Section: Evolutionary Biology
Topic:
Evolution,
Genetics/Genomics,
Population biology
Distribution of iridescent colours in hummingbird communities results from the interplay between selection for camouflage and communication
Corresponding author(s): Gruson, Hugo (hugo.gruson@normalesup.org)
10.24072/pcjournal.7 - Peer Community Journal, Volume 1 (2021), article no. e64.
Get full text PDF Peer reviewed and recommended by PCIIdentification errors between closely related, co-occurring, species may lead to misdirected social interactions such as costly interbreeding or misdirected aggression. This selects for divergence in traits involved in species identification among co-occurring species, resulting from character displacement. On the other hand, predation may select for crypsis, potentially leading co-occurring species that share the same environment and predators to have a similar appearance. However, few studies have explored how these antagonistic processes influence colour at the community level. Here, we assess colour clustering and overdispersion in 189 hummingbird communities, tallying 112 species, across Ecuador and suggest possible evolutionary mechanisms at stake by controlling for species phylogenetic relatedness. In hummingbirds, most colours are iridescent structural colours, defined as colours that change with the illumination or observation angle. Because small variations in the underlying structures can have dramatic effects on the resulting colours and because iridescent structures can produce virtually any hue and brightness, we expect iridescent colours to respond finely to selective pressures. Moreover, we predict that hue angular dependence a specific aspect of iridescent colours may be used as an additional channel for species recognition. In our hummingbird assemblages in Ecuador, we find support for colour overdispersion in ventral and facial patches at the community level even after controlling for the phylogeny, especially on iridescence-related traits, suggesting character displacement among co-occurring species. We also find colour clustering at the community level on dorsal patches, suspected to be involved in camouflage, suggesting that the same cryptic colours are selected among co-occurring species.
Type: Research article
Gruson, Hugo 1; Elias, Marianne 2; Parra, Juan L. 3; Andraud, Christine 4; Berthier, Serge 5; Doutrelant, Claire 1; Gomez, Doris 1, 5
@article{10_24072_pcjournal_7, author = {Gruson, Hugo and Elias, Marianne and Parra, Juan L. and Andraud, Christine and Berthier, Serge and Doutrelant, Claire and Gomez, Doris}, title = {Distribution of iridescent colours in hummingbird communities results from the interplay between selection for camouflage and communication}, journal = {Peer Community Journal}, eid = {e64}, publisher = {Peer Community In}, volume = {1}, year = {2021}, doi = {10.24072/pcjournal.7}, url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.7/} }
TY - JOUR AU - Gruson, Hugo AU - Elias, Marianne AU - Parra, Juan L. AU - Andraud, Christine AU - Berthier, Serge AU - Doutrelant, Claire AU - Gomez, Doris TI - Distribution of iridescent colours in hummingbird communities results from the interplay between selection for camouflage and communication JO - Peer Community Journal PY - 2021 VL - 1 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.7/ DO - 10.24072/pcjournal.7 ID - 10_24072_pcjournal_7 ER -
%0 Journal Article %A Gruson, Hugo %A Elias, Marianne %A Parra, Juan L. %A Andraud, Christine %A Berthier, Serge %A Doutrelant, Claire %A Gomez, Doris %T Distribution of iridescent colours in hummingbird communities results from the interplay between selection for camouflage and communication %J Peer Community Journal %D 2021 %V 1 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.7/ %R 10.24072/pcjournal.7 %F 10_24072_pcjournal_7
Gruson, Hugo; Elias, Marianne; Parra, Juan L.; Andraud, Christine; Berthier, Serge; Doutrelant, Claire; Gomez, Doris. Distribution of iridescent colours in hummingbird communities results from the interplay between selection for camouflage and communication. Peer Community Journal, Volume 1 (2021), article no. e64. doi : 10.24072/pcjournal.7. https://peercommunityjournal.org/articles/10.24072/pcjournal.7/
PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100086
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] Resolution of a paradox: Hummingbird flight at high elevation does not come without a cost, Proceedings of the National Academy of Sciences, Volume 101 (2004) no. 51, pp. 17731-17736 | DOI
[2] Of Hummingbirds and Helicopters: Hovering Costs, Competitive Ability, and Foraging Strategies, The American Naturalist, Volume 163 (2004) no. 1, pp. 16-25 | DOI
