The Evolutionary Importance of Intraspecific Variation in Sexual Communication Across Sensory Modalities.

The evolution of sexual communication is critically important in the diversity of arthropods, which are declining at a fast pace worldwide. Their environments are rapidly changing, with increasing chemical, acoustic, and light pollution. To predict how arthropod species will respond to changing climates, habitats, and communities, we need to understand how sexual communication systems can evolve. In the past decades, intraspecific variation in sexual signals and responses across different modalities has been identified, but never in a comparative way. In this review, we identify and compare the level and extent of intraspecific variation in sexual signals and responses across three different modalities, chemical, acoustic, and visual, focusing mostly on insects. By comparing causes and possible consequences of intraspecific variation in sexual communication among these modalities, we identify shared and unique patterns, as well as knowledge needed to predict the evolution of sexual communication systems in arthropods in a changing world.

Noise and light pollution elicit endocrine responses in urban but not forest frogs.

Urban areas are characterised by the presence of sensory pollutants, such as anthropogenic noise and artificial light at night (ALAN). Animals can quickly adapt to novel environmental conditions by adjusting their behaviour, which is proximately regulated by endocrine systems. While endocrine responses to sensory pollution have been widely reported, this has not often been linked to changes in behaviour, hampering the understanding of adaptiveness of endocrine responses. Our aim was, therefore, to investigate the effects of urbanisation, specifically urban noise and light pollution, on hormone levels in male urban and forest túngara frogs (Engystomops pustulosus), a species with reported population divergence in behaviour in response to urbanisation. We quantified testosterone and corticosterone release rates in the field and in the lab before and after exposure to urban noise and/or light. We show that urban and forest frogs differ in their endocrine phenotypes under field as well as lab conditions. Moreover, in urban frogs exposure to urban noise and light led, respectively, to an increase in testosterone and decrease in corticosterone, whereas in forest frogs sensory pollutants did not elicit any endocrine response. Our results show that urbanisation, specifically noise and light pollution, can modulate hormone levels in urban and forest populations differentially. The observed endocrine responses are consistent with the observed behavioural changes in urban frogs, providing a proximate explanation for the presumably adaptive behavioural changes in response to urbanisation.

Genomic footprints of (pre) colonialism: Population declines in urban and forest túngara frogs coincident with historical human activity.

Urbanisation is rapidly altering ecosystems, leading to profound biodiversity loss. To mitigate these effects, we need a better understanding of how urbanisation impacts dispersal and reproduction. Two contrasting population demographic models have been proposed that predict that urbanisation either promotes (facilitation model) or constrains (fragmentation model) gene flow and genetic diversity. Which of these models prevails likely depends on the strength of selection on specific phenotypic traits that influence dispersal, survival, or reproduction. Here, we a priori examined the genomic impact of urbanisation on the Neotropical túngara frog (Engystomops pustulosus), a species known to adapt its reproductive traits to urban selective pressures. Using whole-genome resequencing for multiple urban and forest populations we examined genomic diversity, population connectivity and demographic history. Contrary to both the fragmentation and facilitation models, urban populations did not exhibit substantial changes in genomic diversity or differentiation compared with forest populations, and genomic variation was best explained by geographic distance rather than environmental factors. Adopting an a posteriori approach, we additionally found both urban and forest populations to have undergone population declines. The timing of these declines appears to coincide with extensive human activity around the Panama Canal during the last few centuries rather than recent urbanisation. Our study highlights the long-lasting legacy of past anthropogenic disturbances in the genome and the importance of considering the historical context in urban evolution studies as anthropogenic effects may be extensive and impact nonurban areas on both recent and older timescales.

Ripple effects in a communication network: anti-eavesdropper defence elicits elaborated sexual signals in rival males.

