Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects

Abstract

Mate choice is considered an important influence in the evolution of mating signals and other sexual traits, and--since divergence in sexual traits causes reproductive isolation--it can be an agent of population divergence. The importance of mate choice in signal evolution can be evaluated by comparing male signal traits with female preference functions, taking into account the shape and strength of preferences. Specifically, when preferences are closed (favouring intermediate values), there should be a correlation between the preferred values and the trait means, and stronger preferences should be associated with greater preference-signal correspondence and lower signal variability. When preferences are open (favouring extreme values), signal traits are not only expected to be more variable, but should also be shifted towards the preferred values. We tested the role of female preferences in signal evolution in the Enchenopa binotata species complex of treehoppers, a clade of plant-feeding insects hypothesized to have speciated in sympatry. We found the expected relationship between signals and preferences, implicating mate choice as an agent of signal evolution. Because differences in sexual communication systems lead to reproductive isolation, the factors that promote divergence in female preferences--and, consequently, in male signals--may have an important role in the process of speciation.

Figure 1

(a) Spectrogram and waveform of a recording of a signal produced by a male E. binotata ‘Viburnum’. (b) Bout consisting of four signals that increase in amplitude.

Figure 2

Proportion of females responding to stimuli varying in frequency, whine length, signal number, signal interval, pulse number and pulse rate. Each column corresponds to one species. Dots indicate the proportion of females that responded; lines indicate the spline regressions of those proportions ±1 s.e. The x-axes show the range of variation tested for each signal trait, which corresponds to the range in the E. binotata species complex.

Figure 3

Comparison of preferences and signals. Curves indicate spline regressions as in figure 2, shown are the ±1 s.e. curves for frequency and whine length to emphasize species differences in preference peaks. For other preferences, differences lay in the shape rather than in the peaks, so we only show the regression curves for simplicity. Histograms show the distribution of male traits. Species are indicated by colours: black, E. binotata ‘Cercis’; red, E. binotata ‘Viburnum’; green, E. binotata ‘Ptelea’; blue, E. binotata ‘Celastrus’.

Figure 4

Preference–signal relationships. Species are indicated by colours as in figure 3. (a(i), (ii)) For frequency and whine length there was a strong correlation between preference peaks and mean signal values; dashed lines indicate a 1:1 relationship. (a(iii)) Stronger closed preferences were associated with smaller preference–signal mismatches. (b(i), (ii)) Preference, strength influenced signal trait CVs for closed but not for open preferences. (b(iii)) Closed preferences were stronger than open preferences. (c) Closed preferences were associated with lower signal trait CVs than open preferences.