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

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    Evaluation Summary:

    Zhao et al. present an interesting proposal for the evolution of complex multimodal signals based on the analysis of the mating display of small torrent frogs. Combining observational and experimental evidence, they suggest that male limb movements, which are used to swat away blood-sucking midges, have become attractive to female frogs, enhancing the acoustic mating call of these males.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.

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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.

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  1. Version published to 10.7554/elife.76083 on eLife
  2. eLife

    Author Response:

    Reviewer #2 (Public Review):

    Organisms communicate using different sets of signals, ranging from visual, acoustic, chemical, to tactile cues. Such signals transfer information about the signaler to an intended receiver that decodes such cues. Natural selection (and sexual selection) usually can shape how exclusive such signals become for their intended receivers. Depending on the context, some signals might include more than one information channel and become multimodal (e.g., visual + acoustic). Such complex signals might allow receivers to better decode information about the signaler (e.g., genetic quality, health, resources). However, most signalers avoid being detected by predators in their habitat, thus there is generally a conflict between signal detectability by partners and predation avoidance by signalers. In anurans (frogs and toads), the dominant mating signals are acoustic, but visual cues can be combined in the courtship display if the signalers are active during the day and combine those with their vocalizations.

    In the present study, the authors focused on the evolution of mating signals in torrent frogs (Amolops torrentis) from noisy mountain streams of the Hainan Island (China). Males of this species are active during day and night; and their displays include acoustic and visual cues that attract females. The authors show that the acoustic signals might also attract unintended parasites; in this case, midges (small flies) that locate vocalizing males and try to get a blood-meal. Such interaction seems to incite the males to move their limbs as if they are trying to swat away the parasites. By studying such displays, the authors show that body movements in males might increase female preference for them in addition of the acoustic signal. The authors hypothesize that limb movement has been adopted as part of a multimodal mating display where limb movements and vocalizations further entice female preference. For this purpose, the researchers filmed frogs in the field and classified their limb displays. Then, the authors showed evidence that, when males call, these animals tend to attract more midge parasites and such interaction increased the frequency of limb movements as males try to swat away these midges. Interestingly, such body movements, including foot-flagging and leg-stretching, if combined with mating calls, seem to make males more attractive to females.

    This study provides an intriguing hypothesis -- namely, that mating displays might become more attractive if males are engaged in antiparasitic movements. These alleged visual cues capture the attention of females and effectively enhance the sensory components of this mating display. However, it is not clear how much of this antiparasitic (swatting) behavior has become a component of the mating display. For instance, such body movements might be a rather chaotic visual display in a vocalizing male that is trying to "scare away" the parasitic flies. Most amphibians have mating displays that are usually structured (i.e., a specific sequence of components in the signal) and partners can decode such sequences of signal components, which are genetically determined (i.e., they are not learned).

    Thank you for your insightful comments. In this study, parasites can locate male little torrent frogs by exploiting their advertisement calls. In order to repel these insects, this species usually displays various limb movements. So there may be a predictable connection between stereotyped calls and limb movements that seem to be chaotic. We have examined if there is a specific sequence on acoustic (advertisement calls) and visual (attractive limb movements) signals according to the suggestions below. We built a dyadic transition matrix (table S2) for three behavioral units (i.e. advertisement call, AW and HFL), and determined the associations between the three displays using a method from Preininger et al. (2009) and Grafe et al. (2012). Interestingly, we show that the AW and HFL displays tend to be emitted following advertisement calls. So there is a pattern on the sequence of advertisement calls and limb movements that influences female preference. The pattern is similar with the coupling between calls and FF in some other torrent frogs. Such call-mediated pattern allows anti-parasitic movements to be a component of multimodal displays. We have added the relevant details in the manuscript.

    I consider this study a nice natural history report, yet it is not conclusive on the integration of acoustic vocalization and defensive body movements as parts of a multimodal mating display. In other words, such body movements are not coevolving with acoustic signals, rather they are capturing the attention of females as a by-product of males that are frantically trying to scare away flies while vocalizing. I believe that vocalizations are the main signal that females are paying the most attention to, to evaluate the quality of potential male partners.

    We agree with the reviewer that the acoustic signal is the dominant part of the frog’s complex sexual display behaviour that can influence female mate choice. The associated limb movements are indeed just a by-product of fending of eavesdropping parasites, which may only increase receiver’s attention for a brief moment, but which may or may not influence mate choices in other ways (e.g. mate quality assessment). However, under a scenario where two competing males have matching calls, any additional cue that can influence the mating decision can become target of sexual selection and over time become an integrated part of the sexual display. We do not claim this is already the case in our study system, however we do claim that some of the prerequisites for such process of co-option are at least in place.

    We do however agree that in our study system, it remains unclear whether parasite-induced movements reflect the quality of males. We thus cautiously say the limb movements are a part of “signal display” rather than previous “sexual signal display” in the revised manuscript.

