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Research Article

Tradeoffs in the evolution of plant farming by ants

View ORCID ProfileGuillaume Chomicki, Gudrun Kadereit, View ORCID ProfileSusanne S. Renner, and E. Toby Kiers
PNAS first published January 21, 2020 https://doi.org/10.1073/pnas.1919611117
Guillaume Chomicki
aDepartment of Bioscience, Durham University, DH1 3LE Durham, United Kingdom;
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  • ORCID record for Guillaume Chomicki
  • For correspondence: guillaume.chomicki@gmail.com
Gudrun Kadereit
bInstitute of Molecular Physiology, University of Mainz, 55099 Mainz, Germany;
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Susanne S. Renner
cSystematic Botany and Mycology, Department of Biology, University of Munich, 80638 Munich, Germany;
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  • ORCID record for Susanne S. Renner
E. Toby Kiers
dDepartment of Ecological Science, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, Netherlands
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  1. Edited by Joan E. Strassmann, Washington University in St. Louis, St. Louis, MO, and approved December 18, 2019 (received for review November 9, 2019)

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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.

Abstract

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.

  • insect agriculture
  • ants
  • symbioses
  • plants
  • ant-plant interactions

Footnotes

  • ↵1To whom correspondence may be addressed. Email: guillaume.chomicki{at}gmail.com.
  • Author contributions: G.C. and E.T.K. designed research; G.C., G.K., and E.T.K. performed research; G.C., S.S.R., and E.T.K. contributed new reagents/analytic tools; G.C. analyzed data; and G.C., S.S.R., and E.T.K. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1919611117/-/DCSupplemental.

Published under the PNAS license.

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Tradeoffs in the evolution of plant farming by ants
Guillaume Chomicki, Gudrun Kadereit, Susanne S. Renner, E. Toby Kiers
Proceedings of the National Academy of Sciences Jan 2020, 201919611; DOI: 10.1073/pnas.1919611117

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Tradeoffs in the evolution of plant farming by ants
Guillaume Chomicki, Gudrun Kadereit, Susanne S. Renner, E. Toby Kiers
Proceedings of the National Academy of Sciences Jan 2020, 201919611; DOI: 10.1073/pnas.1919611117
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