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Evolution of Bird Communication Signals: Transference Between Signals Mediated bioRxiv preprint doi: https://doi.org/10.1101/142463; this version posted May 26, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 1 Evolution of bird communication signals: transference between signals mediated 2 by sensory drive 3 4 Oscar Laverde-R. 5 6 Laboratorio de Biología Evolutiva de Vertebrados, Departamento de Ciencias 7 Biológicas, Universidad de los Andes. Bogotá, D. C. 8 [email protected] 9 Current address: Unidad de Ecología y Sistemática (UNESIS). Facultad de Ciencias, 10 Departamento de Biología, Pontificia Universidad Javeriana. Bogotá, D. C. 11 12 Michael J. Ryan 13 Smithsonian Tropical Research Institute, Balboa, Panama 14 Department of Integrative Biology, University of Texas at Austin, Austin. 15 [email protected] 16 17 Carlos Daniel Cadena 18 Laboratorio de Biología Evolutiva de Vertebrados, Departamento de Ciencias 19 Biológicas, Universidad de los Andes. Bogotá, D. C. 20 [email protected] 21 22 23 24 25 1 bioRxiv preprint doi: https://doi.org/10.1101/142463; this version posted May 26, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 26 Animals communicate using signals perceived via multiple sensory modalities 27 but usually invest more heavily in one of type of signal. This pattern, observed by 28 Darwin1 and many researchers since, led to development of the transfer 29 hypothesis (see also transferal effect2 and tradeoff hypothesis3,4), which predicts a 30 negative relationship between investment in different signaling modalities 31 dictated by the relative costs and benefits of each. One factor that influences 32 costs and benefits, and is central to the sensory drive hypothesis5 posed to 33 account for signal evolution, is the suitability of the environment for different 34 types of signals. Movement into a dark habitat, for example, should favor 35 investment in acoustic over visual signals. We use phylogenetic comparative 36 methods to analyze the joint effect of transfer and sensory drive on plumage and 37 song variation in 52 species of a large radiation of passerine birds, the New 38 World warblers (Parulidae), and to estimate temporal patterns in the 39 accumulation of differences in visual and vocal signals and habitat along the 40 evolutionary history of this lineage. We found evidence for the predicted 41 negative correlations between a variety of song and plumage traits that vary with 42 habitat type. Plumage contrast to background and chromatic diversity were both 43 negatively related to syllable variety when vegetation structure was a covariate: 44 birds with a greater variety of song syllables and less colorful plumages live in 45 closed or darker habitats. Also as predicted, achromatic or brightness diversity 46 was related to vegetation structure. In addition, disparity-through-time analyses 47 showed that when one set of traits (i.e. songs or colors) diversified at a relatively 48 high rate the other did not, as predicted by the transfer hypothesis. Our results 49 show that sensory drive influences the transfer of investment between traits in 2 bioRxiv preprint doi: https://doi.org/10.1101/142463; this version posted May 26, 2017. 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 4.0 International license. 50 different sensory modalities. This interaction between mechanisms shaping 51 signals may be a major determinant in the evolution of animal communication. 52 53 Ever since Darwin1, naturalists have noted a negative relationship between bright 54 colors and the elaboration of songs involved in animal communication. For example, 55 “... in territorial passerine birds, there tends to be an inverse relation between the 56 development of auditory distinctiveness (song of species with cryptic behavior and 57 coloration, e.g., grasshopper warbler, chiffchaff) and visual distinctiveness (pattern of 58 species with conspicuous behavior, e.g., stonechat, pied flycatcher)...” 6. Such 59 observations led to the postulation of the transferal effect2,7 or tradeoff hypothesis3 60 (later named transfer hypothesis), which states that the complexity of signals in 61 different modalities should be negatively related. Animals are expected to invest 62 primarily in one type of signal (i.e., vocal, chemical, or visual8) owing to various 63 factors, including internal limitations in energy expenditure (classical life-history 64 tradeoffs9,10), predators11, parasites12, physical conditions of the habitat2, and the 65 conflicting forces of sexual and natural selection12. Despite the generality and 66 popularity of this hypothesis, there have been few13–15 attempts to test it with a robust, 67 phylogenetically informed data set that includes variation in multiple signal 68 modalities and covariation with the signaling habitat that influences the salience of 69 these signals. 