  3. eLife

    Evaluation Summary:

    Zhao et al. present an interesting proposal for the evolution of complex multimodal signals based on the analysis of the mating display of small torrent frogs. Combining observational and experimental evidence, they suggest that male limb movements, which are used to swat away blood-sucking midges, have become attractive to female frogs, enhancing the acoustic mating call of these males.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.

  4. eLife

    Reviewer #1 (Public Review):

    Zhao and colleagues investigated the multimodal signalling system of the small torrent frog (Amolops torrentis) and its potential link to ecto-parasites (e.g. blood-sucking midges). The authors present an innovative taxon-oriented behavioural field study. I do not know any similar study and I welcome the authors' effort to describe the multimodal signals of A. torrentis in such great detail. They find that male small torrent frogs display a rich repertoire of visual cues, such as wiggling fingers or toes, or stretching and flagging front or hind legs, in addition to movement and sounds associated with advertisement calls. They show that males display more conspicuous visual displays, when conspecific females are in close proximity, and that those displays do influence the behaviour of the female receivers.

    Another intriguing result of the present study is the demonstrated origin of the limb displays. Zhao et al. find that the original function of the diverse limb movements is to fend off blood-sucking parasites. However, these exact movements have been shown to increase the attractiveness of a male's display to female receivers when combined with the advertisement call: a novel result in the field of anuran bio-acoustics, and especially interesting, as the study species is endemic to only two regions in China and currently threatened by habitat loss.

    The authors conducted an impressive study combining observations, audio and video recordings and behavioural experiments in order to reveal the signalling strategies of A. torrentis. The manuscript provides a fascinating example of a potentially highly complex signalling system in an anuran amphibian -- still a vastly understudied area in the field of animal communication. The study design is well thought-out and I cannot detect any faults in the analysis. The authors interpret their data modestly and draw reasonable conclusions. The figures are well presented and self-explanatory. The scientific illustrations and videos help to understand the fascinating signalling behavior. I really enjoyed reading this manuscript and I am sure, many colleagues will too.

  5. eLife

    Reviewer #2 (Public Review):

    Organisms communicate using different sets of signals, ranging from visual, acoustic, chemical, to tactile cues. Such signals transfer information about the signaler to an intended receiver that decodes such cues. Natural selection (and sexual selection) usually can shape how exclusive such signals become for their intended receivers. Depending on the context, some signals might include more than one information channel and become multimodal (e.g., visual + acoustic). Such complex signals might allow receivers to better decode information about the signaler (e.g., genetic quality, health, resources). However, most signalers avoid being detected by predators in their habitat, thus there is generally a conflict between signal detectability by partners and predation avoidance by signalers. In anurans (frogs and toads), the dominant mating signals are acoustic, but visual cues can be combined in the courtship display if the signalers are active during the day and combine those with their vocalizations.

    In the present study, the authors focused on the evolution of mating signals in torrent frogs (Amolops torrentis) from noisy mountain streams of the Hainan Island (China). Males of this species are active during day and night; and their displays include acoustic and visual cues that attract females. The authors show that the acoustic signals might also attract unintended parasites; in this case, midges (small flies) that locate vocalizing males and try to get a blood-meal. Such interaction seems to incite the males to move their limbs as if they are trying to swat away the parasites. By studying such displays, the authors show that body movements in males might increase female preference for them in addition of the acoustic signal. The authors hypothesize that limb movement has been adopted as part of a multimodal mating display where limb movements and vocalizations further entice female preference. For this purpose, the researchers filmed frogs in the field and classified their limb displays. Then, the authors showed evidence that, when males call, these animals tend to attract more midge parasites and such interaction increased the frequency of limb movements as males try to swat away these midges. Interestingly, such body movements, including foot-flagging and leg-stretching, if combined with mating calls, seem to make males more attractive to females.

    This study provides an intriguing hypothesis -- namely, that mating displays might become more attractive if males are engaged in antiparasitic movements. These alleged visual cues capture the attention of females and effectively enhance the sensory components of this mating display. However, it is not clear how much of this antiparasitic (swatting) behavior has become a component of the mating display. For instance, such body movements might be a rather chaotic visual display in a vocalizing male that is trying to "scare away" the parasitic flies. Most amphibians have mating displays that are usually structured (i.e., a specific sequence of components in the signal) and partners can decode such sequences of signal components, which are genetically determined (i.e., they are not learned). I consider this study a nice natural history report, yet it is not conclusive on the integration of acoustic vocalization and defensive body movements as parts of a multimodal mating display. In other words, such body movements are not coevolving with acoustic signals, rather they are capturing the attention of females as a by-product of males that are frantically trying to scare away flies while vocalizing. I believe that vocalizations are the main signal that females are paying the most attention to, to evaluate the quality of potential male partners.

  6. Version published to 10.1101/2021.12.31.474622v1 on bioRxiv