Commonly used Bayesian diversification-rate models produce biologically meaningful differences on empirical phylogenies

Abstract

Identifying along which lineages shifts in diversification rates occur is a central goal of comparative phylogenetics; these shifts may coincide with key evolutionary events such as the development of novel morphological characters, the acquisition of adaptive traits, polyploidization or other structural genomic changes, or dispersal to a new habitat and subsequent increase in environmental niche space. However, while multiple methods now exist to estimate diversification rates and identify shifts using phylogenetic topologies, the appropriate use and accuracy of these methods is hotly debated. Here we test whether five Bayesian methods--Bayesian Analysis of Macroevolutionary Mixtures (BAMM), two implementations of the Lineage-Specific Birth-Death-Shift model (LSBDS and PESTO), the approximate Multi-Type Birth-Death model (MTBD; implemented in BEAST2), and the cladogenetic diversification rate shift model (CLaDS2)--produce comparable results. We apply each of these methods to a set of 65 empirical time-calibrated phylogenies and compare inferences of speciation rate, extinction rate, and net diversification rate. We find that the five methods often infer different speciation, extinction, and net-diversification rates. Consequently, these different estimates may lead to different interpretations of the macroevolutionary dynamics. The different estimates can be attributed to fundamental differences among the compared models. Therefore, the inference of shifts in diver-sification rates is strongly method-dependent. We advise biologists to apply multiple methods to test the robustness of the conclusions or to carefully select the method based on the validity of the underlying model assumptions to their particular empirical system. Lay SummaryUnderstanding why some groups of organisms have more species than others is key to understanding the origin of biodiversity. Theory and empirical evidence suggest that multiple distinct historical events--such as the evolution of particular morphological features (e.g., the flower, the tetrapod limb) and competition amongst species--can produce this pattern of divergent species richness. Identifying when and where on the tree of life shifts in diversification rates occur is important for explaining the origin of modern-day biodiversity and understanding how disparity among species evolves. Several statistical methods have been developed to infer diversification rates and identify these shifts. While these methods each attempt to make inferences about changes in the tempo of diversification, they differ in their underlying statistical models and assumptions. Here we test if these methods draw similar conclusions using a dataset of 65 time-calibrated phylogenies from across multicellular life. We find that inferences of where rate shifts occur strongly depends on the chosen method. Therefore, biologists should choose the model whose assumptions they believe to be the most valid and justify their model choice a priori, or consider using several independent methods to test an evolutionary hypothesis.