Evolution of novel signal traits in the absence of female preferences in Neoconocephalus katydids (Orthoptera, Tettigoniidae)

Abstract

BACKGROUND SIGNIFICANCE: Communication signals that function to bring together the sexes are important for maintaining reproductive isolation in many taxa. Changes in male calls are often attributed to sexual selection, in which female preferences initiate signal divergence. Natural selection can also influence signal traits if calls attract predators or parasitoids, or if calling is energetically costly. Neutral evolution is often neglected in the context of acoustic communication.

Methodology/principal findings: We describe a signal trait that appears to have evolved in the absence of either sexual or natural selection. In the katydid genus Neoconocephalus, calls with a derived pattern in which pulses are grouped into pairs have evolved five times independently. We have previously shown that in three of these species, females require the double pulse pattern for call recognition, and hence the recognition system of the females is also in a derived state. Here we describe the remaining two species and find that although males produce the derived call pattern, females use the ancestral recognition mechanism in which no pulse pattern is required. Females respond equally well to the single and double pulse calls, indicating that the derived trait is selectively neutral in the context of mate recognition.

Conclusions/significance: These results suggest that 1) neutral changes in signal traits could be important in the diversification of communication systems, and 2) males rather than females may be responsible for initiating signal divergence.

Figure 1. Double pulse pattern in the calls of Neoconocephalus.

A. Oscillograms of calls of a single pulse species (N. robustus, top) and two species with double pulse pattern (N. retusus, N. maxillosus). The filled arrowheads indicate the sound produced during closing movements, open arrowheads the sound generated during the opening movements of the forewings . The small opening pulses play little if any role during communication and are included as part of the silent interval between pulses , . sp = single pulse; dp = double pulse. B Total evidence tree of Neoconocephalus based on AFLP, nuclear, and mitochondrial data . All nodes within Neoconocephalus have posterior probabilities of 0.98 or above. Names of species with double pulsed calls shown in bold; arrows indicate species tested here. [Outgroups: Belocephalus davisi Rhen and Hebard 1916 and Bucrates malivolans (Scudder 1878)].

Figure 2. The presence of alternating pulse periods in calls of N. retusus and N. maxillosus.

A, B. Mean (±95% CI) durations of alternating closing pulses and the following intervals making up pulse pairs in the calls of N. retusus (A, N = 10) and N. maxillosus (B, N = 11). The duration of the intervals includes the opening pulses (see Fig. 1A). Time bars are 5 ms. C. The ratio of the longer and shorter of the two alternating pulse periods of N. retusus (RET, N = 28), N. maxillosus (MAX, N = 13), and a species with single pulse calls (N. robustus, ROB, N = 13). D. The CV ratio (see methods) of the pulse periods in the calls of N. retusus (RET, N = 28), N. maxillosus (MAX, N = 13), and a species with single pulse calls (N. robustus, ROB, N = 13). Values close to 1 indicate that the two alternating pulse periods are from the same population, while larger values indicate that they are from different populations. The box and whisker plots in C and D denote median (bar), 25th, 75th (box), 5th, 95th (whiskers) percentile, and the mean (diamond).

Figure 3. Importance of the pulse structure for female call recognition.

A. Phonotaxis scores (mean ± 95% CI) in response to conspecific call models (open bars) and unmodulated sine waves (black bars) in N. retusus and N. maxillosus. B. Previously published data for sibling species N. robustus (single pulse species) and N. bivocatus (double pulse species) for comparison.

Figure 4. Importance of interval duration on female phonotaxis.

In N. retusus (A), interval durations were varied for three different pulse durations (1, 3.5, and 14 ms); in N. maxillosus (B) two different pulse durations (2.5 and 6 ms) were tested. Each point represents the mean phonotaxis scores (±95% CI) of 7–8 (N. retusus) or 5 (N. maxillosus) females.

Figure 5. Absence of female preference for the double pulse structure.

Top: Phonotaxis scores (mean ± 95% CI) of N. retusus females toward calls that vary from single pulses to extreme double pulses as measured by the ratio of period 2/period 1 (p2/p1, see inset). The experiment was run in two consecutive years with different females. N = 9 (year 1) and N = 10 (year 2). Bottom: histogram of the ratio of long to short pulse period (p2/p1) in a population of male N. retusus calls (n = 39).