Testing the role of the Red Queen and Court Jester as drivers of the macroevolution of Apollo butterflies

In macroevolution, the Red Queen (RQ) model posits that biodiversity dynamics depend mainly on species-intrinsic biotic factors such as interactions among species or life-history traits, while the Court Jester (CJ) model states that extrinsic environmental abiotic factors have a stronger role. Until recently, a lack of relevant methodological approaches has prevented the unraveling of contributions from these two types of factors to the evolutionary history of a lineage. Here we take advantage of the rapid development of new macroevolution models that tie diversification rates to changes in paleoenvironmental (extrinsic) and/or biotic (intrinsic) factors. We inferred a robust and fully-sampled species-level phylogeny, as well as divergence times and ancestral geographic ranges, and related these to the radiation of Apollo butterflies (Parnassiinae) using both extant (molecular) and extinct (fossil/morphological) evidence. We tested whether their diversification dynamics are better explained by a RQ or CJ hypothesis, by assessing whether speciation and extinction were mediated by diversity-dependence (niche filling) and clade-dependent host-plant association (RQ) or by large-scale continuous changes in extrinsic factors such as climate or geology (CJ). For the RQ hypothesis, we found significant differences in speciation rates associated with different host-plants but detected no sign of diversity-dependence. For CJ, the role of Himalayan-Tibetan building was substantial for biogeography but not a driver of high speciation, while positive dependence between warm climate and speciation/extinction was supported by continuously varying maximum-likelihood models. We find that rather than a single factor, the joint effect of multiple factors (biogeography, species traits, environmental drivers, and mass extinction) is responsible for current diversity patterns, and that the same factor might act differently across clades, emphasizing the notion of opportunity. This study confirms the importance of the confluence of several factors rather than single explanations in modeling diversification within lineages.

在宏观进化（macroevolution）研究领域，红皇后（Red Queen, RQ）模型提出，生物多样性动态主要由物种内在的生物因素主导，例如物种间的相互作用或生活史特征；而弄臣（Court Jester, CJ）模型则主张，外在的环境非生物因素发挥着更为关键的作用。直至近年，由于缺乏适配的方法论手段，学界始终未能厘清这两类因素对某一演化支演化历史的具体贡献。本研究借助新近快速发展的宏观进化模型——这类模型将物种多样化速率与古环境（外在）及/或生物（内在）因素的变化建立关联——展开相关分析。我们重建了一套完整采样的稳健物种水平系统发育树，同时估算了类群的分化时间与祖先地理分布范围，并结合现存分子证据与灭绝类群的化石/形态学证据，将上述结果与绢蝶亚科（Parnassiinae）的辐射演化过程相关联。我们通过两类检验来评估绢蝶亚科的多样化动态更符合哪一种假说：一是评估物种形成与灭绝过程是否受多样性依赖（生态位填充）以及支系依赖的宿主植物关联所调控（对应红皇后假说）；二是评估其是否由气候、地质等外在因素的大规模连续变化所驱动（对应弄臣假说）。针对红皇后假说，我们发现不同宿主植物对应的物种形成速率存在显著差异，但未检测到多样性依赖的相关信号。对于弄臣假说，喜马拉雅-青藏高原隆升对绢蝶亚科的生物地理格局影响显著，但并未成为高物种形成速率的驱动因子；而基于连续变量的极大似然（maximum-likelihood）模型证实，温暖气候与物种形成、灭绝速率之间存在显著正相关关系。本研究发现，当前的生物多样性格局并非由单一因素所致，而是生物地理过程、物种性状、环境驱动因子以及大规模灭绝等多重因素的共同作用结果；且同一因素在不同演化支中可能发挥截然不同的作用，这凸显了演化机遇的核心概念。本研究证实，在建模演化支内的多样化过程时，综合多种因素的协同效应而非依赖单一解释，才更为科学合理。