Emitting conspicuous signals into the environment to attract mates comes with the increased risk of interception by eavesdropping enemies. As a defence, a commonly described strategy is for signallers to group together in leks, diluting each individual's risk. Lekking systems are often highly social settings in which competing males dynamically alter their signalling behaviour to attract mates. Thus, signalling at the lek requires navigating fluctuations in risk, competition and reproductive opportunities. Here, we investigate how behavioural defence strategies directed at an eavesdropping enemy have cascading effects across the communication network. We investigated these behaviours in the túngara frog (Engystomops pustulosus), examining how a calling male's swatting defence directed at frog-biting midges indirectly affects the calling behaviour of his rival. We found that the rival responds to swat-induced water ripples by increasing his call rate and complexity. Then, performing phonotaxis experiments, we found that eavesdropping fringe-lipped bats (Trachops cirrhosus) do not exhibit a preference for a swatting male compared to his rival, but females strongly prefer the rival male. Defences to minimize attacks from eavesdroppers thus shift the mate competition landscape in favour of rival males. By modulating the attractiveness of signalling prey to female receivers, we posit that eavesdropping micropredators likely have an unappreciated impact on the ecology and evolution of sexual communication systems.

Response to comment on 'Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs'.

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.

Acoustic camouflage increases with body size and changes with bat echolocation frequency range in a community of nocturnally active Lepidoptera.

Body size is an important trait in predator-prey dynamics as it is often linked to detection, as well as the success of capture or escape. Larger prey, for example, often runs higher risk of detection by their predators, which imposes stronger selection on their anti-predator traits compared to smaller prey. Nocturnal Lepidoptera (moths) vary strongly in body size, which has consequences for their predation risk, as bigger moths return stronger echoes for echolocating bats. To compensate for increased predation risk, larger moths are therefore expected to have improved anti-predator defences. Moths are covered by different types of scales, which for a few species are known to absorb ultrasound, thus providing acoustic camouflage. Here, we assessed whether moths differ in their acoustic camouflage in a size-dependent way by focusing on their body scales and the different frequency ranges used by bats. We used a sonar head to measure 3D echo scans of a total of 111 moth specimens across 58 species, from eight different families of Lepidoptera. We scanned all the specimens and related their echo-acoustic target strength to various body size measurements. Next, we removed the scales covering the thorax and abdomen and scanned a subset of specimens again to assess the sound absorptive properties of these scales. Comparing intact specimens with descaled specimens, we found almost all species to absorb ultrasound, reducing detection risk on average by 8%. Furthermore, the sound absorptive capacities of body scales increased with body size suggesting that larger species benefit more from acoustic camouflage. The size-dependent effect of camouflage was in particular pronounced for the higher frequencies (above 29 kHz), with moth species belonging to large-bodied families consequently demonstrating similar target strengths compared to species from small-bodied families. Finally, we found the families to differ in frequency range that provided the largest reduction in detection risk, which may be related to differences in predation pressure and predator communities of these families. In general, our findings have important implications for predator-prey interactions across eco-evolutionary timescales and may suggest that acoustic camouflage played a role in body size evolution of nocturnally active Lepidoptera.

An ultrasound-absorbing inflorescence zone enhances echo-acoustic contrast of bat-pollinated cactus flowers.

Flowering plants have evolved an extraordinary variety of signalling traits to attract their pollinators. Most flowers rely on visual and chemical signals, but some bat-pollinated plants have evolved passive acoustic floral signals. All known acoustic flower signals rely on the same principle of increased sonar reflectivity. Here, we describe a novel mechanism that relies on increased absorption of the area surrounding the flower. In a bat-pollinated cactus (Espostoa frutescens) we found a hairy inflorescence zone, a so-called cephalium. Flowers solely emerge out of this zone. We measured the echoes of cephalia, flowers and unspecialized column surfaces and recorded echolocation calls of approaching bats. We found that the cephalium acts as a strong ultrasound absorber, attenuating the sound by -14 dB. The absorption was highest around the echolocation call frequencies of approaching bats. Our results indicate that, instead of making flowers more reflective, plants can also evolve structures to attenuate the background echo, thereby enhancing the acoustic contrast with the target.

Anthropogenic noise and light alter temporal but not spatial breeding behavior in a wild frog.

