How Well Can We Detect Shifts in Rates of Lineage Diversification? A Simulation Study of Sequential AIC Methods

Abstract

Evolutionary biologists have long been fascinated by the extreme differences in species numbers across branches of the Tree of Life. This has motivated the development of statistical phylogenetic methods for detecting shifts in the rate of lineage diversification (speciation - extinction). One of the most frequently used methods--implemented in the program MEDUSA--explores a set of diversification-rate models, where each model uniquely assigns branches of the phylogeny to a set of one or more diversification-rate categories. Each candidate model is first fit to the data, and the Akaike Information Criterion (AIC) is then used to identify the optimal diversification model. Surprisingly, the statistical behavior of this popular method is completely unknown, which is a concern in light of the poor performance of the AIC as a means of choosing among models in other phylogenetic comparative contexts, and also because of the ad hoc algorithm used to visit models. Here, we perform an extensive simulation study demonstrating that, as implemented, MEDUSA (1) has an extremely high Type I error rate (on average, spurious diversification-rate shifts are identified 42% of the time), and (2) provides severely biased parameter estimates (on average, estimated net-diversification and relative-extinction rates are 183% and 20% of their true values, respectively). We performed simulation experiments to reveal the source(s) of these pathologies, which include (1) the use of incorrect critical thresholds for model selection, and (2) errors in the likelihood function. Understanding the statistical behavior of MEDUSA is critical both to empirical researchers--in order to clarify whether these methods can reliably be applied to empirical datasets--and to theoretical biologists--in order to clarify whether new methods are required, and to reveal the specific problems that need to be solved in order to develop more reliable approaches for detecting shifts in the rate of lineage diversification.