Department of Integrative Biology, University of California, Berkeley, 3040 Valley Life Sciences Building #3140, CA 94720, USA.
Division of Evolutionary Biology, Ludwig-Maximilians-Universität München, Geschwister-Scholl-Platz 1, 80539 Munich, Germany.
Syst Biol. 2019 May 1;68(3):505-519. doi: 10.1093/sysbio/syy078.
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. Herein, 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 (SI) with shifts in diversification rates. We found that self-compatible lineages have higher extinction rates and lower net-diversification rates compared with 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 SI 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.
进化生物学的主要目标是确定与物种形成和灭绝率变化相对应的关键进化转变。随机字符映射已成为推断系统发育分支上字符状态转变的时间、性质和数量的主要方法。该方法广泛用于字符进化的标准替代模型。然而，目前的方法不能用于专门测试特征状态转变与多样化率变化之间关联的模型，例如与状态相关的物种形成和灭绝（SSE）模型。在此，我们引入了一种新的随机字符映射算法，该算法克服了这些限制，并将其应用于研究植物家族柳叶菜科经过时间校准的系统发育中的交配系统进化。利用隐藏状态 SSE 模型，我们测试了自我不亲和性（SI）丧失与多样化率变化之间的关联。我们发现，与自我不亲和的谱系相比，自交亲和的谱系具有更高的灭绝率和更低的净多样化率。此外，这些结果为高度自交谱系中预测的“衰老”多样化率提供了经验证据：我们映射的特征历史表明，SI 的丧失伴随着短期的物种形成率上升，经过数百万年的时间滞后后下降，导致净多样化率为负。像芙蓉和克拉克氏凤仙花这样长期自交的谱系正处于以前未被认识到的和正在进行的进化衰退中。我们的结果表明，SSE 模型的随机字符映射是一种强大的工具，可用于检查系统发育上字符状态转变和多样化率变化的时间和性质。
