Links between prey assemblages and poison frog toxins: a landscape ecology approach to assess how biotic interactions affect species phenotypes

Ecological studies of species pairs showed that biotic interactions promote phenotypic change and eco-evolutionary feedbacks. However, it is unclear how phenotypes respond to synergistic interactions with multiple taxa. We investigate whether interactions with multiple prey species explain spatially structured variation in the skin toxins of the Neotropical poison frog Oophaga pumilio. Specifically, we assess how dissimilarity (i.e., beta diversity) of alkaloid-bearing arthropod prey assemblages (68 ant species) and evolutionary divergence between frog populations (from a neutral genetic marker) contribute to frog poison dissimilarity (toxin profiles composed of 230 different lipophilic alkaloids sampled from 934 frogs at 46 sites). We find that models that incorporate spatial turnover in the composition of ant assemblages explain part of the frog alkaloid variation, and we infer unique alkaloid combinations across the range of O. pumilio. Moreover, we find that alkaloid variation increases weakly with the evolutionary divergence between frog populations. The analytical framework proposed here can be extended to other multi-trophic systems, coevolutionary mosaics, microbial assemblages, and ecosystem services.

针对物种类对的生态学研究表明，生物交互作用可推动表型变化与生态-进化反馈环。然而目前尚不清楚，表型如何响应多类群间的协同交互作用。本研究旨在探究，与多种猎物物种的交互作用能否解释新热带毒蛙（Oophaga pumilio）皮肤毒素的空间结构变异。具体而言，本研究评估了含生物碱的节肢动物猎物群落（涵盖68种蚂蚁）的相异性（即β多样性（beta diversity））、蛙类种群间的进化分化（基于中性遗传标记），如何共同影响蛙类毒素的相异性——该毒素谱由46个采样点的934只蛙类体内的230种不同脂溶性生物碱构成。研究结果显示，纳入蚂蚁群落组成空间周转的模型，可解释部分蛙类生物碱变异；同时我们推断，在O. pumilio的分布范围内存在独特的生物碱组合。此外，我们发现蛙类种群间的进化分化程度与生物碱变异呈微弱正相关。本研究提出的分析框架，可推广应用于其他多营养级系统、协同进化镶嵌体、微生物群落以及生态系统服务研究。