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Munoz, M. I.

Publications and source records attributed to Munoz, M. I..

7 recordsLinked to original sources

Optimal tuning not required: Birds communicate effectively with mismatched auditory filters.

Birds have one of the most remarkable vocal capacities of vertebrates. Yet we know little about the relationship between their hearing and their vocal capacities at large phylogenetic scales, and whether these traits coevolve in a tight or loose fashion. Here we collected vocal and auditory data for 72 bird species from 15 different orders, and tested if hearing is finely tuned to the spectral composition of their vocalizations (i.e., the matched-filter hypothesis). We found bird audition not to be predictive of vocal frequency, and mismatches between hearing and vocalizations to be widespread. We show that the source of these mismatches is allometric: the auditory tuning and the spectral composition of vocalizations scale with body weight to different degrees. Despite the general frequency mismatches, bird hearing remains remarkably sensitive to the main spectral component of their vocalizations. Our results challenge the view that sensory systems must be finely tuned only to conspecific signals for communication to be effective. Our results suggest that selection for a broad auditory tuning has allowed birds to effectively communicate with conspecifics while at the same time permitting general environmental awareness using auditory cues. We argue that the relationship between hearing and vocalizations in birds is better described by the concept of diffuse coevolution, where organism evolve in relation to their broader ecological context instead than on a strictly dyadic fashion. Significance StatementAnimal communication theory often states that signalers and perceivers coevolve, yet the spread and nature of this relationship remains unclear. We tested whether the auditory tuning of birds is tightly matched to the frequency content of their vocalizations -an expected outcome of strong coevolution and the matched-filter hypothesis. We show that although birds hearing does not precisely align with their vocalizations, birds are still highly sensitive to the sounds they produce. This is due to the broad tuning of the avian auditory systems, which supports effective conspecific communication while also allowing the detection of other ecologically relevant sounds. Thus, birds exemplify diffuse rather than tightly coupled coevolution in communication systems.

evolutionary biology↗

Aggressive responses to rivals depend on the interaction between the vocal traits of territory-holder and mimicked intruders in a miniature tropical frog

Territory defence is an important aspect of animal behaviour, and tightly linked to rival assessment and species recognition processes. An important component of these two processes is signalling, and animals must decide how to respond to a challenge based on the signals they perceive from their rivals. Here we manipulated the note repetition rate of rocket frog calls to simulate rivals with high and low vocal performances, and tested the aggressive responses of males in the field. We found that the probability of aggression depended on the interaction between the stimulus treatment and the peak frequency of the territorial males. Low-frequency calling males were more likely to respond aggressively to the fast call, while high-frequency calling males showed a higher probability of aggression towards the slow call. Frogs that responded aggressively approached the slow call 2.4-times faster than the fast call. Low-frequency calling males also increased their peak frequencies in response to the playbacks, while high-frequency calling males did not modify their vocalizations. Body weight was not correlated with the peak frequency or the inter-note interval of males. Peak frequency and amplitude (loudness) are positively interrelated in frogs, and are potential indicators of the motivational state of the signaller. We argue that low-frequency males were not singing at their maximum capacity, and they increased their vocal output when challenged by a rival, especially when the rival was a high-performance individual. We show that rocket frog aggression depends on the temporal parameters of the rival, but also on how territory-holders compare their own calls to those of challengers in terms of their frequency, and therefore demonstrate that frogs pay attention to different aspects of signals during aggressive decision-making.

animal behavior and cognition↗

Tetrapod vocal evolution: higher frequencies and faster rates of evolution in mammalian vocalizations

Using the voice to produce sound is a widespread form of communication and plays an important role in contexts as diverse as parent-offspring interactions and courtship. Variation in the tempo and mode of vocal signal evolution has been studied in a phylogenetic context within orders or classes, but understanding vocal signal evolution ultimately requires comparison across all major lineages involved. Here we used comparative analyses to investigate the evolution of dominant frequency (i.e., the frequency with the highest energy content) and its association with body weight across 873 species of mammals, birds and frogs. In agreement with previous studies, we found that the negative allometric relationship between body weight and vocal frequency is a general feature of vocal systems. In addition, we found mammals to consistently vocalize at higher frequencies, and evolved their vocalizations at around 6-fold faster rates than those of birds and frogs. Although all three groups strongly rely on vocal communication, our findings show that only mammals have extensively explored the spectral acoustic space. We argue that such high vocal diversity of mammals is made possible by their unique hearing system, which evolved in the context of a small, parental-caring, nocturnal and insectivore ancestor, and has allowed them to detect, and therefore to evolve, a richer array of frequencies than other tetrapods.

evolutionary biology↗

The efficacy of chemotherapy is limited by intratumoural senescent cells that persist through the upregulation of PD-L2

