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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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Correlation of male and female timing parameters across populations.(A) Map of southern France and northeastern Spain showing locations of the 17 E. diurnus populations sampled between 2012–2015 (see ref. 30); map was generated with ArcGIS version 10.0 for desktop, ESRI (http://www.esri.com/software/arcgis/arcgis-for-desktop). (B) Ordinary least-squares linear regression of m (minimum post-stimulus call delay in males; Fig. 3B) vs. f (maximum leader-follower call separation for which females prefer the leading call; Fig. 3C) for the 17 sampled populations (m = 31 + 0.79 f; t = 6.56, p < 0.001). (C) Ordinary least-squares linear regression of m vs. f as in Fig. 4b but restricted to those 10 populations where the mean call syllable number in males was ≤2.1 (m = 207 + 0.37 f). Stepwise linear regression (α to enter and α to remove = 0.15) of m on both f and mean syllable number yielded the above model that only included f.
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f4: Correlation of male and female timing parameters across populations.(A) Map of southern France and northeastern Spain showing locations of the 17 E. diurnus populations sampled between 2012–2015 (see ref. 30); map was generated with ArcGIS version 10.0 for desktop, ESRI (http://www.esri.com/software/arcgis/arcgis-for-desktop). (B) Ordinary least-squares linear regression of m (minimum post-stimulus call delay in males; Fig. 3B) vs. f (maximum leader-follower call separation for which females prefer the leading call; Fig. 3C) for the 17 sampled populations (m = 31 + 0.79 f; t = 6.56, p < 0.001). (C) Ordinary least-squares linear regression of m vs. f as in Fig. 4b but restricted to those 10 populations where the mean call syllable number in males was ≤2.1 (m = 207 + 0.37 f). Stepwise linear regression (α to enter and α to remove = 0.15) of m on both f and mean syllable number yielded the above model that only included f.

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
Correlation of male and female timing parameters across populations.(A) Map of southern France and northeastern Spain showing locations of the 17 E. diurnus populations sampled between 2012–2015 (see ref. 30); map was generated with ArcGIS version 10.0 for desktop, ESRI (http://www.esri.com/software/arcgis/arcgis-for-desktop). (B) Ordinary least-squares linear regression of m (minimum post-stimulus call delay in males; Fig. 3B) vs. f (maximum leader-follower call separation for which females prefer the leading call; Fig. 3C) for the 17 sampled populations (m = 31 + 0.79 f; t = 6.56, p < 0.001). (C) Ordinary least-squares linear regression of m vs. f as in Fig. 4b but restricted to those 10 populations where the mean call syllable number in males was ≤2.1 (m = 207 + 0.37 f). Stepwise linear regression (α to enter and α to remove = 0.15) of m on both f and mean syllable number yielded the above model that only included f.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC5037466&req=5

f4: Correlation of male and female timing parameters across populations.(A) Map of southern France and northeastern Spain showing locations of the 17 E. diurnus populations sampled between 2012–2015 (see ref. 30); map was generated with ArcGIS version 10.0 for desktop, ESRI (http://www.esri.com/software/arcgis/arcgis-for-desktop). (B) Ordinary least-squares linear regression of m (minimum post-stimulus call delay in males; Fig. 3B) vs. f (maximum leader-follower call separation for which females prefer the leading call; Fig. 3C) for the 17 sampled populations (m = 31 + 0.79 f; t = 6.56, p < 0.001). (C) Ordinary least-squares linear regression of m vs. f as in Fig. 4b but restricted to those 10 populations where the mean call syllable number in males was ≤2.1 (m = 207 + 0.37 f). Stepwise linear regression (α to enter and α to remove = 0.15) of m on both f and mean syllable number yielded the above model that only included f.
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