Increasing urbanization has led to large-scale land-use changes, exposing persistent populations to drastically altered environments. Sensory pollutants, including low-frequency anthropogenic noise and artificial light at night (ALAN), are typically associated with urban environments and known to impact animal populations in a variety of ways. Both ALAN and anthropogenic noise can alter behavioral and physiological processes important for survival and reproduction, including communication and circadian rhythms. Although noise and light pollution typically co-occur in urbanized areas, few studies have addressed their combined impact on species' behavior. Here, we assessed how anthropogenic noise and ALAN can influence spatial and temporal variation in breeding activity of a wild frog population. By exposing artificial breeding sites inside a tropical rainforest to multiple sensory environments, we found that both anthropogenic noise and ALAN impact breeding behavior of túngara frogs (Engystomops pustulosus), albeit in different ways. Males arrived later in the night at their breeding sites in response to anthropogenic noise. ALAN, on the other hand, led to an increase in calling effort. We found no evidence that noise or light pollution either attracted frogs to or repelled frogs from breeding sites. Thus, anthropogenic noise may negatively affect calling males by shifting the timing of sexual signaling. Conversely, ALAN may increase the attractiveness of calling males. These changes in breeding behavior highlight the complex ways that urban multisensory pollution can influence behavior and suggest that such changes may have important ecological implications for the wildlife that are becoming increasingly exposed to urban multisensory pollution.

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

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.

A comprehensive overview of the effects of urbanisation on sexual selection and sexual traits.

Urbanisation can affect mating opportunities and thereby alter inter- and intra-sexual selection pressures on sexual traits. Biotic and abiotic urban conditions can influence an individual's success in pre- and post-copulatory mating, for example through impacts on mate attraction and mate preference, fertilisation success, resource competition or rival interactions. Divergent sexual selection pressures can lead to differences in behavioural, physiological, morphological or life-history traits between urban and non-urban populations, ultimately driving adaptation and speciation. Most studies on urban sexual selection and mating interactions report differences between urban and non-urban populations or correlations between sexual traits and factors associated with increased urbanisation, such as pollution, food availability and risk of predation and parasitism. Here we review the literature on sexual selection and sexual traits in relation to urbanisation or urban-associated conditions. We provide an extensive list of abiotic and biotic factors that can influence processes involved in mating interactions, such as signal production and transmission, mate choice and mating opportunities. We discuss all relevant data through the lens of two, non-mutually exclusive theories on sexual selection, namely indicator and sensory models. Where possible, we indicate whether these models provide the same or different predictions regarding urban-adapted sexual signals and describe different experimental designs that can be useful for the different models as well as to investigate the drivers of sexual selection. We argue that we lack a good understanding of: (i) the factors driving urban sexual selection; (ii) whether reported changes in traits result in adaptive benefits; and (iii) whether these changes reflect a short-term ecological, or long-term evolutionary response. We highlight that urbanisation provides a unique opportunity to study the process and outcomes of sexual selection, but that this requires a highly integrative approach combining experimental and observational work.

Adding colour-realistic video images to audio playbacks increases stimulus engagement but does not enhance vocal learning in zebra finches.

Bird song and human speech are learned early in life and for both cases engagement with live social tutors generally leads to better learning outcomes than passive audio-only exposure. Real-world tutor-tutee relations are normally not uni- but multimodal and observations suggest that visual cues related to sound production might enhance vocal learning. We tested this hypothesis by pairing appropriate, colour-realistic, high frame-rate videos of a singing adult male zebra finch tutor with song playbacks and presenting these stimuli to juvenile zebra finches (Taeniopygia guttata). Juveniles exposed to song playbacks combined with video presentation of a singing bird approached the stimulus more often and spent more time close to it than juveniles exposed to audio playback only or audio playback combined with pixelated and time-reversed videos. However, higher engagement with the realistic audio-visual stimuli was not predictive of better song learning. Thus, although multimodality increased stimulus engagement and biologically relevant video content was more salient than colour and movement equivalent videos, the higher engagement with the realistic audio-visual stimuli did not lead to enhanced vocal learning. Whether the lack of three-dimensionality of a video tutor and/or the lack of meaningful social interaction make them less suitable for facilitating song learning than audio-visual exposure to a live tutor remains to be tested.

Covariation among multimodal components in the courtship display of the túngara frog.

Communication systems often include a variety of components, including those that span modalities, which may facilitate detection and decision-making. For example, female túngara frogs and fringe-lipped bats generally rely on acoustic mating signals to find male túngara frogs in a mating or foraging context, respectively. However, two additional cues (vocal sac inflation and water ripples) can enhance detection and choice behavior. To date, we do not know the natural variation and covariation of these three components. To address this, we made detailed recordings of calling males, including call amplitude, vocal sac volume and water ripple height, in 54 frogs (2430 calls). We found that all three measures correlated, with the strongest association between the vocal sac volume and call amplitude. We also found that multimodal models predicted the mass of calling males better than unimodal models. These results demonstrate how multimodal components of a communication system relate to each other and provide an important foundation for future studies on how receivers integrate and compare complex displays.

