Acoustic communication in the gray treefrog,Hyla versicolor: evolutionary and neurobiological implications
Acoustic communication in the gray treefrog,H. versicolor, was studied by analyzing the vocalizations of males and observing the phonotactic behavior of gravid females in response to pairs of synthetic stimuli, which usually simulated choices between calls of conspecific males at different temperatures or choices between calls of conspecific males and those of a sibling species,H. chrysoscelis. Calls ofH. chrysoscelis were also analyzed acoustically.
Pulse duty cycle (pulse duration divided by pulse period) averaged about 0.50 in the calls of both species over a wide range of temperature (Table 1). Pulse rise-time (as a percentage of pulse duration), which was also temperature-independent, was significantly longer inH. versicolor than inH. chrysoscelis (Table 1). The species difference in pulse shape was evident at a distance of 10 m from calling frogs (Fig. 1).
Females strongly preferred a linear approximation to the pulse shape (rise-time) typical of conspecific calls to an approximation of the pulse shape typical ofH. chrysoscelis (Figs. 1, 2A). Females did not show a preference between linear and exponential approximations of the conspecific pulse shape (Figs. 1, 2B).
When offered choices between synthetic calls that differed in pulse rate (pulses per s=p/s), females were usually very selective, choosing a stimulus with a pulse rate typical of a conspecific male at the test temperature over alternatives that differed by as little as 25% (Figs. 4–6). When both the call rate and pulse rate of synthetic calls were changed (Fig. 3), females showed temperature-dependent reversals in preference between 16 and 24°C (16 p/s vs 25 p/s) and between 16 and 20°C (15 p/s vs 20 p/s), but not between 20 and 24°C (20 p/s vs 25 p/s) (Table 2A–C).
When the call rates of alternative stimuli were the same, the pulse rate selectivity of females at 20°C was biased toward stimuli with low pulse rates (Table 2F). Females tested at 16°C rejected strongly alternatives with a high pulse rate, but females tested at 24°C did not reject strongly alternatives with a low pulse rate (Table 2E). Females tested at 24°C were also less selective than females tested at 20°C in rejecting alternatives with a high pulse rate, in the range ofH. chrysoscelis (Table 2D). Females tested at 24°C did, however, strongly reject an alternative with both a pulse rate and pulse shape typical ofH. chrysoscelis (Fig. 6).
Call duration and call rate were also relevant properties; changes in these variables modified preferences based on differences in pulse rate, provided that the pulse rates of both alternatives were within the range of variation produced by conspecific males over the normal range of breeding temperatures (Figs. 4–6).
Females showed a weak preference for synthetic calls with a bimodal spectral structure typical of conspecific males (1.1 kHz [−6 dB]+2.2 kHz) to a synthetic call with a single spectral component of 2.2 kHz. In tests of single-component stimuli of 1.9 or 2.2 kHz against alternatives of lower and higher frequencies, female preferences indicated a pattern of relative frequency sensitivity (Fig. 7) that was similar to that of an audiogram based on evoked potentials in the midbrain over the same range of frequency.
About 50% of the females tested responded phonotactically to a recorded call ofH. chrysoscelis when they had no other choice (Table 3). Thus, heterospecific signals were not only audible, but also behaviorally effective in the context of courtship.
Pattern of female preferences with respect to pulse shape and pulse rate suggest that the potential for mismating with males ofH. chrysoscelis has been an important selective force in the evolution of acoustic pattern discrimination inH. versicolor.
Results of this study are compared with those of other anurans and acoustic insects. Temperature-dependent shifts in temporal pattern preference, similar but less pronounced than those reported here for both fine temporal and gross temporal properties, were found in some species but not in others.
The pulse rate of the male's call increases linearly over a wide range of temperature (9–34°C; Gayou 1984), but female selectivity for pulse rate differs within the range of 16–24°C and is biased toward low pulse rates (Table 2). Thus, it is unlikely that both the temporal patterning of the male's call and temporal pattern recognition by the female are controlled rigidly and linearly by the same neural circuitry.
We discuss neurophysiological studies of temporal pattern selectivity in acoustic insects and anurans. There are several neural correlates of behavioral selectivity in gray treefrogs, but no published data concerning a neural correlate of the asymmetry in the strength of pulse rate preferences in gray treefrogs.
pulses per second