Many animals can increase their communication efficiency by enhancing the complexity in a single sensory modality or by evolving displays that target multiple sensory modalities (Cui et al., 2016; Partan and Marler, 1999). Such multimodal signaling can be highly complex, often involving multiple underlying neuronal motor programs that need to be synchronized in order to perform well (Partan and Marler, 1999; Ryan et al., 2019; Halfwerk et al., 2019; Higham and Hebets, 2013). The production and reception of multimodal signals is often more costly in terms of energy loss or predation and parasitism risk when compared to unimodal signals (Bro-Jørgensen, 2010), and their evolution is therefore often explained through functional benefits, such as cross-modal perception by receivers, which can improve signal detection and discrimination, or enhance attention and memory time (Halfwerk et al., 2019; Hebets and Papaj, 2004; Halfwerk et al., 2014b). Contra to why, we know far less how multimodal signals evolve from unimodal ones. An important question remains whether and when multimodal signals evolve de novo, or evolve through a process of co-option, by incorporating additional cues into a unimodal display (Halfwerk et al., 2019).

Human and many animals often generate by-product cues during signaling that can influence the perception of the dominant part of the signal. A famous example in humans is the McGurk effect which shows lip movement (the by-product of pronunciation) affects speech perception (McGurk and MacDonald, 1976). Similarly, floating frogs produce water ripples when calling from the water. These ripple cues are an unintentional by-product of calling, but have become part of the sexual display, as their presence modulates receiver responses to their acoustic signal components (Halfwerk et al., 2014a). Multimodal signals can thus originate from cues associated with primary signal production, either through a physical linkage (e.g. case of call-induced water ripples) or through a temporal linkage, for example, cues generated by other non-communicative behaviors that occur around the time of signaling. Once signal receivers start to pay attention to these other cues, subsequent selection on these physically or temporally linked cues may lead to closer integration and synchronization with the primary signal and become incorporated into a new, multimodal display. Such process of co-option has been proposed for many ritualized visual displays which are predicted to have evolved from different intra- or interspecific activities such as intentional movements, protective and autonomic responses (Harper, 1991; Hödl and Amézquita, 2001). For example, comparative analyses on Anatidae (i.e. ducks) suggest that the precopulatory displays of head-dipping seem to be derived from bathing behavior (Johnsgard, 1962), which may have originally been associated in time with other sexual signaling behaviors. Physical movements are in particular likely to become integrated into sexual displays. In human and some animals, movements are often used to attract the attention of receivers (Clark and Morjan, 2001; Hugill et al., 2010) and may even serve as primary sexual displays providing reliable information on sender quality (Hugill et al., 2010; Hasson, 1997; Taylor et al., 2000).

Anurans (i.e. frogs and toads) provide a good opportunity to test whether non-communicative behaviors can be co-opted into a signal function (Preininger et al., 2013a; Starnberger et al., 2014). In some anurans, for example, arm-waving movements appear to originate from cleaning behavior due to the similarities in both displays (Pombal et al., 1994). Furthermore, many anuran species display defensive movements that are also similar with communicative visual displays of some taxa (de Sá et al., 2016; Preininger et al., 2009). Here, we hypothesized that some of these physical movements originated from anti-parasite behavior in frogs. Amphibians are often confronted with parasitism from a range of different insects, such as mosquitoes or midges (Grafe et al., 2008; Legett et al., 2018; Van Beurden, 1980; Kay et al., 1985; Ferrar, 1987). These parasites are often attracted to the frog’s mating call to collect a blood meal. In return they may transmit blood-borne diseases or endo-parasites, thus imposing a large cost to a calling frog (Bernal and de Silva, 2015; Bernal et al., 2006; Meuche et al., 2016). Some anurans are observed to perform defensive physical movements in response to these parasites.

