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Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous

Abstract

All inferences in comparative biology depend on accurate estimates of evolutionary relationships. Recent phylogenetic analyses have turned away from maximum parsimony towards the probabilistic techniques of maximum likelihood and bayesian Markov chain Monte Carlo (BMCMC). These probabilistic techniques represent a parametric approach to statistical phylogenetics, because their criterion for evaluating a topology—the probability of the data, given the tree—is calculated with reference to an explicit evolutionary model from which the data are assumed to be identically distributed. Maximum parsimony can be considered nonparametric, because trees are evaluated on the basis of a general metric—the minimum number of character state changes required to generate the data on a given tree—without assuming a specific distribution1. The shift to parametric methods was spurred, in large part, by studies showing that although both approaches perform well most of the time2, maximum parsimony is strongly biased towards recovering an incorrect tree under certain combinations of branch lengths, whereas maximum likelihood is not3,4,5,6. All these evaluations simulated sequences by a largely homogeneous evolutionary process in which data are identically distributed. There is ample evidence, however, that real-world gene sequences evolve heterogeneously and are not identically distributed7,8,9,10,11,12,13,14,15,16. Here we show that maximum likelihood and BMCMC can become strongly biased and statistically inconsistent when the rates at which sequence sites evolve change non-identically over time. Maximum parsimony performs substantially better than current parametric methods over a wide range of conditions tested, including moderate heterogeneity and phylogenetic problems not normally considered difficult.

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Figure 1: Likelihood-based methods are less accurate than maximum parsimony (MP) under heterogeneous conditions.
Figure 2: Parsimony outperforms likelihood over a wide range of heterotachous conditions.
Figure 3: Maximum parsimony is more accurate than likelihood methods when techniques to improve phylogenetic performance are used.
Figure 4: Poor maximum likelihood performance is due to assuming homogeneous branch lengths.

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Acknowledgements

We thank J. Conery for advice, support and programming advice. P. Phillips, R. DeSalle and S. Proulx provided comments and discussion. We benefited from discussions of mixed model methods with D. Zwickl. B.K. was supported by an NSF IGERT training grant in Evolution, Development and Genomics to the University of Oregon.

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Correspondence to Joseph W. Thornton.

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Kolaczkowski, B., Thornton, J. Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431, 980–984 (2004). https://doi.org/10.1038/nature02917

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