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A Global Analysis of Song Frequency in Passerines Provides No Support for the Acoustic

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A Global Analysis of Song Frequency in Passerines Provides No Support for the Acoustic bioRxiv preprint doi: https://doi.org/10.1101/2020.06.30.179812; this version posted June 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 A global analysis of song frequency in passerines provides no support for the acoustic 2 adaptation hypothesis but suggests a role for sexual selection 3 Running title: Evolutionary ecology of song frequency 4 5 Peter Mikula1,2, Mihai Valcu3, Henrik Brumm4, Martin Bulla3,5, Wolfgang Forstmeier3, 6 Tereza Petrusková6, Bart Kempenaers3*, Tomáš Albrecht1,2* 7 8 1Department of Zoology, Faculty of Science, Charles University, Viničná 7, 128 44, Praha 2, 9 Czech Republic 10 2Institute of Vertebrate Biology, Czech Academy of Sciences, Květná 8, 603 65, Brno, Czech 11 Republic 12 3Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for 13 Ornithology, Eberhard-Gwinner-Str. 7, 82319 Seewiesen, Germany 14 4Communication and Social Behaviour Group, Max Planck Institute for Ornithology, 15 Eberhard-Gwinner-Str. 11, 82319 Seewiesen, Germany 16 5Department of Ecology, Faculty of Environmental Sciences, Czech University of Life 17 Sciences, 16521 Prague, Czech Republic 18 6Department of Ecology, Faculty of Science, Charles University, Viničná 7, 128 43, Praha 2, 19 Czech Republic 20 *Authors for correspondence: E-mail: [email protected] and [email protected], 21 phone no.: +498 157 932 232 and +420 608 237 158 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.30.179812; this version posted June 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 22 Statement of authorship: TA and PM conceived and designed the study with input from all 23 authors. TA and BK coordinated the study. PM collected the song data. MV performed the 24 statistical analyses with input from WF. MB made the figures with help from MV and PM. TP 25 and HB provided bioacoustic expertise. PM drafted the first version of the manuscript. TA, 26 BK and PM revised and finalized the manuscript with input from all authors. 27 Data availability statement: The data used in this study were collected from publicly 28 available databases. All data and computer code used to generate the results, as well as 29 supplementary figures and tables will be freely available at https://osf.io/fa9ky/. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.30.179812; this version posted June 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 30 Abstract 31 Many animals use acoustic signals for communication, implying that the properties of these 32 signals can be under strong selection. The acoustic adaptation hypothesis predicts that species 33 living in dense habitats emit lower-frequency sounds than those in open areas, because low- 34 frequency sounds generally propagate further in denser vegetation. Signal frequency may also 35 be under sexual selection, because it correlates with body size and lower-frequency sounds are 36 perceived as more intimidating. Here, we evaluate these hypotheses by analysing variation in 37 peak song frequency across 5,085 passerine species (Passeriformes). A phylogenetically- 38 informed analysis revealed that song frequency decreases with increasing body mass and with 39 male-biased sexual size dimorphism. However, we found no support for the predicted 40 relationship between frequency and habitat. Our results suggest that the global variation in 41 passerine song frequency is mostly driven by natural and sexual selection causing 42 evolutionary shifts in body size rather than by habitat-related selection on sound propagation. 