Matched Filters, Mate Choice and the Evolution of Sexually Selected Traits

Background: Fundamental for understanding the evolution of communication systems is both the variation in a signal and how this affects the behavior of receivers, as well as variation in preference functions of receivers, and how this affects the variability of the signal. However, individual differences in female preference functions and their proximate causation have rarely been studied.

Methodology/Principal Findings: Calling songs of male field crickets represent secondary sexual characters and are subject to sexual selection by female choice. Following predictions from the ‘‘matched filter hypothesis’’ we studied the tuning of an identified interneuron in a field cricket, known for its function in phonotaxis, and correlated this with the preference of the same females in two-choice trials. Females vary in their neuronal frequency tuning, which strongly predicts the preference in a choice situation between two songs differing in carrier frequency. A second ‘‘matched filter’’ exists in directional hearing, where reliable cues for sound localization occur only in a narrow frequency range. There is a strong correlation between the directional tuning and the behavioural preference in no-choice tests. This second ‘‘matched filter’’ also varies widely in females, and surprisingly, differs on average by 400 Hz from the neuronal frequency tuning.

Conclusions/Significance: Our findings on the mismatch of the two ‘‘matched filters’’ would suggest that the difference in these two filters appears to be caused by their evolutionary history, and the different trade-offs which exist between sound emission, transmission and detection, as well as directional hearing under specific ecological settings. The mismatched filter situation may ultimately explain the maintenance of considerable variation in the carrier frequency of the male signal despite stabilizing selection.