Rates of niche and phenotype evolution lag behind diversification in a temperate radiation

Environmental change can create opportunities for increased rates of lineage diversification, but continued species accumulation has been hypothesized to lead to slowdowns via competitive exclusion and niche partitioning. Such density-dependent models imply tight linkages between diversification and trait evolution, but there are plausible alternative models. Little is known about the association between diversification and key ecological and phenotypic traits at broad phylogenetic and spatial scales. Do trait evolutionary rates coincide with rates of diversification, are there lags among these rates, or is diversification niche-neutral? To address these questions, we combine a deeply sampled phylogeny for a major flowering plant clade-Saxifragales-with phenotype and niche data to examine temporal patterns of evolutionary rates. The considerable phenotypic and habitat diversity of Saxifragales is greatest in temperate biomes. Global expansion of these habitats since the mid-Miocene provided ecological opportunities that, with density-dependent adaptive radiation, should result in simultaneous rate increases for diversification, niche, and phenotype, followed by decreases with habitat saturation. Instead, these rates have significantly different timings, with increases in diversification occurring at the mid-Miocene Climatic Optimum (~15 mya), followed by increases in niche and phenotypic evolutionary rates by ~5 mya; all rates increase exponentially to the present. We attribute this surprising lack of temporal coincidence to initial niche-neutral diversification followed by ecological and phenotypic divergence coincident with more extreme cold and dry habitats that proliferated into the Pleistocene. A lack of density-dependence contrasts with investigations of other cosmopolitan lineages, suggesting alternative patterns may be common in the diversification of temperate lineages.

环境变化可为支系分化速率提升创造契机，但此前有假说提出，持续的物种积累会通过竞争排斥与生态位分区作用导致分化速率放缓。这类依赖种群密度的模型暗示分化与性状演化之间存在紧密关联，但也存在诸多合理的替代模型。目前学界对大系统发育与空间尺度下，分化速率与关键生态、表型性状之间的关联仍知之甚少。性状演化速率是否与分化速率同步？二者之间是否存在时间滞后？抑或是分化过程不受生态位调控（即生态位中性）？为解答上述问题，本研究结合被子植物主要支系——虎耳草目（Saxifragales）的深度采样系统发育树、表型与生态位数据，探究演化速率的时间变化模式。虎耳草目丰富的表型与生境多样性在温带生物群区中最为显著。自中新世中期以来，这类生境在全球范围内扩张，为物种分化提供了生态契机。若按照依赖种群密度的适应性辐射模型，分化、生态位与表型的演化速率应同步提升，随后随着生境饱和而下降。但本研究结果显示，这些速率的变化时序存在显著差异：分化速率在中新世中期气候最适宜期（约1500万年前）率先提升，生态位与表型演化速率则在约500万年前才随之上升；所有速率至今仍呈指数级增长。我们将这种令人意外的时序错位归因于：最初的分化过程为生态位中性模式，随后随着极端寒冷与干旱生境在更新世大规模扩张，生态位与表型才出现同步分化。这种不依赖种群密度的分化模式与其他广布支系的研究结果相悖，这表明替代演化模式可能在温带支系的分化过程中普遍存在。