43 44 Keywords: acoustic adaptation hypothesis, allometry, animal communication, bird song, 45 macroecology, morphological constraints, sexual selection 46 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.30.179812; this version posted June 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 47 INTRODUCTION 48 Acoustic signalling is widespread among animals (Bradbury & Vehrencamp 1998; Gerhardt 49 & Huber 2002; Catchpole & Slater 2008). Successful transmission and reception of acoustic 50 signals between conspecifics are essential in diverse contexts, including predation avoidance 51 (alerting others to a threat), territory defence, mate attraction, and synchronization of breeding 52 activities (Bradbury & Vehrencamp 1998; Catchpole & Slater 2008). One of the fundamental 53 characteristics of acoustic signals is the frequency of the sound, because it strongly affects 54 signal propagation through the environment (Morton 1975; Wiley & Richards 1982; Padgham 55 2004). Low frequency sounds are generally less attenuated during transmission than high 56 frequency sounds (Wiley & Richards 1982; Padgham 2004). Nevertheless, the frequency of 57 acoustic signals is tremendously diverse across the animal kingdom (Gerhardt 1994; Fitch 58 2006; Gillooly & Ophir 2010; Pijanowski et al. 2011) and several hypotheses have been 59 proposed to explain this diversity. Here, we focus on the three most compelling ones: (1) the 60 acoustic adaptation hypothesis, (2) the morphological constraint hypothesis, and (3) the sexual 61 selection hypothesis. 62 Since the 1970s, it has been postulated that the frequency of acoustic signals could reflect an 63 adaptation to maximize the effectiveness of sound transmission in specific habitats (Morton 64 1975). This is known as the acoustic adaptation hypothesis (Boncoraglio & Saino 2007; Ey & 65 Fischer 2009). Sounds transmitted through the natural environment are subject to degradation, 66 for example due to environmental absorption, reverberation and scattering. The degree of this 67 degradation depends both on the sound structure and on the physical characteristics of the 68 environment (Wiley & Richards 1982; Brumm & Naguib 2009). Specifically, because of 69 frequency-dependent attenuation, low-frequency sounds transmit generally further than high- 70 frequency sounds. However, the slope of the frequency dependence is steeper in dense, 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.30.179812; this version posted June 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 71 forested habitats because of the high degree of sound absorption and scattering from foliage. 72 Hence, high-frequency signals are attenuated more strongly in closed than in open habitats 73 (Morton 1975; Marten & Marler 1977; Wiley & Richards 1978). Therefore, species living in 74 forested habitats are expected to produce vocalizations of lower frequencies than those living 75 in open habitats (Ey & Fischer 2009). Despite this strong theoretical underpinning, empirical 76 evidence for the acoustic adaptation hypothesis is equivocal (Morton 1975; Wiley 1991; 77 Buskirk 1997; Bertelli & Tubaro 2002; Blumstein & Turner 2005; Ey & Fischer 2009). For 78 instance, a meta-analysis by Boncoraglio & Saino (2007) showed that song frequency in birds 79 tends to be lower in closed compared with open habitats, but the effect size was small. A 80 review by Ey & Fischer (2009) concluded that habitat-related adjustments of frequency 81 parameters of acoustic signals of birds, anurans and mammals are not as widespread as 82 previously thought. 83 The morphological constraint hypothesis simply posits that body size sets a limit on the 84 frequency of the sound an animal can produce. Morphological constraints generally seem to 85 play a pervasive role in the evolution of animal acoustic communication (Ryan & Brenowitz 86 1985; Bradbury & Vehrencamp 1998; Fitch & Hauser 2002). A negative relationship between 87 body size and frequency of acoustic signals, i.e. larger species tend to produce lower 88 frequency sounds than smaller species, seems to be a general rule in animal bioacoustics and 89 has been documented across various groups, including insects, fishes, amphibians, reptiles, 90 birds, and mammals (Wallschläger 1980; McClatchie et al. 1996; Fitch & Hauser 2002; 91 Gillooly & Ophir 2010; Pearse et al. 2018). In birds, it has been suggested that the frequency 92 of vocalizations negatively scales with body size, simply because body size influences the 93 morphology and functional aspects of the vocal apparatus, such as the size of vibratory 94 structures (Bertelli & Tubaro 2002; Suthers & Zollinger 2008; Seneviratne et al. 2012; 95 Gonzalez-Voyer et al. 2013; Tietze et al. 2015). However, body size alone does not explain 5 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.30.179812; this version posted June 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint
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