Sarah L. Bush

Non-parallel coevolution of sender and receiver in the acoustic communication system of treefrogs

Advertisement calls of closely related species often differ in quantitative features such as the repetition rate of signal units. These differences are important in species recognition. Current models of signal–receiver coevolution predict two possible patterns in the evolution of the mechanism used by receivers to recognize the call: (i) classical sexual selection models (Fisher process, good genes/indirect benefits, direct benefits models) predict that close relatives use qualitatively similar signal recognition mechanisms tuned to different values of a call parameter; and (ii) receiver bias models (hidden preference, pre–existing bias models) predict that if different signal recognition mechanisms are used by sibling species, evidence of an ancestral mechanism will persist in the derived species, and evidence of a pre–existing bias will be detectable in the ancestral species. We describe qualitatively different call recognition mechanisms in sibling species of treefrogs. Whereas Hyla chrysoscelis uses pulse rate to recognize male calls, Hyla versicolor uses absolute measurements of pulse duration and interval duration. We found no evidence of either hidden preferences or pre–existing biases. The results are compared with similar data from katydids (Tettigonia sp.). In both taxa, the data are not adequately explained by current models of signal–receiver coevolution.

Pulse-rate recognition in an insect: evidence of a role for oscillatory neurons.

Various mechanisms have been proposed as the neural basis for pulse-rate recognition in insects and anurans, including models employing high- and low-pass filters, autocorrelation, and neural resonance. We used the katydid Tettigonia cantans to test these models by measuring female responsiveness on a walking compensator to stimuli varying in temporal pattern. Each model predicts secondary responses to certain stimuli other than the standard conspecific pulse rate. Females responded strongly to stimuli with a pulse-rate equal to half the standard rate, but not to stimuli with double the standard rate. When every second pulse or interval was varied in length, females responded only when the resulting stimuli were rhythmic with respect to the period of the standard signal. These results provide evidence rejecting the use of either high-/low-pass filter networks or autocorrelation mechanisms. We suggest that rate recognition in this species relies on the resonant properties of neurons involved in signal recognition. According to this model, signals with a pulse rate equal to the resonant frequency of the neurons stimulate the female to respond. The results are discussed with regard to both neural and evolutionary implications of resonance as a mechanism for signal recognition.

Selective Phonotaxis by Males in the Majorcan Midwife Toad

Males are expected to exhibit mating preferences when there is high variance in the quality of females or when males are limited to a small number of matings. In the Majorcan midwife toad, Alytes muletensis, the male performs parental care by carrying the eggs wrapped in a string around his hind legs. Both sexes possess courtship vocalizations which they use to advertise receptivity. We looked for evidence of male mating preferences in a phonotaxis arena in which males were presented with two alternative synthetic female calls. We predicted that males should prefer to mate with large females because of maternal effects on egg size, and that this preference would be manifest by selective phonotaxis toward low frequency calls. We also predicted that males should prefer high intensity calls as indicators of the energetic or motivational state of the female. Contrary to our prediction, males did not exhibit a preference for low frequency calls. The results suggest that there is stabilizing selection on call frequency and directional selection on call intensity.

A complex mechanism of call recognition in the katydid Neoconocephalus affinis (Orthoptera: Tettigoniidae)

SUMMARY Acoustic pattern recognition is important for bringing together males and females in many insect species. We used phonotaxis experiments on a walking compensator to study call recognition in the katydid Neoconocephalus affinis, a species with a double-pulsed call and an atypically slow pulse rate for the genus. Call recognition in this species is unusual because females require the presence of two alternating pulse amplitudes in the signal. A Fourier analysis of the stimulus-envelopes revealed that females respond only when both the first and second harmonics of the AM spectrum are of similar amplitude. The second harmonic is generated by the amplitude difference between the two pulses making up a pulse-pair. Females respond to double pulses that have been merged into a single pulse only if this amplitude modulation is preserved. Further experiments suggest that females use a resonance mechanism to recognize the pulse rate of the call, supporting a neural model of rate recognition in which periodic oscillations in membrane potential are used to filter the pulse rate of the signal. Our results illustrate how a reduction in pulse rate extends the opportunities for females to evaluate fine-scale temporal properties of calls, and provide further evidence for the importance of oscillatory membrane properties in temporal processing. The results are discussed with regard to evolutionary changes in call recognition mechanisms within the genus.

Resonant neurons and bushcricket behaviour

The resonant properties of the intrinsic dynamics of single neurons could play a direct role in behaviour. One plausible role is in the recognition of temporal patterns, such as that seen in the auditory communication systems of Orthoptera. Recent behavioural data from bushcrickets suggests that this behaviour has interesting resonance properties, but the underlying mechanism is unknown. Here we show that a very simple and general model for neural resonance could directly account for the different behavioural responses of bushcrickets to different song patterns.

