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Variation in Courtship Ultrasounds of Three Ostrinia Moths With Different Sex Pheromones

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Variation in Courtship Ultrasounds of Three Ostrinia Moths With Different Sex Pheromones

Takuma Takanashi et al. PLoS One.

Abstract

Moths use ultrasounds as well as pheromones for sexual communication. In closely related moth species, variations in ultrasounds and pheromones are likely to profoundly affect mate recognition, reproductive isolation, and speciation. The European corn borer, Ostrinia nubilalis, and its Asian congeners, Ostrinia furnacalis and Ostrinia scapulalis, exhibit within-species and between-species variation in their pheromone communication. Recently, we reported ultrasound communication in O. furnacalis; however, variations in ultrasounds in the three congeners have not been addressed to date. Here we investigated features of ultrasound production and hearing in O. nubilalis and O. scapulalis, and compared them with those of O. furnacalis. As in O. furnacalis, males of O. nubilalis and O. scapulalis produced ultrasounds during courtship by rubbing specialized scales on the wings against scales on the thorax. The covering of these scales with nail polish muffled the sounds and significantly reduced mating success in O. nubilalis, showing the importance of ultrasound signaling in mating. The ultrasounds produced by O. nubilalis and O. scapulalis were similar, consisting of long trains of pairs of pulses with a main energy at 40 kHz, but distinctly different from the ultrasound produced by O. furnacalis, consisting of groups of pulses peaking at 50 kHz and with substantially more energy up to 80 kHz. Despite overall similarities, temporal features and patterns of amplitude modulation differed significantly among the geographic populations of O. nubilalis and O. scapulalis, which differed in pheromone type. In contrast, no significant difference in hearing was found among the three species with regard to the most sensitive frequencies and hearing threshold levels. The patterns of variations in the songs and pheromones well reflected those of the phylogenetic relationships, implying that ultrasound and pheromone communications have diverged concordantly. Our results suggest that concordant evolution in sexual signals such as courtship ultrasounds and sex pheromones occurs in moths.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Phylogenetic relationships of Ostrinia moths and sex pheromones.
Minor components of sex pheromones are indicated by an asterisk. O. nubilalis and O. scapulalis exhibit polymorphism in sex pheromones (Z and E types). Z11-14:OAc, E11-14:OAc, Z12-14:OAc, and E12-14:OAc denote (Z)-11-tetradecenyl acetate, (E)-11-tetradecenyl acetate, (Z)-12-tetradecenyl acetate, and (E)-12-tetradecenyl acetate, respectively. The phylogenetic tree was constructed by the neighbor-joining method using mitochondrial COII gene sequences .
Figure 2
Figure 2. Ultrasound-producing scales on the wings and thoraxes of the males of O. nubilalis and O. scapulalis.
A) Photograph showing areas bearing the male-specific scales (indicated by dotted boxes) in O. nubilalis (Z type, Darmstadt). Left and right arrowheads indicate the male-specific scales on the right of the notum (dorsal plate of mesothorax) and basal part of the right forewing, respectively. The right tegula was removed to show the male-specific scales. Scale bar: 500 µm. B, C) Scanning electron micrographs showing male-specific scales (indicated by a black dotted ellipse) on the right mesothorax (B) and on the right forewing (white dotted ellipse) in O. nubilalis (Z type, Darmstadt) (C). D, E) Male-specific scales (black dotted ellipse) on the right mesothorax (D) and those (white dotted ellipse) on the right forewing in O. scapulalis (E type, Matsudo) (E). Note that some scales have naturally fallen out. Scale bars: B–E, 200 µm. See Table 1 for collection sites of the populations examined.
Figure 3
Figure 3. Courtship ultrasounds of O. nubilalis, O. scapulalis, and O. furnacalis.
A) Ultrasounds of O. nubilalis (Z type, Darmstadt). Upper: oscillogram showing the entire song train. Middle: expanded oscillogram showing pulse pairs including pulse 1 (P1) and pulse 2 (P2), which exhibit different temporal features and amplitudes. Lower: spectrogram of the three pulse pairs. P1 is defined as the pulse in a pulse pair with the shorter pulse interval. PD and PI denote pulse duration and pulse interval, respectively. B) Pulse pairs of O. scapulalis (Z type, Morioka). C) A pulse group of O. furnacalis. Audio files of Z-type O. nubilalis, Z-type O. scapulalis and O. furnacalis are available online in the supplementary materials (Audio S1, S2, and S3). See Table 1 for collection sites of the populations examined.
Figure 4
Figure 4. The frequency–sound pressure level distribution of pulses in O. nubilalis, O. scapulalis, and O. furnacalis.
Black lines are spectra of pulse 1 (P1), and red lines are those of pulse 2 (P2). A) Thin lines are individual spectra of P1 and P2, and thick lines are the mean spectra of P1 and P2 in Z-type O. nubilalis (Darmstadt, n = 5). One spectrum with low peak level of P2 differed from all others, and might be a noise. B) Solid lines are the mean spectra of P1 and P2 in Z-type O. nubilalis (Toulouse, n = 9), and dotted lines are the mean spectra of P1 and P2 in E-type O. nubilalis (Warloy, n = 5). C) Solid lines are the mean spectra of P1 and P2 in Z-type O. scapulalis (Morioka, n = 7), and dotted lines are the mean spectra of P1 and P2 in E-type O. scapulalis (Furukawa, n = 7). The blue line is the mean spectrum of O. furnacalis (n = 5) obtained from Nakano et al. (2008) . See Table 1 for collection sites of the populations examined.
Figure 5
Figure 5. Autocorrelation coefficients of pulse amplitudes in O. nubilalis and O. scapulalis.
A) Examples of waveforms of pulse 1 in Z-type O. nubilalis (Toulouse) and in E-type O. nubilalis (Warloy). Two figures are drawn to the same scale. B) The autocorrelation coefficients of the amplitudes were calculated up to 30 lags corresponding to 0.1 ms in Z-type O. nubilalis (Toulouse) (left) and E-type O. nubilalis (Warloy) (right). C) Plots of the first two canonical variate scores for autocorrelation coefficients of pulse envelops in O. nubilalis and O. scapulalis (n = 33). Ninety-five percent confidence ellipses of the centroid of the first two canonical variate scores are shown. The first and second canonical variates (CV1 and CV2) explained 73.9% of the total variance (46.8% attributed to CV1, and 27.1% to CV2), successfully summarizing overall differences. nub Z, Z-type O. nubilalis (Darmstadt and Toulouse); nub E, E-type O. nubilalis (Warloy); sca Z, Z-type O. scapulalis (Morioka); sca E, E-type O. scapulalis (Furukawa). P1 and P2 denote pulse 1 and pulse 2, respectively. See Table 1 for collection sites of the populations examined.
Figure 6
Figure 6. Hearing threshold curves in O. nubilalis and O. scapulalis.
A) Black lines are hearing threshold curves obtained from four females of Z-type O. nubilalis (Darmstadt), and black dotted lines are those from three males. The red line is a curve from both sexes (n = 7). B) The red dotted line is a curve of E-type O. nubilalis (Paris, n = 5 for both sexes). The black line is a curve of Z-type O. scapulalis (Matsudo, n = 6) and black dotted line, E-type O. scapulalis (Matsudo, n = 6). The blue line is a curve from pooled populations of the two species. All curves were drawn using tensor product smoothers implemented by generalized additive models . See Table 1 for collection sites of the populations examined.

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