of different “gene shopping” schemes on divergence time estimation using a carefully, and previously validated, set of fossils. Our results found commonly used clock-like schemes may not be suitable for UCE dating (or other data types) where some loci have little information. We suggest use of partitioning (e.g., PartitionFinder) and selection of tree-like partitions may be good strategies to select a subset of data for divergence time estimation from UCEs. Our galliform time tree is largely consistent with other molecular clock studies of mitochondrial and nuclear loci. With our increased taxon sampling, a well-resolved topology, carefully vetted fossil calibrations, and suitable molecular dating methods, we obtained a high quality galliform time tree. Conclusions We provide a robust galliform backbone time tree that can be combined with more fossil records to further facilitate our understanding of the evolution of Galliformes and can be used as a resource for comparative and biogeographic studies in this group.


Author(s):  
Daniel Wood ◽  
Guillaume Besnard ◽  
David J. Beerling ◽  
Colin P. Osborne ◽  
Pascal-Antoine Christin

AbstractThe fossil record provides an invaluable insight into the temporal origins of extant lineages of organisms. However, establishing the relationships between fossils and extant lineages can be difficult in groups with low rates of morphological change over time. Molecular dating can potentially circumvent this issue by allowing distant fossils to act as calibration points, but rate variation across large evolutionary scales can bias such analyses. In this study, we apply multiple dating methods to genome-wide datasets to infer the origin of extant species of Isoetes, a group of mostly aquatic and semi-aquatic isoetalean lycopsids, which closely resemble fossil forms dating back to the Triassic. Rate variation observed in chloroplast genomes hampers accurate dating, but genome-wide nuclear markers place the origin of extant diversity within this group in the mid-Paleogene, 45-60 million years ago. Our genomic analyses coupled with a careful evaluation of the fossil record indicate that despite resembling forms from the Triassic, extant Isoetes species do not represent the remnants of an ancient and widespread group, but instead have spread around the globe in the relatively recent past.


2019 ◽  
Author(s):  
Daniel J. Field ◽  
Jacob S. Berv ◽  
Allison Y. Hsiang ◽  
Robert Lanfear ◽  
Michael J. Landis ◽  
...  

Unravelling the phylogenetic relationships among the major groups of living birds has been described as the greatest outstanding problem in dinosaur systematics. Recent work has identified portions of the avian tree of life that are particularly challenging to reconstruct, perhaps as a result of rapid cladogenesis early in crown bird evolutionary history (specifically, the interval immediately following the end-Cretaceous mass extinction). At face value this hypothesis enjoys support from the crown bird fossil record, which documents the first appearances of most major crown bird lineages in the early Cenozoic—in line with a model of rapid post-extinction niche filling among surviving avian lineages. However, molecular-clock analyses have yielded strikingly variable estimates for the age of crown birds, and conflicting inferences on the impact of the end-Cretaceous mass extinction on the extant bird radiation. This uncertainty has often been ascribed to a patchy avian fossil record, but the possibility of model misspecification in molecular divergence time analyses represents an important and relatively underexplored alternative hypothesis. Here, we highlight the necessity of further developing and using models that account for coordinated variation in rates of molecular evolution across a phylogeny (e.g. molecular early bursts) as a means of assessing support for a rapid post-Cretaceous radiation of crown birds. We discuss how relationships between life-history and substitution rates can mislead divergence time studies that do not account for directional changes in substitution rates over time, and suggest that these effects might have caused some of the variation in existing molecular date estimates for birds. We suggest multiple paths forward that could help resolve this and similar conflicts within other major eukaryotic clades.


Author(s):  
Daniel J. Field ◽  
Jacob S. Berv ◽  
Allison Y. Hsiang ◽  
Robert Lanfear ◽  
Michael J. Landis ◽  
...  

Unravelling the phylogenetic relationships among the major groups of living birds has been described as the greatest outstanding problem in dinosaur systematics. Recent work has identified portions of the avian tree of life that are particularly challenging to reconstruct, perhaps as a result of rapid cladogenesis early in crown bird evolutionary history (specifically, the interval immediately following the end-Cretaceous mass extinction). At face value this hypothesis enjoys support from the crown bird fossil record, which documents the first appearances of most major crown bird lineages in the early Cenozoic—in line with a model of rapid post-extinction niche filling among surviving avian lineages. However, molecular-clock analyses have yielded strikingly variable estimates for the age of crown birds, and conflicting inferences on the impact of the end-Cretaceous mass extinction on the extant bird radiation. This uncertainty has often been ascribed to a patchy avian fossil record, but the possibility of model misspecification in molecular divergence time analyses represents an important and relatively underexplored alternative hypothesis. Here, we highlight the necessity of further developing and using models that account for coordinated variation in rates of molecular evolution across a phylogeny (e.g. molecular early bursts) as a means of assessing support for a rapid post-Cretaceous radiation of crown birds. We discuss how relationships between life-history and substitution rates can mislead divergence time studies that do not account for directional changes in substitution rates over time, and suggest that these effects might have caused some of the variation in existing molecular date estimates for birds. We suggest multiple paths forward that could help resolve this and similar conflicts within other major eukaryotic clades.


2018 ◽  
Author(s):  
Matthew J Phillips ◽  
Carmelo Fruciano

AbstractRecent 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. 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. 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.


2020 ◽  
Vol 36 (Supplement_2) ◽  
pp. i884-i894
Author(s):  
Jose Barba-Montoya ◽  
Qiqing Tao ◽  
Sudhir Kumar

Abstract Motivation As the number and diversity of species and genes grow in contemporary datasets, two common assumptions made in all molecular dating methods, namely the time-reversibility and stationarity of the substitution process, become untenable. No software tools for molecular dating allow researchers to relax these two assumptions in their data analyses. Frequently the same General Time Reversible (GTR) model across lineages along with a gamma (+Γ) distributed rates across sites is used in relaxed clock analyses, which assumes time-reversibility and stationarity of the substitution process. Many reports have quantified the impact of violations of these underlying assumptions on molecular phylogeny, but none have systematically analyzed their impact on divergence time estimates. Results We quantified the bias on time estimates that resulted from using the GTR + Γ model for the analysis of computer-simulated nucleotide sequence alignments that were evolved with non-stationary (NS) and non-reversible (NR) substitution models. We tested Bayesian and RelTime approaches that do not require a molecular clock for estimating divergence times. Divergence times obtained using a GTR + Γ model differed only slightly (∼3% on average) from the expected times for NR datasets, but the difference was larger for NS datasets (∼10% on average). The use of only a few calibrations reduced these biases considerably (∼5%). Confidence and credibility intervals from GTR + Γ analysis usually contained correct times. Therefore, the bias introduced by the use of the GTR + Γ model to analyze datasets, in which the time-reversibility and stationarity assumptions are violated, is likely not large and can be reduced by applying multiple calibrations. Availability and implementation All datasets are deposited in Figshare: https://doi.org/10.6084/m9.figshare.12594638.


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