Evolution of deceptive and true courtship songs in moths

Abstract

Ultrasonic mating signals in moths are argued to have evolved via exploitation of the receivers' sensory bias towards bat echolocation calls. We have demonstrated that female moths of the Asian corn borer are unable to distinguish between the male courtship song and bat calls. Females react to both the male song and bat calls by "freezing", which males take advantage of in mating (deceptive courtship song). In contrast, females of the Japanese lichen moth are able to distinguish between the male song and bat calls by the structure of the sounds; females emit warning clicks against bats, but accept males (true courtship song). Here, we propose a hypothesis that deceptive and true signals evolved independently from slightly different precursory sounds; deceptive/true courtship songs in moths evolved from the sounds males incidentally emitted in a sexual context, which females could not/could distinguish, respectively, from bat calls.

Figure 1. Examples of sound stimuli.

Male songs of (A) the Asian corn borer Ostrinia furnacalis and (B) the Japanese lichen moth Eilema japonica japonica. Simulations of terminal phase calls of (C) the big brown bat Eptesicus fuscus (FM bat) and (D) the Japanese greater horseshoe bat Rhinolophus ferrumequinum nippon (CF bat). Magnified images of sound-producing organs, forewing and thoracic scales of the Asian corn borer and a thoracic tymbal of the Japanese lichen moth, are also shown. Scale bar, 500 μm. Images of bats are courtesy of J. A. Simmons and S. Hiryu (E. fuscus), and Y. Sato (R. f. nippon).

Figure 2. Effects of sound stimuli on the mating success and bat-avoidance responses in the Asian corn borer.

(A) Mating success of intact females with muted males under the influence of different sound stimuli. Sample sizes are denoted on each column. (B) The number of copulation attempts that a courting male, which could not achieve copulation by artificially damaged genital claspers, could repeat while the female remained stationary by different sound stimuli. A large number means that the females' escape behavior was suppressed in the course of courtship. Box-and-whisker plots show the median, first/third quartile, and range within 1.5 times the difference between each quartile and median. n = 20 pairs in each stimulus. The natural male song indicates the sound produced by sham-operated male, which served as a positive control (A, B). **p < 0.01. (C–G) Proportion of females that ceased releasing sex pheromone in response to sound stimuli. n = 15 females in each combination of sound stimuli and sound levels (n = 120 in each sound stimulus; n = 480 in total). (H–L) Proportion of tethered moths that showed evasive flight. n = 5–6 males and 5–6 females with 5–15 replicates in each combination of sound stimuli and sound levels. Effects of (C, H) male song playback, (D, I) simulated FM bat calls, (E, J) simulated CF bat calls, and (F, K) a continuous sine wave. Error bars represent the standard error of the mean. (G, L) Logistic regression curves for each stimulus. Some data were obtained from our previous studies.

Figure 3. Effects of sound stimuli on the mating success and bat-avoidance responses in the Japanese lichen moth.

(A) Mating success between females (♀) and males (♂), which underwent different surgical operations. Intact pairs served as a positive control. Sample sizes are denoted on each column. (B) Mating success of intact females with muted males under the influence of different sound stimuli. The natural male song indicates the sound produced by sham-operated male, which served as a positive control. Sample sizes are denoted on each column. (C) Phonoresponse (click production) of stationary moths to different sound stimuli. n = 10 males and 10–13 females with 5 replicates in each sound stimulus. (D) Phonoresponse, (E) evasive flight response, and (F) the sum of the phonoresponses and evasive flight responses of tethered flying moths to sound stimuli. Note that some moths showed both responses to a single stimulus. n = 6–8 males and 9–10 females with 3–10 replicates in each sound stimulus. Stimuli were all presented at 98 dB at the position of the moth. The male song served as a positive control in C–F. Error bars represent the standard error of the mean. **p < 0.01 and ***p < 0.0001.

Figure 4. Evolution of deceptive and true courtship songs in moths.

(A) In the Asian corn borer, female receivers freeze in response to bat calls (i) and a male song (ii). The male signaler can easily copulate with the female immobilized by the deceptive signal. (B) In the Japanese lichen moth, females return phonoresponses to bat calls (i) but recognize the male sound as a courtship song (ii). The male signaler can copulate with the female that has become receptive. (C) A hypothesis on the evolutionary processes of deceptive and true courtship songs in moths. Deceptive courtship songs evolved from the sounds males incidentally emitted, which females were unable to discriminate from bat calls (a). On the other hand, true courtship songs evolved from the sounds males incidentally emitted, which females were able to discriminate from bat calls (b). In this case, male ultrasound is likely to have been meaningless at first but subsequently may have evolved into an attractive mating signal via coevolutionary sexual selection. The bat image is courtesy of M. B. Fenton.

Figure 5. Evolution of acoustic communication in moths.

Features of intraspecific acoustic communication and hearing mapped onto a molecular phylogeny of Lepidoptera modified from Regier et al.. Songs with verified function(s) are denoted with asterisks. ^§The Asian corn borer moth and Japanese lichen moth belong to Crambidae and Arctiidae, respectively. Bombycidae, Lacturidae, and Cossidae are divided into a few groups denoted as I–III.