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Animal choruses emerge from receiver psychology

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ABSTRACT

Synchrony and alternation in large animal choruses are often viewed as adaptations by which cooperating males increase their attractiveness to females or evade predators. Alternatively, these seemingly composed productions may simply emerge by default from the receiver psychology of mate choice. This second, emergent property hypothesis has been inferred from findings that females in various acoustic species ignore male calls that follow a neighbor’s by a brief interval, that males often adjust the timing of their call rhythm and reduce the incidence of ineffective, following calls, and from simulations modeling the collective outcome of male adjustments. However, the purported connection between male song timing and female preference has never been tested experimentally, and the emergent property hypothesis has remained speculative. Studying a distinctive katydid species genetically structured as isolated populations, we conducted a comparative phylogenetic analysis of the correlation between male call timing and female preference. We report that across 17 sampled populations male adjustments match the interval over which females prefer leading calls; moreover, this correlation holds after correction for phylogenetic signal. Our study is the first demonstration that male adjustments coevolved with female preferences and thereby confirms the critical link in the emergent property model of chorus evolution.

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Timing parameters in male chorusing and female preference.(A) Call delay histograms of representative males from 2 populations (Col de Chioula, Font Romeu; Fig. 4A). The numbers of calls produced during 50-ms bins beginning at the onset of a synthetic call stimulus broadcast at random intervals are shown. The post-stimulus delay of the earliest of the male’s 40 calls following inhibition is equivalent to m in Fig. 1. (B) Minimum post-stimulus call delay, m, for each of 8 males tested via playback in the 2 populations. A male’s m is determined as the average of his 3 shortest delays. The population’s m is the average of the individual male values. (C) Index of preference by females in the 2 populations for the leading of 2 synthetic call stimuli broadcast in close succession. For a given population, the maximum leader-follower call separation at which the index remained ≥50% of the highest index value observed across all call separations was designated as f; in all but one population this highest index value was significant (Ho: index = 0.0; 1-tailed sign test, α = 0.05; each female that preferred the leader in >50% of trials was labelled ‘+’ and labelled ‘−’ if < 50%; the sign test was performed on the labels of all females tested for responses to a given call separation). *Index of preference >0.0.
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f3: Timing parameters in male chorusing and female preference.(A) Call delay histograms of representative males from 2 populations (Col de Chioula, Font Romeu; Fig. 4A). The numbers of calls produced during 50-ms bins beginning at the onset of a synthetic call stimulus broadcast at random intervals are shown. The post-stimulus delay of the earliest of the male’s 40 calls following inhibition is equivalent to m in Fig. 1. (B) Minimum post-stimulus call delay, m, for each of 8 males tested via playback in the 2 populations. A male’s m is determined as the average of his 3 shortest delays. The population’s m is the average of the individual male values. (C) Index of preference by females in the 2 populations for the leading of 2 synthetic call stimuli broadcast in close succession. For a given population, the maximum leader-follower call separation at which the index remained ≥50% of the highest index value observed across all call separations was designated as f; in all but one population this highest index value was significant (Ho: index = 0.0; 1-tailed sign test, α = 0.05; each female that preferred the leader in >50% of trials was labelled ‘+’ and labelled ‘−’ if < 50%; the sign test was performed on the labels of all females tested for responses to a given call separation). *Index of preference >0.0.

Mentions: We reasoned that if male resetting adjustment evolved in response to female preference for leading calls, the timing of these 2 traits would be interconnected such that males seldom produce calls that most local females perceive as following ones and therefore ignore. As in other acoustic species using resetting mechanisms, male E. diurnus initiate few or no calls during a delay interval of minimum length m following the onset of a neighbor’s call or a synthetic song stimulus21 (Fig. 3A,B). Females show a pronounced preference for a leading over a following call if the latter begins during an interval f after the onset of the leading call (Fig. 3C). When m is ≥ f, males will avoid broadcasting ineffective following calls, and when m = f, males will maximize their call rate and improve their chance of broadcasting leading calls as well. We sampled 17 E. diurnus populations from southern and central France and northeastern Spain chosen to cover a broad geographic range, genetic variation as suggested by earlier phylogeographic studies22, and a diversity of male songs and chorusing patterns (Fig. 4A). In each population we determined m by testing male acoustic responses to the playback of song stimuli and f by testing female movement toward the leading of 2 song stimuli. We also developed a neighbor-joining (NJ) tree, based on microsatellite markers26, to serve as our ‘working phylogeny’ of E. diurnus populations.