Complex sensory environments alter mate choice outcomes.

Noise is a common problem in animal communication. We know little, however, about how animals communicate in the presence of noise using multimodal signals. Multimodal signals are hypothesised to be favoured by evolution because they increase the efficacy of detection and discrimination in noisy environments. We tested the hypothesis that female túngara frogs' responses to attractive male advertisement calls are improved in noise when a visual signal component is added to the available choices. We tested this at two levels of decision complexity (two and three choices). In a two-choice test, the presence of noise did not reduce female preferences for attractive calls. The visual component of a calling male, associated with an unattractive call, also did not reduce preference for attractive calls in the absence of noise. In the presence of noise, however, females were more likely to choose an unattractive call coupled with the visual component. In three-choice tests, the presence of noise alone reduced female responses to attractive calls and this was not strongly affected by the presence or absence of visual components. The responses in these experiments fail to support the multimodal signal efficacy hypothesis. Instead, the data suggest that audio-visual perception and cognitive processing, related to mate choice decisions, are dependent on the complexity of the sensory scene.

Variation in plant leaf traits affects transmission and detectability of herbivore vibrational cues.

Many insects use plant-borne vibrations to obtain important information about their environment, such as where to find a mate or a prey, or when to avoid a predator. Plant species can differ in the way they vibrate, possibly affecting the reliability of information, and ultimately the decisions that are made by animals based on this information. We examined whether the production, transmission, and possible perception of plant-borne vibrational cues is affected by variation in leaf traits. We recorded vibrations of 69 Spodoptera exigua caterpillars foraging on four plant species that differed widely in their leaf traits (cabbage, beetroot, sunflower, and corn). We carried out a transmission and an airborne noise absorption experiment to assess whether leaf traits influence amplitude and frequency characteristics, and background noise levels of vibrational chewing cues. Our results reveal that species-specific leaf traits can influence transmission and potentially perception of herbivore-induced chewing vibrations. Experimentally-induced vibrations attenuated stronger on plants with thicker leaves. Amplitude and frequency characteristics of chewing vibrations measured near a chewing caterpillar were, however, not affected by leaf traits. Furthermore, we found a significant effect of leaf area, water content and leaf thickness-important plant traits against herbivory, on the vibrations induced by airborne noise. On larger leaves higher amplitude vibrations were induced, whereas on thicker leaves containing more water airborne noise induced higher peak frequencies. Our findings indicate that variation in leaf traits can be important for the transmission and possibly detection of vibrational cues.

Environmental and morphological constraints interact to drive the evolution of communication signals in frogs.

Animals show a rich diversity of signals and displays. Among the many selective forces driving the evolution of communication signals, one widely recognized factor is the structure of the environment where animals communicate. In particular, animals communicating by sounds often emit acoustic signals from specific locations, such as high up in the air, from the ground or in the water. The properties of these different display sites may impose different constraints on sound production, and therefore drive signal evolution. Here, we used comparative phylogenetic analyses to assess the relationship between calling site (aquatic versus nonaquatic), body size and call dominant frequency of 160 frog species from the families Ranidae, Leptodactylidae and Hylidae. We found that the frequency of frogs calling from the water was lower than that of species calling outside of the water, a trend that was consistent across the three families studied. Furthermore, phylogenetic path analysis revealed that call site had both direct and indirect effects on call frequency. Indirect effects were mediated by call site influencing male body size, which in turn was negatively associated with call frequency. Our results suggest that properties of display sites can drive signal evolution, most likely not only through morphological constraints imposed on the sound production mechanism, but also through changes in body size, highlighting the relevance of the interplay between morphological adaptation and signal evolution. Changes in display site may therefore have important evolutionary consequences, as it may influence sexual selection processes and ultimately may even promote speciation.

Floating frogs sound larger: environmental constraints on signal production drives call frequency changes.

