Tradeoffs in the evolution of plant farming by ants

Tradeoffs in the evolution of plant farming by ants
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DOI:
10.1073/pnas.1919611117
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发表时间:
2020-01
期刊:
Proceedings of the National Academy of Sciences
影响因子:
--
通讯作者:
G. Chomicki;G. Kadereit;S. Renner;Toby Kiers
G. Chomicki;G. Kadereit;S. Renner;Toby Kiers
中科院分区:
其他
文献类型:
--
作者:
G. Chomicki;G. Kadereit;S. Renner;Toby Kiers

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在人类的种植系统中,农民越来越多地使用技术来收集数据,以评估不同(有时是冲突的)作物需求之间的权衡,以最大限度地提高产量。一些社会性昆虫也进化出了农业实践,但尚不清楚它们如何评估当地条件以平衡相互冲突的作物需求。在斐济热带雨林中蚂蚁和植物之间的专性农业共生关系中,我们展示了蚂蚁农民如何在作物种植中也面临关键的权衡。虽然蚂蚁不能同时最大限度地提高对作物的所有服务,但我们的工作表明,它们在强光条件下种植作物,以最大限度地提高花卉食物的回报,尽管这种策略的氮成本。作物权衡的评估在农业战略的演变中起着关键作用。在生命之树上,已经进化出了各种各样的耕作形式。高效耕作要求农民理解并积极促进提高作物产量的条件。对于植物栽培,这可以包括评估光、营养和保护免受食草动物侵害之间的权衡。目前还不清楚非人类农民是否或如何评估当地条件以增加收益。在这里,我们解决这个问题,使用专性的农业互惠互利之间的蚂蚁Philidris Nagasau和附生植物的属Squamellaria的种植,为他们的筑巢地点和花卉的奖励。我们关注的是蚂蚁对农作物的积极施肥以及它们对食草动物的保护。我们发现,蚂蚁受益于在阳光充足的情况下种植植物,与在阴凉处种植的植物相比,它们获得的花卉食物奖励是在阳光充足的情况下种植的植物的7.5倍。较高的奖励水平与蚂蚁提供的较高水平的作物保护相关。然而,虽然高光种植产生了最大的直接食物回报,但阳光种植的作物比阴影种植的作物含有更少的氮。这是由于较低的氮输入从蚂蚁喂养花的奖励,而不是昆虫蛋白质获得捕食。尽管有这种权衡,农业蚂蚁通过选择性地在阳光充足的地方种植作物来优化作物产量。这一蚂蚁-植物分支的祖先状态重建表明,全日照农业策略已经存在了数百万年,这表明非人类农民已经进化出评估和平衡相互冲突的作物需求的方法,以使自己受益。
Significance In human cultivation systems, farmers increasingly use technology to gather data for evaluating tradeoffs between diverse—and sometimes conflicting—crop requirements to maximize yield. Some social insects have also evolved agricultural practices, but it is unknown how they evaluate local conditions to balance conflicting crop requirements. In the obligate farming symbiosis between ants and plants in Fijian rainforests, we show how ant farmers also face key tradeoffs in crop cultivation. While ants cannot simultaneously maximize all services to their crops, our work demonstrates that they cultivate crops in high-light conditions to maximize floral food rewards, despite the nitrogen costs of this strategy. Evaluation of crop tradeoffs plays a key role in the evolution of farming strategies. Diverse forms of cultivation have evolved across the tree of life. Efficient farming requires that the farmer deciphers and actively promotes conditions that increase crop yield. For plant cultivation, this can include evaluating tradeoffs among light, nutrients, and protection against herbivores. It is not understood if, or how, nonhuman farmers evaluate local conditions to increase payoffs. Here, we address this question using an obligate farming mutualism between the ant Philidris nagasau and epiphytic plants in the genus Squamellaria that are cultivated for their nesting sites and floral rewards. We focused on the ants’ active fertilization of their crops and their protection against herbivory. We found that ants benefited from cultivating plants in full sun, receiving 7.5-fold more floral food rewards compared to shade-cultivated plants. The higher reward levels correlated with higher levels of crop protection provided by the ants. However, while high-light planting yielded the greatest immediate food rewards, sun-grown crops contained less nitrogen compared to shade-grown crops. This was due to lower nitrogen input from ants feeding on floral rewards instead of insect protein gained from predation. Despite this tradeoff, farming ants optimize crop yield by selectively planting their crops in full sun. Ancestral state reconstructions across this ant–plant clade show that a full-sun farming strategy has existed for millions of years, suggesting that nonhuman farmers have evolved the means to evaluate and balance conflicting crop needs to their own benefit.