[3] Selection on male sex pheromone composition contributes to butterfly reproductive isolation, Proceedings of the Royal Society B: Biological Sciences, Volume 282 (2015) no. 1804 | DOI
[4] Conformal predictions for information fusion, Annals of Mathematics and Artificial Intelligence, Volume 74 (2015) no. 1-2, pp. 45-65 | DOI
[5] Using functional traits and phylogenetic trees to examine the assembly of tropical tree communities, Journal of Ecology, Volume 100 (2012) no. 3, pp. 690-701 | DOI
[6] Decoupling phylogenetic and functional diversity to reveal hidden signals in community assembly, Methods in Ecology and Evolution, Volume 8 (2017) no. 10, pp. 1200-1211 | DOI
[7] Sexual Selection and the Mismeasure of Color, The American Naturalist, Volume 144 (1994) no. 5, pp. 848-860 | DOI
[8] Principles of animal communication. 2. ed, Sinauer Associates, Sunderland, Mass, (2011), 697 pages
[9] Character Displacement, Systematic Zoology, Volume 5 (1956) no. 2, pp. 49-64 | DOI
[10] Speciation by reinforcement, Trends in Ecology & Evolution, Volume 2 (1987) no. 1, pp. 8-13 | DOI
[11] The behavior and diet of the Shining Sunbeam (Aglaeactis cupripennis): A territorial high-elevation hummingbird, The Wilson Journal of Ornithology, Volume 131 (2019) no. 1, pp. 24-34 | DOI
[12] Four spectral classes of cone in the retinas of birds, Journal of Comparative Physiology A, Volume 159 (1986) no. 4, pp. 473-479 | DOI
[13] Wing, tail, and vocal contributions to the complex acoustic signals of courting Calliope hummingbirds, Current Zoology, Volume 57 (2011) no. 2, pp. 187-196 | DOI
[14] Aeroelastic Flutter Produces Hummingbird Feather Songs, Science, Volume 333 (2011) no. 6048, pp. 1430-1433 | DOI
[15] The Anna's hummingbird chirps with its tail: a new mechanism of sonation in birds, Proceedings of the Royal Society B: Biological Sciences, Volume 275 (2008) no. 1637, pp. 955-962 | DOI
[16] Courtship Displays and Natural History of Scintillant (Selasphorus scintilla) and Volcano (S. flammula) Hummingbirds, The Wilson Journal of Ornithology, Volume 123 (2011) no. 2, pp. 218-228 | DOI
[17] Plumage Reflectance and the Objective Assessment of Avian Sexual Dichromatism, The American Naturalist, Volume 153 (1999) no. 2, pp. 183-200 | DOI
[18] Eye for an eyespot: how iridescent plumage ocelli influence peacock mating success, Behavioral Ecology, Volume 24 (2013) no. 5, pp. 1048-1057 | DOI
[19] Roses are red, violets are blue - so how much replication should you do? An assessment of variation in the colour of flowers and birds, Biological Journal of the Linnean Society, Volume 114 (2015) no. 1, pp. 69-81 | DOI
[20] Handbook of the Birds of the World Alive, Lynx Edicions, (2017)
[21] Revealing the colourful side of birds: spatial distribution of conspicuous plumage colours on the body of Australian birds, Journal of Avian Biology, Volume 51 (2020) no. 1 | DOI
[22] Recherches sur la structure des plumes des trochilidés, Université de Paris, Paris, (1951), 260 pages
[23] Do museum specimens accurately represent wild birds? A case study of carotenoid, melanin, and structural colours in long-tailed manakins Chiroxiphia linearis, Journal of Avian Biology, Volume 40 (2009) no. 2, pp. 146-156 | DOI
[24] Iridescence: a functional perspective, Journal of The Royal Society Interface, Volume 6 (2009) no. suppl_2, p. S115-S132 | DOI
[25] Worldwide patterns of bird colouration on islands, Ecology Letters, Volume 19 (2016) no. 5, pp. 537-545 | DOI
[26] Schillerfarben der Vogelfeder als Evolutionsproblem. Medizinischen Fakultät der Universität Basel, (1977)
[27] Human vision fails to distinguish widespread sexual dichromatism among sexually "monochromatic" birds, Proceedings of the National Academy of Sciences, Volume 102 (2005) no. 31, pp. 10942-10946 | DOI
[28] Evolutionary shifts in the melanin-based color system of birds, Evolution, Volume 70 (2016) no. 2, pp. 445-455 | DOI
[29] The Color of Light in Forests and Its Implications, Ecological Monographs, Volume 63 (1993) no. 1, pp. 1-27 | DOI
[30] Comparing entire colour patterns as birds see them, Biological Journal of the Linnean Society, Volume 86 (2005) no. 4, pp. 405-431 | DOI
[31] Reproductive character displacement of female mate choice in the grey treefrog, Hyla chrysoscelis, Animal Behaviour, Volume 47 (1994) no. 4, pp. 959-969 | DOI
[32] Influence of ambient light on the evolution of colour signals: comparative analysis of a Neotropical rainforest bird community, Ecology Letters, Volume 7 (2004) no. 4, pp. 279-284 | DOI
[33] Simultaneous Crypsis and Conspicuousness in Color Patterns: Comparative Analysis of a Neotropical Rainforest Bird Community, The American Naturalist, Volume 169 (2007) no. S1 | DOI
[34] Phylogenetic structure in tropical hummingbird communities, Proceedings of the National Academy of Sciences, Volume 106 (2009) no. Supplement_2, pp. 19673-19678 | DOI