PHONOTAXIS BY FEMALE MAJORCAN MIDWIFE TOADS, ALYTES MULETENSIS

Female choice based on male call characteristics has been experimentally demonstrated in a number of species of anurans. In the Majorcan midwife toad, the male performs parental care by carrying the eggs in a string around his hind legs until they are ready to hatch. Both sexes produce calls to advertise sexual receptivity and both show phonotaxis towards the calls of the opposite sex. We used two-choice phonotaxis experiments to investigate whether females assess male caretaking ability using variation in call characteristics. Both call frequency and call duration are good indicators of male size, a characteristic that potentially influences the ability of males to successfully brood a clutch. Variation in call repetition rate and call intensity may also reflect differences in male caretaking ability, given the high energetic demands of calling behaviour in anurans. We predicted that females should prefer to mate with larger males and that this would be manifest in selective phonotaxis to low frequency and/or long duration calls. We also predicted that they would prefer calls produced at a fast rate and a high intensity. Contrary to our predictions females did not prefer lower frequency calls, longer calls or louder calls. They did however, selectively approach calls produced at a faster rate. These results are discussed in the context of sexual selection theory.

Evolution of novel signal traits in the absence of female preferences in Neoconocephalus katydids (Orthoptera, Tettigoniidae).

Background Significance Communication signals that function to bring together the sexes are important for maintaining reproductive isolation in many taxa. Changes in male calls are often attributed to sexual selection, in which female preferences initiate signal divergence. Natural selection can also influence signal traits if calls attract predators or parasitoids, or if calling is energetically costly. Neutral evolution is often neglected in the context of acoustic communication. Methodology/Principal Findings We describe a signal trait that appears to have evolved in the absence of either sexual or natural selection. In the katydid genus Neoconocephalus, calls with a derived pattern in which pulses are grouped into pairs have evolved five times independently. We have previously shown that in three of these species, females require the double pulse pattern for call recognition, and hence the recognition system of the females is also in a derived state. Here we describe the remaining two species and find that although males produce the derived call pattern, females use the ancestral recognition mechanism in which no pulse pattern is required. Females respond equally well to the single and double pulse calls, indicating that the derived trait is selectively neutral in the context of mate recognition. Conclusions/Significance These results suggest that 1) neutral changes in signal traits could be important in the diversification of communication systems, and 2) males rather than females may be responsible for initiating signal divergence.

Why is double clutching rare in the Majorcan midwife toad

In species with male parental care, multiple clutching is the provisioning of care to the eggs or offspring of two or more females simultaneously. Multiple clutching represents a strategy by which males reduce the reproductive costs associated with male parental care relative to the reproductive gains. Although multiple clutching is common in two species of midwife toads (Alytes obstetricansandA. cisternasii), double clutching in the Majorcan midwife toad,A. muletensis, is rare and triple clutching has never been observed. In this paper, the reasons for the low frequency of double clutching inA. muletensisrelative to the other species are examined. Two hypotheses were experimentally disproved: double clutching is not limited to particularly large males, and females do not prefer to mate with non-brooding than brooding males. The low incidence of double clutching inA. muletensisappears to result from a time constraint on males. Males only advertise for second clutches within 3 days of the first. This time limit may have evolved as a result of energetic constraints on either the duration of the brooding period of males, or the developmental plasticity of larvae. A model was constructed which illustrates that if females mate randomly with respect to the brooding status of males, the time limit for obtaining a second clutch partially explains the differences in frequencies of double clutching observed betweenA. muletensisand the other species of midwife toads. The female inter-clutch interval and the male brooding period are also likely to contribute significantly to the rate of double clutching in a population.

Evolution of Call Patterns and Pattern Recognition Mechanisms in Neoconocephalus Katydids

In the katydid genus Neoconocephalus, males typically produce continuous calls with an extremely fast pulse rate of about 200/s. Divergence from this ancestral pattern includes alternation of pulse periods resulting in a double-pulse pattern, and the grouping of pulses into chirps. Double-pulse patterns evolved five times independently in the genus. Analysis of the female preferences and call recognition mechanisms revealed that in three species with double-pulse pattern, females have independently evolved new mechanisms for recognizing the derived call pattern. In the remaining two species with double-pulse pattern, females retain the ancestral recognition mechanism and exhibit no preference for the derived temporal pattern. These results suggest that males are leading the evolutionary divergence of call patterns in this genus. We propose a hypothetical scenario in which genetic bottlenecks and founder effects arising from the climatic history of North America contributed to the rapid diversification of calls in this genus.

Nonparallel coevolution of sender and receiver in the acoustic communication system of treefrogs

Advertisement calls of closely related species often differ in quantitative features such as the repetition rate of signal units. These differences are important in species recognition. Current models of signal/receiver co‐evolution predict two possible patterns in the evolution of the mechanism used by receivers to recognize the call. (1) Classical sexual selection models (Fisher‐Process, good‐genes/indirect benefits, direct benefits models) predict that close relatives use qualitatively similar signal recognition mechanisms tuned to different values of a call parameter. (2) Receiver bias models (hidden preference, pre‐existing bias models) predict that if different signal recognition mechanisms are used by sibling species, evidence of an ancestral mechanism will persist in the derived species, and evidence of a pre‐existing bias will be detectable in the ancestral species. We describe qualitatively different call recognition mechanisms in sibling species of treefrogs. Whereas Hyla chrysoscelis uses puls...