70 71 Here, we test for a negative relationship between elaboration in song and plumage 72 coloration in the context of the signaling habitat, thus linking the transfer hypothesis 73 with another leading hypothesis posed to account for signal evolution, namely sensory 74 drive5. The sensory drive hypothesis posits that variation in habitat features leads to 3 bioRxiv preprint doi: https://doi.org/10.1101/142463; this version posted May 26, 2017. 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 4.0 International license. 75 variation in selection pressures by affecting the ease with which different traits are 76 perceived. For example, because the use of visual signals for communication in dark 77 habitats (e.g. forest understory, turbid waters) is expected to be ineffective5,16, acoustic 78 or olfactory signals should be more prevalent as targets of sexual selection in such 79 environments. In turn, in open areas or clear waters one expects visual signals to be 80 more elaborate than vocal or chemical signals. Although several studies have 81 supported the sensory drive hypothesis, they have largely focused on a single 82 communication channel (i.e., visual15,17–20, olfactory16, or acoustic signals21–23) and 83 have not considered interactions among channels as those implied by the transfer 84 hypothesis. Similarly, the few existing examinations of the transfer hypothesis13–15,24 85 have not considered the influence of habitat on signal salience. 86 87 Using data on plumage, song, and habitat, we examined correlations between visual 88 and acoustic signals mediated by the environment across a large radiation of passerine 89 birds. The New World warblers (Parulidae) are a group of small, often colorful, 90 primarily insectivorous oscines with diverse songs and a broad diversity of habitat 91 affinities and life histories25. The tuning of the visual system of warblers varies with 92 habitat and this should generate differential, habitat-specific selection on visual 93 signals. Expression of opsins varies with the light environment occupied by different 94 species26; specifically, short-wavelength sensitive type 2 opsins (SWS2) are shifted to 95 longer wavelengths in species living in closed forest environments27 where most of 96 the short wavelengths are filtered by vegetation28. In addition, female expression of 97 these same opsins varies with plumage dichromatism, suggesting a role for sensory 98 drive26. 99 4 bioRxiv preprint doi: https://doi.org/10.1101/142463; this version posted May 26, 2017. 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 4.0 International license. 100 In analyses that did not account for the habitat preferences of species, we found no 101 support for the prediction of the transfer hypothesis that elaboration in plumage 102 coloration (chromatic diversity of plumage and chromatic contrast to the back) and 103 song traits (vocal deviation -a measure of vocal performance-, syllable variety and 104 song length) should be negatively related (Table 1, 2). However, when we included 105 vegetation structure as a covariate (i.e., open vs. closed habitats), significant negative 106 relationships between variables emerged, suggesting that apparent transfers in 107 investment between signals in different communication channels are mediated by 108 habitat. Specifically, chromatic contrast to background (β= -6.79, t= -2.69, p=0.01) 109 and chromatic diversity of plumage were negatively related to song syllable variety 110 (β= -1.51, t= -3.31, p=0.001, Table 1), such that species with less colorful plumage 111 exhibit songs with a greater variety of syllables and live in closed habitats (β = 1.96, 112 t= 2.76, p=0.008). Additionally, achromatic diversity of plumage was significantly 113 related to vegetation structure (β= 3.22, t= -2.16, p=0.03, Table 2) and to vocal 114 deviation (β= 1.6290, t=2.0145, p=0.05, Fig. 1); this indicates that birds with darker 115 backs live in darker habitats and communicate using songs demanding greater 116 performance. A plausible interpretation of these results is that in forest species natural 117 selection to reduce conspicuousness due to predation has resulted in a match between 118 plumage coloration and background color; this has presumably triggered an 119 investment transfer between visual and vocal signals, resulting in more elaborate 120 songs favored by sexual selection.
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