Inferring speciation and extinction rates under different sampling schemes
Open accessAbstract
The birth-death process is widely used in phylogenetics to model speciation and extinction. Recent studies have shown that the inferred rates are sensitive to assumptions about the sampling probability of lineages. Here, we examine the effect of the method used to sample lineages. Whereas previous studies have assumed random sampling (RS), we consider two extreme cases of biased sampling: "diversified sampling" (DS), where tips are selected to maximize diversity and "cluster sampling (CS)," where sample diversity is minimized. DS appears to be standard practice, for example, in analyses of higher taxa, whereas CS may occur under special circumstances, for example, in studies of geographically defined floras or faunas. Using both simulations and analyses of empirical data, we show that inferred rates may be heavily biased if the sampling strategy is not modeled correctly. In particular, when a diversified sample is treated as if it were a random or complete sample, the extinction rate is severely underestimated, often close to 0. Such dramatic errors may lead to serious consequences, for example, if estimated rates are used in assessing the vulnerability of threatened species to extinction. Using Bayesian model testing across 18 empirical data sets, we show that DS is commonly a better fit to the data than complete, random, or cluster sampling (CS). Inappropriate modeling of the sampling method may at least partly explain anomalous results that have previously been attributed to variation over time in birth and death rates.
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At least two additional sources of uncertainty not studied here are uncertainty introduced by the birth-death time prior and its failure to accommodate diversified sampling of species in phylogenies, and uncertainty due to the substitution model, which may have an important effect when estimating branch lengths in ancient phylogenies.
“The situation is compounded by at least two additional sources of uncertainty that we did not study here: uncertainty introduced by the birth-death time prior, and its failure to accommodate diversified sampling of species in phylogenies [65], and uncertainty due to the substitution model, which may have an important effect when estimating branch lengths in ancient phylogenies [66, 67].”
From Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales (2015) · cites this paper as [65]
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Cites
Equation of State Calculations by Fast Computing Machines
Metropolis, N., Rosenbluth, A. W., Rosenbluth, M. N., Teller, A. H., & Teller, E. (1953) · The Journal of Chemical Physics · doi:10.1063/1.1699114 · Cited by 37,192 · see citing works
An introduction to probability theory and its applications
(1958) · Journal of the Franklin Institute · doi:10.1016/0016-0032(58)90688-4 · Cited by 29,620 · see citing works
A Simplex Method for Function Minimization
Nelder, J. A., & Mead, R. (1965) · The Computer Journal · doi:10.1093/comjnl/7.4.308 · Cited by 28,905 · see citing works
Monte Carlo sampling methods using Markov chains and their applications.
Hastings, W. K. (1970) · Biometrika · doi:10.1093/biomet/57.1.97 · Cited by 15,195 · see citing works
CODA: convergence diagnosis and output analysis for MCMC
Plummer, M., Best, N., Cowles, K., & Vines, K. (2006) · Open Research Online (The Open University) · Cited by 3,317 · see citing works
Probability Distribution of Molecular Evolutionary Trees: A New Method of Phylogenetic Inference
Rannala, B. H., & Yang, Z. (1996) · Journal of Molecular Evolution · doi:10.1007/bf02338839 · Cited by 1,751 · see citing works
Evaluating the Accuracy of Sampling-Based Approaches to the Calculation of Posterior Moments
Geweke, J. F. (1992) · doi:10.1093/oso/9780198522669.003.0010 · Cited by 1,526 · see citing works
Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo Method
Yang, Z., & Rannala, B. (1997) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025811 · Cited by 1,274 · see citing works
In all likelihood : statistical modelling and inference using likelihood
Pawitan, Y. (2001) · Cited by 1,068 · see citing works
The conditioned reconstructed process
Gernhard, T. (2008) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2008.04.005 · Cited by 1,049 · see citing works
On the Generalized "Birth-and-Death" Process
Kendall, D. G. (1948) · The Annals of Mathematical Statistics · doi:10.1214/aoms/1177730285 · Cited by 937 · see citing works
The reconstructed evolutionary process
Nee, S., May, R. M., & Harvey, P. (1994) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1994.0068 · Cited by 850 · see citing works
Testing macro–evolutionary models using incomplete molecular phylogenies
Pybus, O. G., & Harvey, P. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1278 · Cited by 802 · see citing works
Computing Bayes factors using thermodynamic integration.
Lartillot, N., & Philippe, H. (2006) · Systematic Biology · doi:10.1080/10635150500433722 · Cited by 668 · see citing works
EXTINCTION RATES SHOULD NOT BE ESTIMATED FROM MOLECULAR PHYLOGENIES
Rabosky, D. L. (2009) · Evolution · doi:10.1111/j.1558-5646.2009.00926.x · Cited by 595 · see citing works
Sampling-through-time in birth–death trees
Stadler, T. (2010) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2010.09.010 · Cited by 550 · see citing works
Self-citationStochastic Processes and Population Growth
Kendall, D. G. (1949) · Journal of the Royal Statistical Society Series B (Statistical Methodology) · doi:10.1111/j.2517-6161.1949.tb00032.x · Cited by 494 · see citing works
Estimating diversification rates from phylogenetic information
Ricklefs, R. E. (2007) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.06.013 · Cited by 493 · see citing works
Density-Dependent Cladogenesis in Birds
Phillimore, A. B., & Price, T. D. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060071 · Cited by 465 · see citing works
Rambaut, A. (2009) · Medical Entomology and Zoology · Cited by 427 · see citing works
Extinction rates can be estimated from molecular phylogenies
Nee, S., Holmes, E. C., May, R. M., & Harvey, P. (1994) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1994.0054 · Cited by 421 · see citing works
Diversity dynamics: molecular phylogenies need the fossil record
Quental, T. B., & Marshall, C. R. (2010) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2010.05.002 · Cited by 409 · see citing works
On incomplete sampling under birth–death models and connections to the sampling-based coalescent
Stadler, T. (2009) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2009.07.018 · Cited by 406 · see citing works
Self-citationStochastic Processes and Population Growth
Kendall, D. G. (1977) · Biomathematics · doi:10.1007/978-3-642-81046-6_52 · Cited by 396 · see citing works
EXPLOSIVE EVOLUTIONARY RADIATIONS: DECREASING SPECIATION OR INCREASING EXTINCTION THROUGH TIME?