Anti-cancer therapies often result in a subset of surviving cancer cells that undergo therapy-induced senescence (TIS). Senescent cancer cells strongly modify the intratumoural microenvironment favoring immunosuppression and, thereby, tumour growth. An emerging strategy to optimise current therapies is to combine them with treatments that eliminate senescent cells. To this end, we undertook an unbiased proteomics approach to identify surface markers contributing to senescent cells immune evasion. Through this approach, we discovered that the immune checkpoint inhibitor PD-L2, but not PD-L1, is upregulated across multiple senescent human and murine cells. Importantly, blockade of PD-L2 strongly synergises with genotoxic chemotherapy, causing remission of solid tumours in mice. We show that PD-L2 inhibition prevents the persistence of chemotherapy-induced senescent cells, which exert cell-extrinsic immunomodulatory actions. In particular, upon chemotherapy, tumours deficient in PD-L2 fail to produce cytokines of the CXCL family, do not recruit myeloid-derived suppressor cells (MDSCs) and are eliminated in a CD8 T cell-dependent manner. We conclude that blockade of PD-L2 improves chemotherapy efficacy by reducing the intratumoural burden of senescent cells and their associated recruitment of immunosuppressive cells. These findings provide a novel strategy to exploit vulnerabilities arising in tumour cells as a result of therapy-induced damage and cellular senescence.

cancer biology↗

Amplification of frog calls by leaf substrates: implications for terrestrial and arboreal species

Signal detection is a minimum requirement for any communicative interaction. Acoustic signals, however, often experience amplitude losses during their transmission through the environment, reducing their detection range. Displaying from sites that increase the amplitude of the sound produced, such as cavities or some reflective surfaces, can improve the detectability of signals by distant receivers. Understanding how display sites influence sound production is, however, far from understood. We measured the effect of leaf calling sites on the calls of an arboreal (Hyalinobatrachium fleischmanni) and a leaf-litter specialist (Silverstoneia flotator) frog species. We collected the leaves where males of both species were observed calling, and conducted playback experiments to measure their effect on the amplitude of frog calls. Overall, the leaves used by H. fleischmanni and S. flotator were of similar dimensions, and amplified the calls of each species by about 5.0 and 2.5 dB, respectively. The degree of call amplification was unrelated to leaf dimensions or the position of the frogs on the leaves, but explained by the different frequency content of the calls of each species. Depending on the spatial location of intended and unintended receivers, we suggest that amplification of frog calls by leaves could represent either a benefit or impose costs for arboreal and terrestrial species. We argue that the microhabitat of the substrate from which animals display needs to be considered when addressing signal evolution. Lay summaryAnimals produce signals from specific locations in the environment, yet we know surprisingly little about the effects of the small-scale habitat on animal communication. Here we show that the calls of a terrestrial and an arboreal frog species are amplified by the leaves they use as calling sites. We argue that the consequences of this enhancement need to be considered in relation to the spatial location of intended (males and females) and unintended receivers (predators and parasites).

animal behavior and cognition↗

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 between individuals, one widely recognized factor is the structure of the environment in which signals are produced, transmitted and received. 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 will impose different constraints on sound production and transmission and may therefore drive signal evolution. Here, we used comparative phylogenetic analyses to assess the relationship between the display site properties and the structure of reproductive calls from 161 frog species from the frog families Ranidae, Leptodactylidae and Hylidae. Specifically, we compared the dominant frequency of species that vocalize from aquatic versus non-aquatic sites, and its relation with body size. We found that the dominant 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 the call site had both direct and indirect effects on the dominant frequency. Indirect effects were mediated by call site influencing male body size, which in turn was negatively associated to call dominant frequency. Our results suggest that properties of display sites can drive signal evolution, most likely through morphological constraints, in particular the ones imposed on the sound production mechanism. Also, variation in body size between calling sites explained some of the differences we found in call frequency, highlighting the relevance of the interplay between morphological adaptation and signal evolution. Changes of display site may therefore have important evolutionary consequences, as it may influence sexual selection processes and ultimately may even promote speciation. Impact summaryTo attract or impress mates, animals have evolved a great diversity of communication signals, such as song and dance, or brightly colored body parts. Whether these sexual signals are successful depends to a large extent on the environment in which they are produced, transmitted and perceived. For acoustic signals, such as the mating calls of frogs, the environment is well known to influence both their transmission and perception. The impact of the environment on the production of sounds is however far less understood. Here we studied the relation between the environment and signal design across a wide range of frog species, specifically comparing calls of aquatic versus non-aquatic species. Frogs that called from water were found to call at lower pitch, which was partly explained by the fact that they were also larger. Our results point towards an important environmental driver of signal evolution, namely morphological constraints on signal production. We argue that the environment can impose limits on morphological traits that are either directly or indirectly involved in signal production. Such a mechanism would in particular be important when species move into new habitats, as rapid changes to display sites may lead to rapid changes in sexual signaling and sexual attractiveness.

evolutionary biology↗

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

In animal communication, receivers benefit from signals providing reliable information on signallers 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 senders body size and the dominant frequency of their vocalizations. Dominant frequency may however not only depend on an animals 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. More specifically, we altered water level, which forced frogs to float on the surface and tested how this manipulation affected the shuttling of air between the lungs and the vocal sac, and how this in turn impacted the calls dominant frequency. Our results show that frogs that are floating are able to fully inflate their lungs and vocal sacs, and that the associated change in airflow or air pressure is correlated with a decrease of call dominant frequency.

evolutionary biology↗