In animal communication, receivers benefit from signals providing reliable information on signalers' traits of interest. Individuals involved in conflicts, such as competition between rivals, should pay particular attention to cues that are "unfakeable" by the senders due to the intrinsic properties of the production process. In bioacoustics, the best-known example of such "index signals" is the relationship between a sender's body size and the dominant frequency of their vocalizations. Dominant frequency may, however, not only depend on an animal's morphology but also on the interaction between the sound production system and its immediate environment. Here, we experimentally altered the environment surrounding calling frogs and assessed its impact on the signal produced. Our results show that frogs that are floating are able to inflate their vocal sacs fully and that this change in inflation level is correlated with a decrease of call dominant frequency.

Anthropogenic noise impairs foraging for cryptic prey via cross-sensory interference.

Anthropogenic noise levels are globally rising with profound impacts on ecosystems and the species that live in them. Masking or distraction by noise can interfere with relevant sounds and thereby impact ecological interactions between individuals of the same or different species. Predator-prey dynamics are particularly likely to be influenced by rising noise levels, with important population- and community-level consequences, as species may differentially adapt to noise disturbance. Acoustic noise can, however, also impair the use of visual information by animals through the process of cross-sensory interference, possibly impacting species interactions that have so far been largely ignored by noise impact studies. Here, we assessed how noise affected the performance of great tit (Parus major) foraging on cryptic prey. Birds trained individually to search for paper moths differing in the level of camouflage with the test background were tested in the presence and absence of noise. We found that noise significantly increased approach and attack latencies, but that the effect depended on the level of crypsis. Noise increased latencies for cryptic prey targets, but not for conspicuous and colour-matched prey targets. Our results show that noise can interfere with the processing of visual information, particularly in difficult tasks such as separating objects from a similar looking background. These results have important ecological and evolutionary implications as they demonstrate how globally rising anthropogenic noise levels can influence the arms race between predators and prey across sensory domains.

Why conservation biology can benefit from sensory ecology.

Global expansion of human activities is associated with the introduction of novel stimuli, such as anthropogenic noise, artificial lights and chemical agents. Progress in documenting the ecological effects of sensory pollutants is weakened by sparse knowledge of the mechanisms underlying these effects. This severely limits our capacity to devise mitigation measures. Here, we integrate knowledge of animal sensory ecology, physiology and life history to articulate three perceptual mechanisms-masking, distracting and misleading-that clearly explain how and why anthropogenic sensory pollutants impact organisms. We then link these three mechanisms to ecological consequences and discuss their implications for conservation. We argue that this framework can reveal the presence of 'sensory danger zones', hotspots of conservation concern where sensory pollutants overlap in space and time with an organism's activity, and foster development of strategic interventions to mitigate the impact of sensory pollutants. Future research that applies this framework will provide critical insight to preserve the natural sensory world.

Multisensory pollution: Artificial light at night and anthropogenic noise have interactive effects on activity patterns of great tits (Parus major).

Urbanisation is increasing globally at a rapid pace. Consequently, wild species face novel environmental stressors associated with urban sprawl, such as artificial light at night and noise. These stressors have pervasive effects on the behaviour and physiology of many species. Most studies have singled out the impact of just one of these stressors, while in the real world they are likely to co-occur both temporally and spatially, and we thus lack a clear understanding of the combined effect of anthropogenic stressors on wild species. Here, we experimentally exposed captive male great tits (Parus major) to artificial light at night and 24 h noise in a fully factorial experiment. We then measured the effect of both these stressors on their own and their combination on the amount and timing of activity patterns. We found that both light and noise affected activity patterns when presented alone, but in opposite ways: light increased activity, particularly at night, while noise reduced it, particularly during the day. When the two stressors were combined, we found a synergistic effect on the total activity and the nighttime activity, but an antagonistic effect on daytime activity. The significant interaction between noise and light treatment also differed among forest and city birds. Indeed, we detected a significant interactive effect on light and noise on daytime, nighttime, dusktime and offset of activity of urban birds, but not of forest birds. These results suggest that both artificial light at night and anthropogenic noise can drive changes in activity patterns, but that the specific impacts depend on the habitat of origin. Furthermore, our results demonstrate that co-occurring exposure to noise and light can lead to a stronger impact at night than predicted from the additive effects and thus that multisensory pollution may be a considerable threat for wildlife.