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The enemy of my enemy: multiple interacting selection pressures lead to unexpected anti-predator responses

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Abstract

Despite being a major selective force, predation can induce puzzling variability in anti-predator responses—from lack of predator aversion to lifelong predator-induced fear. This variability is hypothesised to result from variation in the trade-offs associated with avoiding predators. But critical information on fitness outcomes of these trade-offs associated with anti-predator behaviours is lacking. We tested this trade-off hypothesis in Aedes aegypti, by examining oviposition site selection decisions in response towards larval predation risk and comprehensively measuring the fitness implications of trade-offs of avoiding larval predators, using three fitness measures: larval survival, development time and size. In a field study, we find that adult females show a surprisingly variable response to predators, ranging from attraction to avoidance. This variation is explained by fitness outcomes of oviposition along a predation-risk gradient that we measured in the laboratory. We show that ovipositing females could gain fitness benefits from ovipositing in pools with a low density of predators, rather than in predator-free pools, as predators provide a release from negative density effects of conspecific larvae that might co-occur in a pool. Interacting selection pressures may thus explain diverse prey responses. We suggest other systems in which similarly unexpected prey behaviour is likely to occur.

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Data accessibility

We would be happy to provide the raw data for the analyses and results reported in this manuscript. On acceptance, we would be happy to archive the data files, R code supporting the results.

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Acknowledgements

We thank Mahalakshmi and Rajashree for maintenance of mosquito colony; Karthikeyan Chandrasegaran for discussions; Rishi Valley School and Indian Institute of Science for providing infrastructure. The work was supported by Department of Biotechnology—Indian Institute of Science (DBT-IISc) partnership Grant, Department of Science and Technology—Fund for Improvement of S&T infrastructure (DST-FIST) Grant and Ministry of Human Resource Development—Indian Institute of Science for graduate scholarship. Funding was provided by Department of Biotechnology, Ministry of Science and Technology.

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Authors

Contributions

MS and KI designed the study. MS collected the data and wrote the first draft of the manuscript. MS, SQ, VG, and KI contributed substantially to revisions.

Corresponding author

Correspondence to Manvi Sharma.

Additional information

Communicated by Aaron J. Wirsing.

We wish to submit this work for the Highlighted student research category. This work was done as part of the Ph.D. thesis of the lead author. In this study, we take a rare approach of measuring fitness pay-offs in multiple currencies to explain the puzzle of how predation risk can induce variability in anti-predator responses—from attraction to aversion towards predators.

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Sharma, M., Quader, S., Guttal, V. et al. The enemy of my enemy: multiple interacting selection pressures lead to unexpected anti-predator responses. Oecologia 192, 1–12 (2020). https://doi.org/10.1007/s00442-019-04552-4

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  • DOI: https://doi.org/10.1007/s00442-019-04552-4

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