BackgroundMale field crickets produce pure-tone calling songs to attract females. Receivers are expected to have evolved a "matched filter" in the form of a tuned sensitivity for this frequency. In addition, the peripheral directionality of field crickets is sharply tuned as a result of a pressure difference receiver. We studied both forms of tuning in the same individuals of four species of cricket, where Gryllus bimaculatus and G. campestris are largely allopatric, whereas Teleogryllus oceanicus and T. commodus occur also sympatrically.ResultsThe sharpness of the sensitivity filter is highest for T. commodus, which also exhibits low interindividual variability. Individual receivers may also vary strongly in the best frequency for directional hearing. In G. campestris, such best frequencies occur even at frequencies outside the range of carrier frequencies of males. Contrary to the predictions from the "matched filter hypothesis", in three of the four species the frequency optima of the two involved filters are not matched to each other, and the mismatch can amount to 1.2 kHz. The mean carrier frequency of the male population is between the frequency optima of both filters in three species. Only in T. commodus we found a match between both filters and the male carrier frequency.ConclusionOur results show that a mismatch between the sensitivity and directionality tuning is not uncommon in crickets, and an observed match (T. commodus) appears to be the exception rather than the rule. The data suggests that independent variation of both filters is possible. During evolution each sensory task may have been driven by independent constraints, and may have evolved towards its own respective optimum.
How neural networks evolve to recognize species-specific communication signals is unknown. One hypothesis is that novel recognition phenotypes are produced by parameter variation in a computationally flexible “mother network”. We test this hypothesis in crickets, where males produce and females recognize mating songs with a species-specific pulse pattern. Whether the song recognition network in crickets is computationally flexible to recognize the diversity of pulse patterns and what network properties support and constrain this flexibility is unknown. Using electrophysiological recordings from the cricket Gryllus bimaculatus, we built a model of the song recognition network that reproduces the network dynamics as well as the neuronal and behavioral tuning for that species. An analysis of the model’s parameter space reveals that the network can produce all recognition phenotypes known in crickets and even other insects. Biases in phenotypic diversity produced by the model are consistent with the existing behavioral diversity in crickets, and arise from computations that likely evolved to increase energy efficiency and robustness of song recognition. The model’s parameter to phenotype mapping is degenerate – different network parameters can create similar changes in the phenotype – which is thought to support evolutionary plasticity. Our study suggest that a computationally flexible mother network could underlie the diversity of song recognition phenotypes in crickets and we reveal network properties that constrain and support behavioral diversity.
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