Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs

  1. Longhui Zhao
  2. Jichao Wang
  3. Haodi Zhang
  4. Tongliang Wang
  5. Yue Yang
  6. Yezhong Tang
  7. Wouter Halfwerk
  8. Jianguo Cui  Is a corresponding author
  1. Chinese Academy of Sciences, China
  2. Hainan Normal University, China
  3. Vrije Universiteit Amsterdam, Netherlands

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.

The following data sets were generated

Article and author information

Author details

  1. Longhui Zhao

    Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Jichao Wang

    Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Haodi Zhang

    Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Tongliang Wang

    College of Life Sciences, Hainan Normal University, Haikou, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Yue Yang

    Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Yezhong Tang

    Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Wouter Halfwerk

    Department of Ecological Sciences, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  8. Jianguo Cui

    Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
    For correspondence
    cuijgcn@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8746-2803

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.

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).

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.

Metrics

  • 1,123
    views
  • 223
    downloads
  • 4
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Longhui Zhao
  2. Jichao Wang
  3. Haodi Zhang
  4. Tongliang Wang
  5. Yue Yang
  6. Yezhong Tang
  7. Wouter Halfwerk
  8. Jianguo Cui
(2022)
Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs
eLife 11:e76083.
https://doi.org/10.7554/eLife.76083

Share this article

https://doi.org/10.7554/eLife.76083

Further reading

    1. Ecology
    2. Evolutionary Biology
    Longhui Zhao, Wouter Halfwerk, Jianguo Cui

    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.

    1. Ecology
    Itai Bloch, David Troupin ... Nir Sapir
    Research Article

    Optimal foraging theory posits that foragers adjust their movements based on prey abundance to optimize food intake. While extensively studied in terrestrial and marine environments, aerial foraging has remained relatively unexplored due to technological limitations. This study, uniquely combining BirdScan-MR1 radar and the Advanced Tracking and Localization of Animals in Real-Life Systems biotelemetry system, investigates the foraging dynamics of Little Swifts (Apus affinis) in response to insect movements over Israel’s Hula Valley. Insect movement traffic rate (MoTR) substantially varied across days, strongly influencing swift movement. On days with high MoTR, swifts exhibited reduced flight distance, increased colony visit rate, and earlier arrivals at the breeding colony, reflecting a dynamic response to prey availability. However, no significant effects were observed in total foraging duration, flight speed, or daily route length. Notably, as insect abundance increased, inter-individual distances decreased. These findings suggest that Little Swifts optimize their foraging behavior in relation to aerial insect abundance, likely influencing reproductive success and population dynamics. The integration of radar technology and biotelemetry systems provides a unique perspective on the interactions between aerial insectivores and their prey, contributing to a comprehensive understanding of optimal foraging strategies in diverse environments.