Stochastic Character Mapping of State-Dependent Diversification Reveals the Tempo of Evolutionary Decline in Self-Compatible Onagraceae Lineages

Abstract

A major goal of evolutionary biology is to identify key evolutionary transitions that correspond with shifts in speciation and extinction rates. Stochastic character mapping has become the primary method used to infer the timing, nature, and number of character state transitions along the branches of a phylogeny. The method is widely employed for standard substitution models of character evolution. However, current approaches cannot be used for models that specifically test the association of character state transitions with shifts in diversification rates such as state-dependent speciation and extinction (SSE) models. Here we introduce a new stochastic character mapping algorithm that overcomes these limitations, and apply it to study mating system evolution over a time-calibrated phylogeny of the plant family Onagraceae. Utilizing a hidden state SSE model we tested the association of the loss of self-incompatibility with shifts in diversification rates. We found that self-compatible lineages have higher extinction rates and lower net-diversification rates compared to self-incompatible lineages. Furthermore, these results provide empirical evidence for the "senescing" diversification rates predicted in highly selfing lineages: our mapped character histories show that the loss of self-incompatibility is followed by a short-term spike in speciation rates, which declines after a time lag of several million years resulting in negative net-diversification. Lineages that have long been self-compatible, such as Fuchsia and Clarkia, are in a previously unrecognized and ongoing evolutionary decline. Our results demonstrate that stochastic character mapping of SSE models is a powerful tool for examining the timing and nature of both character state transitions and shifts in diversification rates over the phylogeny..

Hybridizing salamanders experience accelerated diversification

“…That being said, averaged extinction rates across all analyses for hybridizing and non-hybridizing taxa led to more reasonable waiting times of 127.9 and 54.2 MY respectively. Further, recent studies have documented even more negative net-diversification rates than inferred herein 105 . Taken together, it appears that extinction plays an important role in the diversification of salamanders, leading to a reduction in net-diversification rates towards the present relative to hybridizing species.…”

Technical comment on Condamine et al. (2019): a cautionary note for users of linear diversification dependencies

“…While negative net diversification rates ( r = λ–µ) are plausible under certain circumstances (e.g. evolutionary dead ends; Freyman & Höhna 2019 and references therein), negative speciation or extinction rates make little sense biologically. For this latter reason, the RPANDA fit_bd function uses absolute values for the computation, no matter what kind of function is specified (H. Morlon, personal communication).…”

The ancestral population size conditioned on the reconstructed phylogenetic tree with occurrence data

“…The challenge here boils down to dealing with an increase of dimensionality, where we would be interested in the joint distribution of subpopulation sizes. Recent work by Freyman and Höhna (2018) could first allow us to find the distribution of the types along sampled lineages in the tree. If we have j types, we would then be interested in…”