Abstract

Sexual signals are archetypes of contingent evolution: hyper-diverse across species, often evolving fast and in unpredictable directions. It is unclear to which extent their evolutionary unpredictability weakens deterministic evolution, or takes place bounded by deterministic patterns of trait evolution. We compared the evolution of sound frequency in sexual signals (advertisement songs) and non-sexual social signals (calls) across > 500 genera of the crown songbird families. Contrary to the acoustic adaptation hypothesis, we found no evidence that forest species used lower sound frequencies in songs or calls. Consistent with contingent evolution in song, we found lower phylogenetic signal for the sound frequency of songs than calls, which suggests faster and less predictable evolution, and found unpredictable direction of evolution in lineages with longer songs, which presumably experience stronger sexual selection on song. Nonetheless, the most important deterministic pattern of sound frequency evolution—its negative association with body size—was stronger in songs than calls. This can be explained by songs being longer-range signals than most calls, and thus using sound frequencies that animals of a given size produce best at high amplitude. Results indicate that sexual selection can increase aspects of evolutionary contingency while strengthening, rather than weakening, deterministic patterns of evolution.

Highlights

  • Despite sexual signals being archetypes of contingent evolution, they are subject to deterministic selective ­pressures[12]

  • We found that absolute values of residual frequency were not related to song duration (PGLS: βst = 0.01, P = 0.37, N = 591 spp., model λ = 0.96), indicating that song duration does not predict the extent of deviations from the frequencies predicted by body size

  • Since sound frequency of songs and calls is distributed over the same frequency range across species (Fig. 2), the lower phylogenetic signal of sound frequency in songs implies that, on average, it evolved at a faster rate than in calls

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Summary

Introduction

Despite sexual signals being archetypes of contingent evolution, they are subject to deterministic selective ­pressures[12]. It is unclear to which extent the contingency associated with sexual selection weakens deterministic evolution (i.e., weakening cross-species associations between properties of sexual signals and their morphological or ecological predictors), as opposed to contingent effects taking place bounded by deterministic patterns of trait ­evolution[12]. Here we compared deterministic patterns of sound frequency evolution between bird songs, which are an important type of acoustic sexual signal, and, as a control, contact calls, which are acoustic signals that include more general, non-sexually-selected social functions. Since sexually-selected signals typically evolve in a highly contingent manner, with phenotypic changes in unpredictable or opposed d­ irections[6], we expected that the sound frequency of songs should be more evolutionary labile and show weaker phylogenetic s­ ignal[32,33] than that of calls. Regarding deterministic evolution, and since body size and habitat type are the two best understood predictors of sound frequency in acoustic s­ ignals[16,17,19], we evaluated the strength of deterministic evolutionary patterns by the strength of the cross-species association between sound frequency and either body size or habitat type

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