Anurans primarily communicate with acoustic signals. Background noise generated by flowing water is an impediment to acoustic communication of torrent anuran species (Preininger et al., 2013a; Grafe et al., 2012). Multimodal displays may increase the efficiency of signal detection and perception (Hebets and Papaj, 2004), and thus are favored in complex noisy environments. Researches on some torrent frogs have showed that the coupling between physical displays (e.g. vocal sac and limb movements) with calls may direct the receiver’s attention and play an important role in conspecific interactions (Preininger et al., 2013a; Preininger et al., 2009; Grafe et al., 2012; Grafe and Wanger, 2007). Insect-evoked movements are often similar to limb movements that act as visual signal. The movements evoked by host-parasite interactions may increase the complexity of signal displays and can potentially increase female preference for acoustic signals in frogs. Thus, the parasite-host interaction may provide an important source of evolutionary raw material for ritualized visual displays in anurans, which in turn may have led to the evolution of multimodal displays in which visual movements and acoustic calls have been combined.

In the present study we examined the role of insect parasites in driving multimodal signal evolution in the little torrent frog (Amolops torrentis), a tropical species that breeds in noisy mountain streams and displays both day and night. Male little torrent frogs prefer to emit advertisement calls from the rocks near streams or near vegetation. Calling males are also often observed to be disturbed by various insects including midges and some other potential parasites. In order to repel these insects, they usually display limb movements that are similar to some spontaneous movements as well as to visual displays that have been reported in other torrent frogs (de Sá et al., 2016; Caldart et al., 2014). Frog-biting midges often locate male anuran hosts by exploiting their advertisement calls (Grafe et al., 2008; Bernal et al., 2006; Meuche et al., 2016). So, there may be a predictable connection between stereotyped calls and limb movements that seem to be chaotic in this species. These contents suggest that their defensive movements may act as a visual cue component in addition to the acoustic component of little torrent frogs.

Here, we evaluated whether the presence of eavesdropping parasites increases limb movements and determined whether and how these parasite-evoked physical displays influence female preference for multimodal signals. First, we filmed little torrent frogs in the field and classified their physical displays involving limb movements. Second, we assessed the link between parasitism and male limb display by quantifying the frequency of parasite interactions as well as limb movements, and tested whether calling males produced more parasite-evoked displays compared to silent males. In order to avoid assessing individual differences, we collected sufficient samples (at least 30 males in each group) to compare the defend displays between calling frogs and silent frogs inhabited in same environment. Third, we determined the effect of midge-evoked visual movements on female mate choice with and without the advertisement calls presented, and examined if there was a specific sequence of attractive limb movements and calls. Finally, we tested whether exaggerated movements play a role in mate choice by analyzing the change of male foot flagging (FF) and leg stretching (LS) displays when females approached them in the field.

Male little torrent frogs show a rich repertoire of limb displays. By performing female choice tests and observing male-female interactions in the field, we showed that several of these limb displays (AW, HFL, and LS + FF) can serve as visual signal components and influence female mate choice. All limb movements could be spontaneously generated, but their rates were increased by call-induced parasite presence. We also found calling males to produce more limb displays than silent males. Such parasite-host interactions may have important evolutionary consequences because females in our choice tests showed a strong preference for males that emitted advertisement calls accompanied by parasite-evoked movements (e.g. AW and HFL). We did not find such preference for limb movements in the absence of call playback, demonstrating that these visual components are part of a multimodal display.

Color, vocal sac, and physical movement, as visual subcomponents, can be added to acoustic signals in anuran multimodal communication (de Luna et al., 2010). For example, agonistic behaviors of male Allobates femoralis are only evoked when males are exposed to vocal sac pulsations combined with acoustic signals during playback experiments (Narins et al., 2005). More and more studies show that streamside-breeding anurans often have complex physical displays including vocal sac inflation, limb movement, as well as body movement. For example, a recent investigation found that male Brazilian torrent frogs (Hylodes japi) have 18 distinct physical displays which may be associated with different social contexts (de Sá et al., 2016). Female little torrent frogs have been shown to prefer the vocal sac movements synchronized with calls over calls only (Zhao, 2021). In the present study, we further showed that this species performed diverse common limb displays. However, we did not observe a potential visual signal related with body displays.

