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.

Reviewing Editor

  1. 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

  1. Received: December 3, 2021
  2. Preprint posted: January 1, 2022 (view preprint)
  3. Accepted: May 3, 2022
  4. Accepted Manuscript published: May 6, 2022 (version 1)
  5. 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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  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
    Shuai-Shuai Zhang, Pei-Chao Wang ... Chen-Zhu Wang
    Research Article

    Almost all herbivorous insects feed on plants and use sucrose as a feeding stimulant, but the molecular basis of their sucrose reception remains unclear. Helicoverpa armigera as a notorious crop pest worldwide mainly feeds on reproductive organs of many plant species in the larval stage, and its adult draws nectar. In this study, we determined that the sucrose sensory neurons located in the contact chemosensilla on larval maxillary galea were 100–1000 times more sensitive to sucrose than those on adult antennae, tarsi, and proboscis. Using the Xenopus expression system, we discovered that Gr10 highly expressed in the larval sensilla was specifically tuned to sucrose, while Gr6 highly expressed in the adult sensilla responded to fucose, sucrose and fructose. Moreover, using CRISPR/Cas9, we revealed that Gr10 was mainly used by larvae to detect lower sucrose, while Gr6 was primarily used by adults to detect higher sucrose and other saccharides, which results in differences in selectivity and sensitivity between larval and adult sugar sensory neurons. Our results demonstrate the sugar receptors in this moth are evolved to adapt toward the larval and adult foods with different types and amounts of sugar, and fill in a gap in sweet taste of animals.