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      Comparison of Bayesian Coalescent Skyline Plot Models for Inferring Demographic Histories

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          Abstract

          Bayesian coalescent skyline plot models are widely used to infer demographic histories. The first (non-Bayesian) coalescent skyline plot model assumed a known genealogy as data, while subsequent models and implementations jointly inferred the genealogy and demographic history from sequence data, including heterochronous samples. Overall, there exist multiple different Bayesian coalescent skyline plot models which mainly differ in two key aspects: (i) how changes in population size are modeled through independent or autocorrelated prior distributions, and (ii) how many change-points in the demographic history are used, where they occur and if the number is pre-specified or inferred. The specific impact of each of these choices on the inferred demographic history is not known because of two reasons: first, not all models are implemented in the same software, and second, each model implementation makes specific choices that the biologist cannot influence. To facilitate a detailed evaluation of Bayesian coalescent skyline plot models, we implemented all currently described models in a flexible design into the software RevBayes. Furthermore, we evaluated models and choices on an empirical dataset of horses supplemented by a small simulation study. We find that estimated demographic histories can be grouped broadly into two groups depending on how change-points in the demographic history are specified (either independent of or at coalescent events). Our simulations suggest that models using change-points at coalescent events produce spurious variation near the present, while most models using independent change-points tend to over-smooth the inferred demographic history.

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          Most cited references37

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          Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10

          Abstract The Bayesian Evolutionary Analysis by Sampling Trees (BEAST) software package has become a primary tool for Bayesian phylogenetic and phylodynamic inference from genetic sequence data. BEAST unifies molecular phylogenetic reconstruction with complex discrete and continuous trait evolution, divergence-time dating, and coalescent demographic models in an efficient statistical inference engine using Markov chain Monte Carlo integration. A convenient, cross-platform, graphical user interface allows the flexible construction of complex evolutionary analyses.
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            Inference of Human Population History From Whole Genome Sequence of A Single Individual

            The history of human population size is important to understanding human evolution. Various studies 1-5 have found evidence for a founder event (bottleneck) in East Asian and European populations associated with the human dispersal out-of-Africa event around 60 thousand years ago (kya) before present. However, these studies have to assume simplified demographic models with few parameters and do not precisely date the start and stop times of the bottleneck. Here, with fewer assumptions on population size changes, we present a more detailed history of human population sizes between approximately ten thousand to a million years ago, using the pairwise sequentially Markovian coalescent (PSMC) model applied to the complete diploid genome sequences of a Chinese male (YH) 6 , a Korean male (SJK) 7 , three European individuals (Venter 8 , NA12891 and NA12878 9 ) and two Yoruba males (NA18507 10 and NA19239). We infer that European and Chinese populations had very similar population size histories before 10–20kya. Both populations experienced a severe bottleneck between 10–60kya while African populations experienced a milder bottleneck from which they recovered earlier. All three populations have an elevated effective population size between 60–250kya, possibly due to a population structure 11 . We also infer that the differentiation of genetically modern humans may have started as early as 100–120kya 12 , but considerable genetic exchanges may still have occurred until 20–40kya.
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              Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty.

              Recent developments in marginal likelihood estimation for model selection in the field of Bayesian phylogenetics and molecular evolution have emphasized the poor performance of the harmonic mean estimator (HME). Although these studies have shown the merits of new approaches applied to standard normally distributed examples and small real-world data sets, not much is currently known concerning the performance and computational issues of these methods when fitting complex evolutionary and population genetic models to empirical real-world data sets. Further, these approaches have not yet seen widespread application in the field due to the lack of implementations of these computationally demanding techniques in commonly used phylogenetic packages. We here investigate the performance of some of these new marginal likelihood estimators, specifically, path sampling (PS) and stepping-stone (SS) sampling for comparing models of demographic change and relaxed molecular clocks, using synthetic data and real-world examples for which unexpected inferences were made using the HME. Given the drastically increased computational demands of PS and SS sampling, we also investigate a posterior simulation-based analogue of Akaike's information criterion (AIC) through Markov chain Monte Carlo (MCMC), a model comparison approach that shares with the HME the appealing feature of having a low computational overhead over the original MCMC analysis. We confirm that the HME systematically overestimates the marginal likelihood and fails to yield reliable model classification and show that the AICM performs better and may be a useful initial evaluation of model choice but that it is also, to a lesser degree, unreliable. We show that PS and SS sampling substantially outperform these estimators and adjust the conclusions made concerning previous analyses for the three real-world data sets that we reanalyzed. The methods used in this article are now available in BEAST, a powerful user-friendly software package to perform Bayesian evolutionary analyses.
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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                Mol Biol Evol
                Mol Biol Evol
                molbev
                Molecular Biology and Evolution
                Oxford University Press (UK )
                0737-4038
                1537-1719
                May 2024
                17 April 2024
                17 April 2024
                : 41
                : 5
                : msae073
                Affiliations
                GeoBio-Center, Ludwig-Maximilians-Universität München , Munich 80333, Germany
                Department of Earth and Environmental Sciences, Paleontology & Geobiology, Ludwig-Maximilians-Universität München , Munich 80333, Germany
                GeoBio-Center, Ludwig-Maximilians-Universität München , Munich 80333, Germany
                Department of Earth and Environmental Sciences, Paleontology & Geobiology, Ludwig-Maximilians-Universität München , Munich 80333, Germany
                Author notes
                Corresponding author: E-mail: sebastian.hoehna@ 123456gmail.com .
                Author information
                https://orcid.org/0009-0003-1812-4212
                https://orcid.org/0000-0001-6519-6292
                Article
                msae073
                10.1093/molbev/msae073
                11068272
                38630635
                1d8bc989-9672-4fa7-865d-8574e69b8903
                © The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 26 September 2023
                : 16 February 2024
                : 01 April 2024
                : 03 May 2024
                Page count
                Pages: 14
                Funding
                Funded by: Deutsche Forschungsgemeinschaft, DOI 10.13039/501100001659;
                Award ID: HO 6201/1–1
                Award ID: HO 6201/2-1
                Categories
                Methods
                AcademicSubjects/SCI01130
                AcademicSubjects/SCI01180

                Molecular biology
                demographic histories,coalescent,heterochronous samples,revbayes
                Molecular biology
                demographic histories, coalescent, heterochronous samples, revbayes

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