Binary-state speciation and extinction method is conditionally robust to realistic violations of its assumptions

Background: Phylogenetic comparative methods allow us to test evolutionary hypotheses without the benefit of an extensive fossil record. These methods, however, make simplifying assumptions, among them that clades are always increasing or stable in diversity, an assumption we know to be false. This study simulates hypothetical clades to test whether the Binary State Speciation and Extinction (BiSSE) method can be used to correctly detect relative differences in diversification rate between ancestral and derived character states even as net diversification rates are declining overall. We simulate clades with declining but positive diversification rates, as well those in which speciation rates decline below extinction rates so that they are losing richness for part of their history. We run these analyses both with simulated symmetric and asymmetric speciation rates to test whether BiSSE can be used to detect them correctly.
Results: For simulations with a neutral character, the fit for a BiSSE model with a neutral character is better than alternative models so long as net diversification rates remain positive. Once net diversification rates become negative, the BiSSE model with the greatest likelihood often has a non-neutral character, even though there is no such character in the simulation. BiSSE's usefulness in detecting real asymmetry in speciation rates improves with clade age, even well after net diversification rates have become negative.
Conclusions: BiSSE is most useful in analyzing clades of intermediate age, before they have reached peak diversity and gone into decline. After this point, users of BiSSE risk incorrectly inferring differential evolutionary rates when none exist. Fortunately, most studies using BiSSE and similar models focus on rapid, recent diversifications, and are less likely to encounter the biases BiSSE models are subject to for older clades. For extant groups that were once more diverse than now, however, caution should be taken in inferring past diversification patterns without fossil data.

背景：系统发育比较方法（Phylogenetic comparative methods）使我们能够在缺乏大量化石记录的情况下检验演化假说。然而，这类方法会做出若干简化假设，其中一项假设认为演化支的多样性始终处于增长或稳定状态，而我们已知该假设并不成立。本研究通过模拟假想演化支系，旨在检验二元性状物种形成与灭绝（Binary State Speciation and Extinction, BiSSE）方法是否能够在支系整体净多样化速率下降的情况下，正确检测祖先与衍生性状状态间的多样化速率相对差异。本研究模拟了两类演化支系：一类拥有持续下降但仍为正值的多样化速率，另一类的物种形成速率下降至低于灭绝速率，导致其在部分演化历史中类群丰富度不断降低。此外，我们分别在模拟对称与非对称物种形成速率的场景下开展分析，以检验BiSSE方法能否正确检测此类差异。
结果：对于中性性状模拟场景，只要净多样化速率仍为正值，带中性性状的BiSSE模型的拟合效果均优于备选模型。一旦净多样化速率变为负值，似然值最高的BiSSE模型往往会被推断为带有非中性性状，而模拟过程中实际上并不存在此类性状。随着演化支系时长增加，BiSSE检测真实物种形成速率非对称性的能力会有所提升，即使在净多样化速率变为负值之后亦是如此。
结论：BiSSE方法在分析中等演化时长的支系时效果最佳，这类支系尚未达到多样性峰值并进入衰退阶段。在此之后，使用BiSSE方法的研究者可能会错误推断出不存在的差异化演化速率。值得庆幸的是，多数使用BiSSE及类似模型的研究聚焦于快速发生的近期多样化事件，因此较少会遇到针对古老支系的BiSSE模型偏倚问题。但对于那些曾经比现今更为多样的现存类群而言，在缺乏化石数据的情况下推断过去的多样化模式时，研究者应当格外谨慎。