Decision-making processes, like all traits of an organism, are shaped by evolution; they thus carry a signature of the selection pressures associated with choice behaviors. The way sexual communication signals are integrated during courtship likely reflects the costs and benefits associated with mate choice. Here, we study the evaluation of male song by females during acoustic courtship in grasshoppers. Using playback experiments and computational modeling we find that information of different valence (attractive vs. nonattractive) is weighted asymmetrically: while information associated with nonattractive features has large weight, attractive features add little to the decision to mate. Accordingly, nonattractive features effectively veto female responses. Because attractive features have so little weight, the model suggests that female responses are frequently driven by integration noise. Asymmetrical weighting of negative and positive information may reflect the fitness costs associated with mating with a nonattractive over an attractive singer, which are also highly asymmetrical. In addition, nonattractive cues tend to be more salient and therefore more reliable. Hence, information provided by them should be weighted more heavily. Our findings suggest that characterizing the integration of sensory information during a natural behavior has the potential to provide valuable insights into the selective pressures shaping decision-making during evolution.O ne crucial decision in the lifetime of an animal is the decision with whom to mate. The males of many animals have evolved elaborate traits to attract females (1). These traits often involve the production of calling or courtship songs (2-4). Females base their decision to engage in courtship and to mate on the properties of these signals. Though many different factors drive and constrain the evolution of behavioral decisions in general (5, 6), the way information is integrated in the context of mate selection may reflect the fitness costs and benefits associated with mate choice. These costs depend on the mating system, e.g., the abundance of potential mating partners, the likelihood and costs of multiple matings, direct benefits of mating, and the costs of assessing a potential mate (7-10).Here, we investigate the implementation of a decision-making strategy by studying the integration of song features during courtship in grasshoppers. Acoustic courtship in the species Chorthippus biguttulus involves bidirectional communication. Males produce calling songs consisting of a sequence of simple stereotyped subunits-30-50 syllable-pause pairs. The female waits until the end of this song and indicates her readiness to further engage in a courtship ritual by producing a response song that allows the male to localize and approach the female (11) (Fig. 1A). This phase of courtship constitutes a first, important preselection step before females make their final assessment of an approaching mating partner. Not responding or responding to a male calling from a distance i...
Acoustic communication plays a key role for mate attraction in grasshoppers. Males use songs to advertise themselves to females. Females evaluate the song pattern, a repetitive structure of sound syllables separated by short pauses, to recognize a conspecific male and as proxy to its fitness. In their natural habitat females often receive songs with degraded temporal structure. Perturbations may, for example, result from the overlap with other songs. We studied the response behavior of females to songs that show different signal degradations. A perturbation of an otherwise attractive song at later positions in the syllable diminished the behavioral response, whereas the same perturbation at the onset of a syllable did not affect song attractiveness. We applied naïve Bayes classifiers to the spike trains of identified neurons in the auditory pathway to explore how sensory evidence about the acoustic stimulus and its attractiveness is represented in the neuronal responses. We find that populations of three or more neurons were sufficient to reliably decode the acoustic stimulus and to predict its behavioral relevance from the single-trial integrated firing rate. A simple model of decision making simulates the female response behavior. It computes for each syllable the likelihood for the presence of an attractive song pattern as evidenced by the population firing rate. Integration across syllables allows the likelihood to reach a decision threshold and to elicit the behavioral response. The close match between model performance and animal behavior shows that a spike rate code is sufficient to enable song pattern recognition.
Noise is a challenge for animals that use acoustic communication to find a mate. A potent source of noise in animal communication is that arising from other conspecific signals, whose co-occurrence can result in extensive interference-evident as the so called "cocktail-party problem"-that may affect the receiver mechanisms to detect potential mates. We studied grasshopper females to explore how modifications of the song pattern influence song recognition. First, we degraded an attractive model song with random fluctuations of increasing amplitudes out of different frequency bands, and determined "critical degradation levels" at which the females ceased to respond. A masker band with frequencies between 0 and 200 Hz, which covers the frequency range of the natural song envelope, was by 3-5 dB more destructive in hampering signal recognition than frequencies above 200 Hz. As second approach, we applied temporal disturbances such as accentuations or gaps at different positions within the song subunits and observed how response behavior was affected. Accentuations at subunit start increased, whereas those in the midst or at the end of a subunit reduced attractiveness. Gaps at these positions had diverse effects. The results are discussed with respect to neuronal filtering.
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