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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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Comparative phylogenetic analysis of male and female timing parameters.(A) Unrooted neighbor-joining (NJ) tree of 17 E. diurnus populations from southern France and northeastern Spain (Fig. 4A) generated from microsatellite loci. Scale at bottom left indicates 0.05 nucleotide substitutions per site; values over branches represent posterior probabilities. Red and blue bars to the right of each population indicate the values of m (minimum post-stimulus call delay in males) and f (maximum leader-follower call separation for which females prefer the leader); see Figs 3B,C and 4B. syl is mean syllable number in the male call. (B) Correlation between m and f among the 17 populations corrected by phylogenetically independent contrasts (PIC). Black line is ordinary least-squares linear regression through the origin for the 16 standardized, positivized contrasts (ρ = 0.76, p < 0.001; df reduced by 2 to account for polytomy); red line is reduced major axis regression. (C) Unrooted NJ tree of 7 genetically distinct clusters determined via Bayesian clustering (Fig. 6). Each cluster comprises 1–4 of the 17 populations. (D) Correlation between mean m and f among the 7 clusters from Fig. 5C corrected by PIC (ρ = 0.94, p < 0.01; n = 6 contrasts).
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f5: Comparative phylogenetic analysis of male and female timing parameters.(A) Unrooted neighbor-joining (NJ) tree of 17 E. diurnus populations from southern France and northeastern Spain (Fig. 4A) generated from microsatellite loci. Scale at bottom left indicates 0.05 nucleotide substitutions per site; values over branches represent posterior probabilities. Red and blue bars to the right of each population indicate the values of m (minimum post-stimulus call delay in males) and f (maximum leader-follower call separation for which females prefer the leader); see Figs 3B,C and 4B. syl is mean syllable number in the male call. (B) Correlation between m and f among the 17 populations corrected by phylogenetically independent contrasts (PIC). Black line is ordinary least-squares linear regression through the origin for the 16 standardized, positivized contrasts (ρ = 0.76, p < 0.001; df reduced by 2 to account for polytomy); red line is reduced major axis regression. (C) Unrooted NJ tree of 7 genetically distinct clusters determined via Bayesian clustering (Fig. 6). Each cluster comprises 1–4 of the 17 populations. (D) Correlation between mean m and f among the 7 clusters from Fig. 5C corrected by PIC (ρ = 0.94, p < 0.01; n = 6 contrasts).

Mentions: In further analyses we dealt with several factors that potentially generated the matching of male and female timing parameters as an artifact. First, we applied the method of independent contrasts (PIC) to our NJ tree of populations to remove any phylogenetic signal from the m-f correlation27. Under most circumstances inter-population gene flow would invalidate the use of PIC to treat intra-specific relationships2829, but the negligible migration in E. diurnus, which are flightless, and the distinctive population genetic structure fully justify its application here. Our NJ tree (Fig. 5A) clearly reveals a branching topology that is consistent, in its details, with another tree based on COI30, indicating that our working phylogeny is most probably an accurate depiction of the true one. To be conservative, we also analyzed our microsatellite data with a Bayesian clustering protocol to identify genetically distinct population clusters and assign individuals to these entities (Fig. 6). We then created a NJ tree for the 7 strongly differentiated clusters identified (Fig. 5C) and again applied the PIC correction. We found that the m-f correlation remained highly significant following PIC correction whether applied to the tree of all 17 populations sampled or to the revised tree of 7 genetically distinct clusters (Fig. 5B,D). Thus, the observed matching of male and female timing parameters is not a phylogenetic artifact of our sampled populations.


Animal choruses emerge from receiver psychology
Comparative phylogenetic analysis of male and female timing parameters.(A) Unrooted neighbor-joining (NJ) tree of 17 E. diurnus populations from southern France and northeastern Spain (Fig. 4A) generated from microsatellite loci. Scale at bottom left indicates 0.05 nucleotide substitutions per site; values over branches represent posterior probabilities. Red and blue bars to the right of each population indicate the values of m (minimum post-stimulus call delay in males) and f (maximum leader-follower call separation for which females prefer the leader); see Figs 3B,C and 4B. syl is mean syllable number in the male call. (B) Correlation between m and f among the 17 populations corrected by phylogenetically independent contrasts (PIC). Black line is ordinary least-squares linear regression through the origin for the 16 standardized, positivized contrasts (ρ = 0.76, p < 0.001; df reduced by 2 to account for polytomy); red line is reduced major axis regression. (C) Unrooted NJ tree of 7 genetically distinct clusters determined via Bayesian clustering (Fig. 6). Each cluster comprises 1–4 of the 17 populations. (D) Correlation between mean m and f among the 7 clusters from Fig. 5C corrected by PIC (ρ = 0.94, p < 0.01; n = 6 contrasts).
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f5: Comparative phylogenetic analysis of male and female timing parameters.(A) Unrooted neighbor-joining (NJ) tree of 17 E. diurnus populations from southern France and northeastern Spain (Fig. 4A) generated from microsatellite loci. Scale at bottom left indicates 0.05 nucleotide substitutions per site; values over branches represent posterior probabilities. Red and blue bars to the right of each population indicate the values of m (minimum post-stimulus call delay in males) and f (maximum leader-follower call separation for which females prefer the leader); see Figs 3B,C and 4B. syl is mean syllable number in the male call. (B) Correlation between m and f among the 17 populations corrected by phylogenetically independent contrasts (PIC). Black line is ordinary least-squares linear regression through the origin for the 16 standardized, positivized contrasts (ρ = 0.76, p < 0.001; df reduced by 2 to account for polytomy); red line is reduced major axis regression. (C) Unrooted NJ tree of 7 genetically distinct clusters determined via Bayesian clustering (Fig. 6). Each cluster comprises 1–4 of the 17 populations. (D) Correlation between mean m and f among the 7 clusters from Fig. 5C corrected by PIC (ρ = 0.94, p < 0.01; n = 6 contrasts).
Mentions: In further analyses we dealt with several factors that potentially generated the matching of male and female timing parameters as an artifact. First, we applied the method of independent contrasts (PIC) to our NJ tree of populations to remove any phylogenetic signal from the m-f correlation27. Under most circumstances inter-population gene flow would invalidate the use of PIC to treat intra-specific relationships2829, but the negligible migration in E. diurnus, which are flightless, and the distinctive population genetic structure fully justify its application here. Our NJ tree (Fig. 5A) clearly reveals a branching topology that is consistent, in its details, with another tree based on COI30, indicating that our working phylogeny is most probably an accurate depiction of the true one. To be conservative, we also analyzed our microsatellite data with a Bayesian clustering protocol to identify genetically distinct population clusters and assign individuals to these entities (Fig. 6). We then created a NJ tree for the 7 strongly differentiated clusters identified (Fig. 5C) and again applied the PIC correction. We found that the m-f correlation remained highly significant following PIC correction whether applied to the tree of all 17 populations sampled or to the revised tree of 7 genetically distinct clusters (Fig. 5B,D). Thus, the observed matching of male and female timing parameters is not a phylogenetic artifact of our sampled 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