Life history trait divergence among populations of a non-palatable species reveals strong non-trophic indirect effects of an abundant herbivore

When large herbivores exert selection on their prey plant species, co-occurring, non-prey species may experience selection through non-trophic indirect effects. Such selection is likely common where herbivores are overabundant. Yet, empirical studies of non-trophic indirect effects as drivers of non-prey trait evolution are lacking. Here we test for adaptive shifts in life history traits in an unpalatable species, Arisaema triphyllum, a common forest perennial that is unique because it exhibits size-dependent sex switching. We collected A. triphyllum from six sites that experience a gradient in abiotic stress caused by deer browse pressure on prey plant species that generate indirect effects. We grew A. triphyllum from these sites in a common garden for five years to evaluate life history predictions linking strong indirect effects and abiotic stress to changes in life history traits: flowering onset size threshold, female flowering size threshold, relative growth rate (RGR), biomass allocation, and asexual reproduction. Despite observed differences among phenotypes in the field, expression of flowering onset size threshold, biomass allocation, and asexual reproduction did not differ among the six populations in the garden, indicating common plastic responses. In contrast, A. triphyllum collected from sites experiencing the two highest deer impacts exhibited smaller female flowering size thresholds and the highest RGR. Responses in these traits support the predictions of adaptive divergence in response to indirect effects. Our results reinforce the idea that non-trophic indirect effects of large herbivores can elicit evolutionary responses in some traits of non-prey species. In general, life history traits of unpalatable species may be cryptically adapting to stressful indirect effects where large herbivores are overabundant.

当大型草食动物对其猎食植物物种施加选择压力时，共存的非猎食物种可能会通过非营养级间接效应受到选择作用。在大型草食动物种群过剩的区域，这类选择作用大概率普遍存在。然而，目前尚缺乏以非营养级间接效应为驱动因子、探究非猎食物种性状演化的实证研究。本研究针对一种具备独特体型依赖性性别转换特性的常见森林多年生草本——非适口物种三叶天南星（Arisaema triphyllum）的生活史性状适应性变化展开检验。我们从六个样地采集了三叶天南星样本，这些样地的非生物胁迫梯度由鹿类对猎食植物的取食压力所介导，进而产生间接效应。我们将采自各样地的三叶天南星置于同质园环境中培育五年，以验证相关生活史预测假说：即强间接效应与非生物胁迫会驱动下述生活史性状发生改变：开花起始体型阈值、雌性开花体型阈值、相对生长率（Relative Growth Rate, RGR）、生物量分配以及无性繁殖。尽管野外观测到不同表型间存在显著差异，但在同质园实验中，六个种群的开花起始体型阈值、生物量分配与无性繁殖性状的表达并无显著差异，这表明上述性状存在普遍的可塑性响应。与之形成鲜明对比的是，采自鹿类干扰程度最高的两个样地的三叶天南星，其雌性开花体型阈值更小，且相对生长率更高。这类性状响应契合间接效应驱动的适应性分化预测。本研究结果佐证了这一观点：大型草食动物的非营养级间接效应可引发非猎食物种部分性状的演化响应。总体而言，在大型草食动物种群过剩的区域，非适口物种的生活史性状可能正隐秘地适应这类胁迫性间接效应。