Test of biotic and abiotic correlates of latitudinal variation in defences in the perennial herb Ruellia nudiflora

1. Geographic variation in abiotic factors and species interactions is widespread and is hypothesized to generate concomitant patterns of species trait variation. For example, higher rates of herbivory at lower latitudes are thought to select for increased plant defences, although latitudinal variation in defences may also be influenced directly by abiotic factors and indirectly by predators and parasitoids reducing herbivore pressure. 2. We measured defences of the herb Ruellia nudiflora among 30 populations spanning a latitudinal gradient from northern Yucatan to southern Belize that vary substantially in leaf herbivory (four-fold), seed herbivory (25-fold), and seed herbivore parasitism (14-fold). These surveyed populations span one-third of the species’ latitudinal distribution (5° of latitude), the entire precipitation gradient of its distribution, and one-third of the temperature gradient of its distribution. Our prior work showed that leaf herbivory decreased with latitude and that seed herbivory increased with latitude. Here, we measured leaf trichome density and leaf and seed phenolics and tested whether latitudinal variation in climate, herbivory, and parasitism explained latitudinal variation in these defensive traits. 3. Patterns of variation in leaf trichomes fully supported predictions, with trichome density increasing with a parallel increase in herbivory towards lower latitudes. While seed phenolics were positively associated with herbivory, and seed herbivory tended to increase with latitude, the predicted (positive) association between latitude and defence was not detectable. There was no detectable association between parasitoids and seed defences. In addition, the association between leaf herbivory and phenolics was weak, and leaf phenolics were not associated with latitude. Importantly, variation in the abiotic environment was associated with plant defence, indicating that abiotic factors can play a major role in shaping plant defences, independently of herbivory. 4. Synthesis: Latitudinal variation in abiotic factors may drive concomitant patterns of variation in plant defences, independently of herbivory. Collectively, these findings highlight the need for assessing geographic variation in plant defences from a multi-factorial perspective, testing for the simultaneous influence of biotic and abiotic factors.

1. 非生物因子（abiotic factors）与物种相互作用（species interactions）的地理分化普遍存在，学界据此推测其会引发物种性状变异的协同格局。例如，低纬度地区更高的植食作用（herbivory）发生率被认为会筛选出更强的植物防御（plant defences）能力；尽管防御性状的纬度变异也可能直接受非生物因子调控，也可通过捕食者与寄生天敌（parasitoids）降低植食压力的间接途径产生影响。
2. 本研究针对从尤卡坦半岛北部至伯利兹南部的纬度梯度（latitudinal gradient）上的30个蓝花草（Ruellia nudiflora）种群开展防御性状测定：这些种群的叶片植食率（leaf herbivory）（差异达4倍）、种子植食率（seed herbivory）（差异达25倍）以及种子植食者（seed herbivore）寄生率（parasitism）（差异达14倍）均存在显著分化。所调查的种群覆盖了该物种纬度分布范围的三分之一（跨度5°纬度）、其分布区内完整的降水梯度，以及三分之一的温度梯度。前期研究已证实，叶片植食率随纬度升高而降低，而种子植食率则随纬度升高而升高。本研究测定了叶片毛状体密度（leaf trichome density）、叶片与种子中的酚类物质（phenolics）含量，并检验了气候、植食作用与寄生作用的纬度变异是否能够解释这些防御性状的纬度分化格局。
3. 叶片毛状体的变异格局完全符合研究预期：随着向低纬度地区推进，植食作用水平同步升高，叶片毛状体密度也随之增加。尽管种子酚类物质含量与植食作用呈正相关，且种子植食率随纬度升高呈升高趋势，但理论预期的纬度与防御性状间的（正向）关联并未被检测到。寄生天敌与种子防御之间未发现显著关联。此外，叶片植食率与酚类物质含量的关联较弱，且叶片酚类物质含量与纬度并无关联。值得注意的是，非生物环境的变异与植物防御性状显著相关，这表明非生物因子可在不依赖植食作用的前提下，对植物防御性状的塑造发挥关键作用。
4. 结论：非生物因子的纬度变异可在不依赖植食作用的前提下，驱动植物防御性状的协同变异格局。综上，本研究结果表明，评估植物防御性状的地理分化时需采用多因子视角，同时检验生物因子（biotic factors）与非生物因子的协同影响。