Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs
Abstract
Many animals rely on complex signals that target multiple senses to attract mates and repel rivals. These multimodal displays can however also attract unintended receivers, which can be an important driver of signal complexity. Despite being taxonomically widespread, we often lack insight into how multimodal signals evolve from unimodal signals and in particular what roles unintended eavesdroppers play. Here we assess whether the physical movements of parasite defense behavior increase the complexity and attractiveness of an acoustic sexual signal in the little torrent frog (Amolops torrentis). Calling males of this species often display limb movements in order to defend against blood-sucking parasites such as frog-biting midges that eavesdrop on their acoustic signal. Through mate choice tests we show that some of these midge-evoked movements influence female preference for acoustic signals. Our data suggest that midge-induced movements may be incorporated into a sexual display, targeting both hearing and vision in the intended receiver. Females may play an important role in incorporating these multiple components because they prefer signals which combine multiple modalities. Our results thus help to understand the relationship between natural and sexual selection pressure operating on signalers and how in turn this may influence multimodal signal evolution.
Data availability
Data used to generate the results are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.f1vhhmgzg.
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The data of parasite-induced and spontaneous displays in each limb movement for calling males, silent males and males that have females nearbyDryad Digital Repository, doi:10.5061/dryad.f1vhhmgzg.
Article and author information
Author details
Funding
Sichuan Science and Technology Program (2022JDTD0026)
- Jianguo Cui
National Natural Science Foundation of China (31772464)
- Jianguo Cui
Youth Innovation Promotion Association (2012274)
- Jianguo Cui
CAS Light of West China" Program" (None)
- Jianguo Cui
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Ammie K Kalan, University of Victoria, Canada
Ethics
Animal experimentation: All procedures were approved by the management office of the Wuzhishan Nature Reserve and the Animal Care and Use Committee of the Chengdu Institute of Biology, CAS (CIB2017050004 & CIB2019060012).
Version history
- Received: December 3, 2021
- Preprint posted: January 1, 2022 (view preprint)
- Accepted: May 3, 2022
- Accepted Manuscript published: May 6, 2022 (version 1)
- Version of Record published: May 20, 2022 (version 2)
Copyright
© 2022, Zhao et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Ecology
- Evolutionary Biology
Recently we showed that limb movements associated with anti-parasite defenses can enhance acoustic signal attraction in male little torrent frogs (Amolops torrentis), which suggests a potential pathway for physical movements to become co-opted into mating displays (Zhao et al., 2022). Anderson et al. argue for alternative explanations of our results and provide a reanalysis of part of our data (Anderson et al., 2023). We acknowledge some of the points raised and provide an additional analysis in support of our hypothesis.
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- Computational and Systems Biology
- Ecology
Collaborative hunting, in which predators play different and complementary roles to capture prey, has been traditionally believed to be an advanced hunting strategy requiring large brains that involve high-level cognition. However, recent findings that collaborative hunting has also been documented in smaller-brained vertebrates have placed this previous belief under strain. Here, using computational multi-agent simulations based on deep reinforcement learning, we demonstrate that decisions underlying collaborative hunts do not necessarily rely on sophisticated cognitive processes. We found that apparently elaborate coordination can be achieved through a relatively simple decision process of mapping between states and actions related to distance-dependent internal representations formed by prior experience. Furthermore, we confirmed that this decision rule of predators is robust against unknown prey controlled by humans. Our computational ecological results emphasize that collaborative hunting can emerge in various intra- and inter-specific interactions in nature, and provide insights into the evolution of sociality.