Stream-breeding frogs often possess abundant limb or body movements, but their communicative functions have rarely been tested (Hödl and Amézquita, 2001). Most previous work analyzed those physical movements based on field observation or video, and few researchers have experimentally explored the effect of these visual displays on female mate choice. In the present study, we experimentally examined whether limb displays can serve as visual signal and influence female choice in little torrent frogs. By video playbacks, we found females show a significant preference for males displaying with AW and HFL as compared to motionless males. FF displays are widespread in anurans, and their functions are mainly explored from the perspective of male-male competition. For instance, male Bornean ranid frogs (Staurois guttatus) significantly increase such display when conspecific advertisement calls are broadcasted from 1 to 2 m distance in the field (Grafe and Wanger, 2007). In our study, males generated more conspicuous LS and FF displays when females were at close range in the field. Because of the difficulties in obtaining male-female interaction data, we only collected four samples which were used to examine the role of LS + FF displays. Similar with results in some other species such as Staurois parvus (Preininger et al., 2013b), males also increased such movements in response to male-male closed interactions (L Zhao et al., unpublished data), indicating that LS and FF actually are used in close-range communication. Moreover, the statistical power was high and p≤0.001 for all tests. So our results about the role of the exaggerated movements may not be biased by sample size. However, playback tests and more accumulation on field data are necessary in the future.

Frogs and toads are known to be able to see well in dim-light (Yovanovich et al., 2017). Many anurans perform behaviors only at environmental illuminations with very low levels (Buchanan, 1993). Due to their phototactic responses (Jaeger and Hailman, 1973), some video playback studies may have obtained odd results in the past. Little torrent frogs are diurnal species who can communicate with acoustic and visual signals under high-light as well as dark environments. In order to avoid possible effects from light, we set a low environmental illumination according to a natural level. In our study, females discriminated between moving and stationary stimuli. Meanwhile, more conspicuous movements (e.g. HFL) had greater attractiveness than less conspicuous movements (e.g. LSA). We thus argue that little torrent frogs actually recognize the video image as a conspecific stimulus.

Among four visual movements in our playback experiments, the attractive AW and HFL are more conspicuous than the unattractive W and LSA because the display of AW and HFL involves more occupation in terms of time and space. More conspicuous physical movements can increase receiver’s attention (Stokes and Williams, 1971; Quaranta et al., 2007), so the difference in conspicuousness may be related to the attractiveness of these movements. According to the efficacy-based hypotheses, if two signals of different modalities are generated sequentially, a signal may alert the receiver to another signal (Hebets and Papaj, 2004; Grafe et al., 2012). In this study, the AW and HFL displays tend to be emitted following advertisement calls. We show there is a pattern on the sequence of advertisement calls and limb movements that can elicit female preference, which is similar with the coupling between calls and FF in some torrent frogs (Preininger et al., 2009; Grafe et al., 2012). The LS and FF movements are the most conspicuous visual signal in little torrent frogs. Males significantly increase the two movements when females appear nearby in the wild. Such conspicuous displays, however, are not used during parasite interactions because male frogs generally perform defensive motions when parasites fall on their body (or limbs) or fly very close to their body (or limbs). Under these conditions, small and medium limb movements are sufficient, while the exaggerated motions (LS and FF) seem to be unnecessary. Therefore, the LS and FF displays are specially performed for conspecific communication, but may have evolved out of the less conspicuous limb movements.

The evolution of dynamic visual signals is often influenced by several social and environmental factors such as territorial aggression (Preininger et al., 2013a; Schuppe et al., 2017; Wu et al., 2018), diurnality (Harper, 1991), background noise (Grafe et al., 2012; Grafe and Tony, 2017), as well as predation pressure (Bradbury and Vehrencamp, 1998). Visual movements or movement-involved multimodal signals can result in senders with more chance of being seen by predators or parasites. Physical displays thus often need to increase the attention of intended receivers while limiting the eavesdropping of unintended receivers (Steinberg et al., 2014). In little torrent frogs, male limb displays increased with parasite stress, and such defensive movements can serve as visual cues. These results suggest that parasite stress can induce more visual movements and increase the complexity of audiovisual multimodal displays in little torrent frogs as a by-product. In this study, calling males had a larger parasitic risk than silent males, and we identified Corethrella spp. midges which are known to localize frog hosts by eavesdropping on their calls (Bernal and de Silva, 2015). However, more studies are needed to further examine whether and how the species is eavesdropped by sound-locating midges.

