Bilateral coordination and the motor basis of female preference for sexual signals in canary song

Abstract

The preference of female songbirds for particular traits in the songs of courting males has received considerable attention, but the relationship of preferred traits to male quality is poorly understood. Female domestic canaries (Serinus canaria, Linnaeus) preferentially solicit copulation with males that sing special high repetition rate, wide-band, multi-note syllables, called 'sexy' or A-syllables. Syllables are separated by minibreaths but each note is produced by pulsatile expiration, allowing high repetition rates and long duration phrases. The wide bandwidth is achieved by including two notes produced sequentially on opposite sides of the syrinx, in which the left and right sides are specialized for low or high frequencies, respectively. The emphasis of low frequencies is facilitated by a positive relationship between syllable repetition rate and the bandwidth of the fundamental frequency of notes sung by the left syrinx, such that bandwidth increases with increasing syllable repetition rate. The temporal offset between notes prevents cheating by unilaterally singing a note on the left side with a low fundamental frequency and prominent higher harmonics. The syringeal and respiratory motor patterns by which sexy syllables are produced support the hypothesis that these syllables provide a sensitive vocal-auditory indicator of a male's performance limit for the rapid, precisely coordinated interhemispheric switching, which is essential for many sensory and motor processes involving specialized contributions from each cerebral hemisphere.

Fig. 1.

Portion of a canary song showing phrases of five different syllables. Songs vary in length and in the number of syllable types they contain. Depending on the individual male, some songs may contain phrases of sexy A-syllables. Sometimes a bird sang successive phrases of different types of A-syllable, often in a sequence with other high repetition rate non-sexy syllables. In this figure, two minibreath A-phrases composed of syllables Ap and Ax are preceded by a phrase of nearly constant frequency m-syllables sung at a low repetition rate and followed by unilaterally produced frequency modulated (FM) syllables n and c. Although the repetition rate of syllables n and c is comparable to that of the sexy syllables, they consist of a single note and their bandwidth is considerably less than that of the preceding A-syllables. Syllable n is sung on the right side with the left side of the syrinx closed during the entire phrase. F_R, airflow through the right bronchus; F_L, airflow through the left bronchus; P, pressure in the cranial thoracic air sac; V, time waveform of song. Horizontal lines indicate zero flow and ambient (zero) pressure. As both inspiratory and expiratory airflow cools the heated thermistor bead, both inspiratory and expiratory airflow produce an upward deflection of the airflow signal. The direction of airflow depends on whether the subsyringeal air sac pressure is less than (inspiration) or greater than (expiration) the external ambient pressure. Phonation during song by these canaries was always accompanied by expiratory airflow. L and R in the spectrogram indicate notes produced on the left or right side of the syrinx, respectively. Syllable type (Syl; each syllable type is identified by a lowercase letter, which is preceded by ‘A’ if the syllable is A-type) is indicated at the top of the figure.

Fig. 2.

Examples of complex syllables sung at high repetition rates. Inspiratory airflow is shaded. (A) The end and beginning of successive phrases containing sexy syllables Ax and Ap, respectively. The first note of both syllable types is produced on the right side of the syrinx and consists of an upward frequency sweep. In syllable Ap the frequency range of this note is shifted upward, minimizing frequency overlap that is present between notes in syllable Ax. The first note in syllable Ap also acquires a small downward ‘hook’ at the top, suggesting tension on the right labia has peaked and is beginning to decrease. The first note is followed immediately, without an intervening minibreath, by a downward sweeping note from the left half of the syrinx. This note is the same in the two syllable types so that, in this example, syllable type is determined by the motor program to the right syrinx and a slight change in the frequency of the respiratory motor program. A minibreath after each syllable replaces the air exhaled to produce both notes. (B) End of a sexy syllable Az phrase and beginning of a phrase with syllable v. The first note of syllable Az is from the right side of the syrinx and is followed immediately by a note from the left side, which remains closed during the subsequent minibreaths between syllables. Syllable v is produced mainly or entirely on the left side. It does not contain two notes and is not a sexy syllable. Repetition rate is indicated at the top of the figure. Open triangles indicate irregular, low amplitude expiratory airflow through the right side of the syrinx, which may contribute a low amplitude sound at about 2.5 kHz simultaneously with the high amplitude sound generated by the high flow rate through the left side of the syrinx. Note that the time constant of the thermistor in the left bronchus does not allow the signal to return to zero between expiration and inspiration. Arrows indicate transitional syllables. Solid triangles indicate the side of the syrinx that is closed during inspiration, resulting in a unilateral minibreath. See legend of Fig. 1 for other symbols.