Animal choruses emerge from receiver psychology
Timing parameters in male chorusing and female preference.(A) Call delay histograms of representative males from 2 populations (Col de Chioula, Font Romeu; Fig. 4A). The numbers of calls produced during 50-ms bins beginning at the onset of a synthetic call stimulus broadcast at random intervals are shown. The post-stimulus delay of the earliest of the male’s 40 calls following inhibition is equivalent to m in Fig. 1. (B) Minimum post-stimulus call delay, m, for each of 8 males tested via playback in the 2 populations. A male’s m is determined as the average of his 3 shortest delays. The population’s m is the average of the individual male values. (C) Index of preference by females in the 2 populations for the leading of 2 synthetic call stimuli broadcast in close succession. For a given population, the maximum leader-follower call separation at which the index remained ≥50% of the highest index value observed across all call separations was designated as f; in all but one population this highest index value was significant (Ho: index = 0.0; 1-tailed sign test, α = 0.05; each female that preferred the leader in >50% of trials was labelled ‘+’ and labelled ‘−’ if < 50%; the sign test was performed on the labels of all females tested for responses to a given call separation). *Index of preference >0.0.
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f3: Timing parameters in male chorusing and female preference.(A) Call delay histograms of representative males from 2 populations (Col de Chioula, Font Romeu; Fig. 4A). The numbers of calls produced during 50-ms bins beginning at the onset of a synthetic call stimulus broadcast at random intervals are shown. The post-stimulus delay of the earliest of the male’s 40 calls following inhibition is equivalent to m in Fig. 1. (B) Minimum post-stimulus call delay, m, for each of 8 males tested via playback in the 2 populations. A male’s m is determined as the average of his 3 shortest delays. The population’s m is the average of the individual male values. (C) Index of preference by females in the 2 populations for the leading of 2 synthetic call stimuli broadcast in close succession. For a given population, the maximum leader-follower call separation at which the index remained ≥50% of the highest index value observed across all call separations was designated as f; in all but one population this highest index value was significant (Ho: index = 0.0; 1-tailed sign test, α = 0.05; each female that preferred the leader in >50% of trials was labelled ‘+’ and labelled ‘−’ if < 50%; the sign test was performed on the labels of all females tested for responses to a given call separation). *Index of preference >0.0.
Mentions: We reasoned that if male resetting adjustment evolved in response to female preference for leading calls, the timing of these 2 traits would be interconnected such that males seldom produce calls that most local females perceive as following ones and therefore ignore. As in other acoustic species using resetting mechanisms, male E. diurnus initiate few or no calls during a delay interval of minimum length m following the onset of a neighbor’s call or a synthetic song stimulus21 (Fig. 3A,B). Females show a pronounced preference for a leading over a following call if the latter begins during an interval f after the onset of the leading call (Fig. 3C). When m is ≥ f, males will avoid broadcasting ineffective following calls, and when m = f, males will maximize their call rate and improve their chance of broadcasting leading calls as well. We sampled 17 E. diurnus populations from southern and central France and northeastern Spain chosen to cover a broad geographic range, genetic variation as suggested by earlier phylogeographic studies22, and a diversity of male songs and chorusing patterns (Fig. 4A). In each population we determined m by testing male acoustic responses to the playback of song stimuli and f by testing female movement toward the leading of 2 song stimuli. We also developed a neighbor-joining (NJ) tree, based on microsatellite markers26, to serve as our ‘working phylogeny’ of E. diurnus populations.

View Article: PubMed Central - PubMed

ABSTRACT

Synchrony and alternation in large animal choruses are often viewed as adaptations by which cooperating males increase their attractiveness to females or evade predators. Alternatively, these seemingly composed productions may simply emerge by default from the receiver psychology of mate choice. This second, emergent property hypothesis has been inferred from findings that females in various acoustic species ignore male calls that follow a neighbor&rsquo;s by a brief interval, that males often adjust the timing of their call rhythm and reduce the incidence of ineffective, following calls, and from simulations modeling the collective outcome of male adjustments. However, the purported connection between male song timing and female preference has never been tested experimentally, and the emergent property hypothesis has remained speculative. Studying a distinctive katydid species genetically structured as isolated populations, we conducted a comparative phylogenetic analysis of the correlation between male call timing and female preference. We report that across 17 sampled populations male adjustments match the interval over which females prefer leading calls; moreover, this correlation holds after correction for phylogenetic signal. Our study is the first demonstration that male adjustments coevolved with female preferences and thereby confirms the critical link in the emergent property model of chorus evolution.

No MeSH data available.


Related in: MedlinePlus