The idea that some physical movements are the raw material of dynamic visual signals has been proposed for many years (Harper, 1991; Johnsgard, 1962). In the Panamanian golden frog (Atelopus zeteki), for instance, the conspicuous semaphore signal is supposed to originate from a standard stepping motion (Lindquist and Hetherington, 1998). However, it is largely unknown how physical movements are incorporated into communicative systems. Sexual selection is believed to be an important driver and the evolution of physical movements may be favored when females are sensitive to some movements in specific environments (Fleishman, 1992). During courtship, complex signals are often preferred by females and males frequently include sexual displays more than one channel (Andersson, 1994; Clark and Feo, 2010). So physical movements from males may be incorporated into multimodal communication systems if they tap into the sensory bias of females and are beneficial to increase the attractiveness of males (sensory exploitation process; Ryan, 1998). In our study, female little torrent frogs showed a significant preference for the conspicuous defensive movements when the advertisement calls were simultaneously broadcasted. In noisy streams, acoustic signals plus the relatively conspicuous movements may benefit animals to overcome auditory masking by flowing water (Partan, 2017). Our study experimentally shows that such incorporation of non-sexual movements may actually work to increase female preference and thus become part of a multimodal display. The associated limb movements are 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). We thus do not argue that we demonstrate a multimodal evolution, but test for prerequisite conditions of a scenario in which multimodal cues evolve from unimodal one via co-option of associated cues.

The simplest movements (LSA/W) are hardly used during parasite interactions and do not induce female preference. The intermediate movements (AW/HFL) are used during parasite interactions and induce a preference. The most complex movements (LS + FF) are only used during male-female (or male-male) interactions. This observed pattern could therefore reflect the evolutionary history of the visual display, from a simple to an advanced stage, where the most complex movements are no longer used in their original context (parasite defense) but only for their new function (sexual communication). Interestingly, in many anurans such as, for example, Micrixalus saxicola and S. parvus (Preininger et al., 2013b), the most complex display also involve FF.

In conclusion, we show that calling behaviors and the levels of parasite interference are correlated and males produce diverse defensive limb movements in order to avoid those unintended receivers in little torrent frogs. By female mate choice tests, we find that relatively conspicuous defensive movements increase the attractiveness of male calls to female frogs. Thus, we suggest that parasite-host interaction may increase the complexity of audiovisual displays. For the first time, we experimentally demonstrate that movements evoked by interspecific activities may evolve via increasing female preference. Our results, together with phylogenetic studies in future, would increase our understanding toward the evolutionary origin of dynamic visual cues and the relationship between natural or sexual selection pressure and multimodal communication behavior.

Data used to generate the results are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.f1vhhmgzg.

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Author details

1. Longhui Zhao

   1. CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
   2. Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, China

   Contribution

   Data curation, Formal analysis, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8746-2803

2. Jichao Wang

   Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, China

   Contribution

   Data curation, Investigation

   Competing interests

   No competing interests declared

3. Haodi Zhang

   CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China

   Contribution

   Data curation, Investigation

   Competing interests

   No competing interests declared

4. Tongliang Wang

   Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, China

   Contribution

   Data curation, Resources

   Competing interests

   No competing interests declared

5. Yue Yang

   CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

6. Yezhong Tang

   CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China

   Contribution

   Methodology, Writing – original draft

   Competing interests

   No competing interests declared

7. Wouter Halfwerk

   Department of Ecological Sciences, Vrije Universiteit Amsterdam, De Boelelaan, Amsterdam, Netherlands

   Contribution

   Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

8. Jianguo Cui

   CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China

   Contribution

   Conceptualization, Funding acquisition, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   cuijg@cib.ac.cn

   Competing interests

   No competing interests declared

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