Rabosky, D. L., & Lovette, I. J. (2008) · Evolution · doi:10.1111/j.1558-5646.2008.00409.x · Cited by 386 · see citing works
Birth-Death Models in Macroevolution
Nee, S. (2006) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.37.091305.110035 · Cited by 342 · see citing works
Harvey, P., May, R. M., & Nee, S. (1994) · Evolution · doi:10.1111/j.1558-5646.1994.tb01341.x · Cited by 238 · see citing works
Phylogenetic Approaches to the Study of Extinction
Purvis, A. (2008) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-063008-102010 · Cited by 228 · see citing works
Slowdowns in Diversification Rates from Real Phylogenies May Not be Real
Cusimano, N., & Renner, S. S. (2010) · Systematic Biology · doi:10.1093/sysbio/syq032 · Cited by 213 · see citing works
Held, V. (1989) · Ethics · doi:10.1086/293070 · Cited by 175 · see citing works
Tanaka, M. M., Francis, A. R., Luciani, F., & Sisson, S. A. (2006) · Genetics · doi:10.1534/genetics.106.055574 · Cited by 152 · see citing works
Green, R. F., & Thompson, E. A. (1977) · Biometrics · doi:10.2307/2529328 · Cited by 118 · see citing works
A critical branching process model for biodiversity
Aldous, D., & Popovic, L. (2005) · Advances in Applied Probability · doi:10.1239/aap/1134587755 · Cited by 108 · see citing works
Complex speciation of humans and chimpanzees
Wakeley, J. (2008) · Nature · doi:10.1038/nature06805 · Cited by 52 · see citing works
Phylogenetic Approaches to the Study of Extinction
Purvis, A. (2008) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.063008.102010 · Cited by 46 · see citing works
A Method for Investigating Relative Timing Information on Phylogenetic Trees
Ford, D., Matsen, F. A., IV, & Stadler, T. (2009) · Systematic Biology · doi:10.1093/sysbio/syp018 · Cited by 31 · see citing works
Self-citation
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Cited by
Sorted by citations
The fossilized birth-death process for coherent calibration of divergence-time estimates
Heath, T. A., Huelsenbeck, J. P., & Stadler, T. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1319091111 · Cited by 834 · see citing works
Self-citationA Total-Evidence Approach to Dating with Fossils, Applied to the Early Radiation of the Hymenoptera
Ronquist, F., Klopfstein, S., Vilhelmsen, L., Schulmeister, S., Murray, D. L., & Rasnitsyn, A. P. (2012) · Systematic Biology · doi:10.1093/sysbio/sys058 · Cited by 930 · see citing works
Self-citationUncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales
dos Reis, M., Thawornwattana, Y., Angelis, K., Telford, M. J., Donoghue, P. C. J., & Yang, Z. (2015) · Current Biology · doi:10.1016/j.cub.2015.09.066 · Cited by 471 · see citing works
Total-Evidence Dating under the Fossilized Birth–Death Process
Zhang, C., Stadler, T., Klopfstein, S., Heath, T. A., & Ronquist, F. (2016) · Systematic Biology · doi:10.1093/sysbio/syv080 · Cited by 419 · see citing works
Self-citationBayesian Total-Evidence Dating Reveals the Recent Crown Radiation of Penguins
Gavryushkina, A., Heath, T. A., Ksepka, D. T., Stadler, T., Welch, D., & Drummond, A. J. (2016) · Systematic Biology · doi:10.1093/sysbio/syw060 · Cited by 372 · see citing works
Self-citationBudd, G. E., & Mann, R. P. (2020) · Interface Focus · doi:10.1098/rsfs.2019.0110 · Cited by 54 · see citing works
Černý, D., Madzia, D., & Slater, G. J. (2021) · Systematic Biology · doi:10.1093/sysbio/syab045 · Cited by 51 · see citing works
- Authors
- Hohna, S., Stadler, T., Ronquist, F., & Britton, T.
- Affiliations
- ETH Zurich (CH)
- Swedish Museum of Natural History (SE)
- Stockholm University (SE)
- Venue
- Molecular Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-04-11
- Volume
- 28
- Issue
- 9
- Pages
- 2577-2589
- ISSN
- 0737-4038 (ISSN-L)
- 1537-1719
- OpenAlex
- W2180090668
- Cited by
- 160
- References
- 36
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 9 · 2023: 13 · 2022: 12 · 2021: 14 · 2020: 17 · 2019: 11 · 2018: 7 · 2017: 10 · 2016: 15 · 2015: 13 · 2014: 6 · 2013: 8 · 2012: 4
- FWCI
- 4.67
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Biology and Evolution (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Vetenskapsrådet
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant Diversity and Evolution
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- speciation rates, extinction rates, birth-death processes, cluster sampling, random sampling, sampling probability, phylogenetic inference
- MeSH terms
- Algorithms, Animals, Bayes Theorem, Birds, Computer Simulation, Models, Genetic, Phylogeny, Selection Bias, Genetic Speciation, Extinction, Biological
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