Fig. 3.

A pulsatile trill that includes a contribution from each side of the syrinx. Air sac pressure remains positive during the trill. The left syrinx opens and closes at a repetition rate of 32 s^–1 to produce a series of brief FM sweeps with most of their energy between about 1 and 3.3 kHz. The right syrinx opens out of phase with the left to generate more nearly tonal sounds at about 3.3 kHz between each FM note. Trill follows a phrase of slow tonal notes creating a striking temporal and spectral contrast.

Fig. 4.

Relationship between syllable repetition rate and bandwidth. (A) All syllable types sung by the three birds. R²=0.017, P=0.321, N=59. (B) Bilaterally produced syllables with components from each side of the syrinx. R²=0.103, P=0.284, N=25. (C) Syllables produced on the left side of the syrinx. R²=0.662, P<0.001, N=20. (D) Syllables produced on the right side of the syrinx. R²=0.035, P=0.370, N=25. The open symbols in A and B are A-syllables. Dashed lines indicate the 95% confidence interval.

Fig. 5

Each syllable type recorded from 3 birds singing with their vocal system intact, plotted according to its fundamental bandwidth, repetition rate and lowest frequency. A-syllables (red circles), including all two-note syllables at repetition rates ≥15 syllables s^–1, stand out from the rest of the repertoire. A-syllable types 1–6 were separated by minibreaths; type 7 (see Fig. 3) was produced by pulsatile expiration but contained two notes. The remaining four two-note syllables (yellow circles) were sung at lower repetition rates and two had a relatively narrow bandwidth. Two syllables (orange squares) included flow through both sides of the syrinx but consisted of only one note. Syllables produced by the left syrinx alone (green triangles) generally had lower fundamental frequencies than syllables produced only by the right syrinx (inverted blue triangles). The high repetition rate left side syllable marked by an asterisk was produced by pulsatile expiration and had one note. Gray horizontal lines from the symbols to the grid at the back of the figure are provided to accurately indicate syllable repetition rates.

Fig. 6.

Examples of complex syllables sung at rates of >15 syllables s^–1 by birds with one side of the syrinx disabled. The syllables in A–C were sung by birds that had their bronchus plugged and tracheosyringeal nerve cut on the right side. The syllable in D, sung by a bird with a bronchial plug and tracheosyringeal nerve cut on the left side, has some amplitude modulation but does not contain distinct notes. Horizontal band of noise just above syllables in B is environmental sound not produced by bird. Number in lower right corner identifies individual bird.

Fig. 7.

The importance of using both sides of the syrinx to produce sexy syllables is illustrated by the properties of unilateral two-note syllables sung by domestic canaries after the right side of their syrinx was disabled by denervation and a bronchial plug [data from Suthers et al. (Suthers et al., 2004)]. After surgery, all pre-operative multinote syllables with repetition rates >13 syllables s^–1 disappeared from the post-operative repertoire, but 3 of 4 birds with the left side of their syrinx intact added between two and five new, high repetition rate (>15 syllables s^–1) multinote syllables to their post-operative repertoires. These unilateral multinote syllables differed from sexy syllables in having a narrow bandwidth (2.1±0.5 kHz, N=11 post-operative left syllables versus 4.1±1.0 kHz, N=7 intact sexy syllables). They were also low intensity and had a simpler, more poorly differentiated note structure compared with sexy syllables. Birds with a bilaterally intact vocal system never sang high repetition rate, unilateral, two-note syllables. Different light blue symbol shapes represent different birds. Red circles are sexy syllables.