[35] Songs of Darwin's finches diverge when a new species enters the community, Proceedings of the National Academy of Sciences, Volume 107 (2010) no. 47, pp. 20156-20163 | DOI
[36] An Intergeneric Hybrid Hummingbird (Heliodoxa leadbeateri X Heliangelus amethysticollis) from Northern Colombia, The Condor, Volume 92 (1990) no. 3, pp. 754-760 | DOI
[37] The role of interspecific interference competition in character displacement and the evolution of competitor recognition, Biological Reviews, Volume 84 (2009) no. 4, pp. 617-635 | DOI
[38] Reproductive Interference Between Animal Species, The Quarterly Review of Biology, Volume 83 (2008) no. 3, pp. 257-282 | DOI
[39] Quantitative characterization of iridescent colours in biological studies: a novel method using optical theory, Interface Focus, Volume 9 (2019) no. 1 | DOI
[40] Hummingbird iridescence: an unsuspected structural diversity influences colouration at multiple scales, Hummingbird iridescence: an unsuspected structural di- versity influences colouration at multiple scales. bioRxiv, 699744, (2019) | DOI
[41] Testing the spatial phylogenetic structure of local communities: statistical performances of different null models and test statistics on a locally neutral community, Journal of Ecology, Volume 96 (2008) no. 5, pp. 914-926 | DOI
[42] Characterizing the phylogenetic structure of communities by an additive partitioning of phylogenetic diversity, Journal of Ecology, Volume 95 (2007) no. 3, pp. 493-506 | DOI
[43] Microspectrophotometry of visual pigments and oil droplets in a marine bird, the wedge-tailed shearwater Puffinus pacificus: topographic variations in photoreceptor spectral characteristics, Journal of Experimental Biology, Volume 207 (2004) no. 7, pp. 1229-1240 | DOI
[44] Colour pattern divergence in reef fish species is rapid and driven by both range overlap and symmetry, Ecology Letters, Volume 22 (2019) no. 1, pp. 190-199 | DOI
[45] Spectral sensitivities of photoreceptors and their role in colour discrimination in the green-backed firecrown hummingbird (Sephanoides sephaniodes), Journal of Comparative Physiology A, Volume 194 (2008) no. 9, pp. 785-794 | DOI
[46] Synchronization of speed, sound and iridescent color in a hummingbird aerial courtship dive, Nature Communications, Volume 9 (2018) no. 1 | DOI
[47] The Function of Displays of Male Rufous Hummingbirds, The Condor, Volume 103 (2001) no. 3, pp. 647-651 | DOI
[48] The global diversity of birds in space and time, Nature, Volume 491 (2012) no. 7424, pp. 444-448 | DOI
[49] The fragility of extreme specialization: Passiflora mixta and its pollinating hummingbird Ensifera ensifera, Journal of Tropical Ecology, Volume 17 (2001) no. 2, pp. 323-329 | DOI
[50] Reinforcement of pre-zygotic isolation and karyotype evolution in Agrodiaetus butterflies, Nature, Volume 436 (2005) no. 7049, pp. 385-389 | DOI
[51] The influence of the acoustic community on songs of birds in a neotropical rain forest, Behavioral Ecology, Volume 20 (2009) no. 4, pp. 864-871 | DOI
[52] pavo 2: New tools for the spectral and spatial analysis of colour in r, Methods in Ecology and Evolution, Volume 10 (2019) no. 7, pp. 1097-1107 | DOI
[53] Color Patterns of Closely Related Bird Species Are More Divergent at Intermediate Levels of Breeding-Range Sympatry, The American Naturalist, Volume 185 (2015) no. 4, pp. 443-451 | DOI
[54] Birds associate species-specific acoustic and visual cues: recognition of heterospecific rivals by male blackcaps, Behavioral Ecology, Volume 16 (2005) no. 2, pp. 467-471 | DOI
[55] Molecular Phylogenetics and the Diversification of Hummingbirds, Current Biology, Volume 24 (2014) no. 8, pp. 910-916 | DOI
[56] Interspecific variation in plumage colour among birds: species recognition or light environment?, Journal of Evolutionary Biology, Volume 15 (2002) no. 4, pp. 505-514 | DOI
[57] Quantifying iridescent coloration in animals: a method for improving repeatability, Behavioral Ecology and Sociobiology, Volume 65 (2011) no. 6, pp. 1317-1327 | DOI
[58] Dietary protein level affects iridescent coloration in Anna's hummingbirds, Calypte anna, Journal of Experimental Biology, Volume 215 (2012) no. 16, pp. 2742-2750 | DOI
[59] Analyzing Colors. In: Bird Coloration, Volume 1: Mechanisms and Mea- surements. Ed. by Geoffrey E. Hill and Kevin J. McGraw. Vol. 1. 2 vols. Bird Coloration, Harvard University Press, (2006), 640 pages
[60] Experimental evidence for extreme dispersal limitation in tropical forest birds, Ecology Letters, Volume 11 (2008) no. 9, pp. 960-968 | DOI
[61] Disruptive sexual selection against hybrids contributes to speciation between Heliconius cydno and Heliconius melpomene, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 268 (2001) no. 1478, pp. 1849-1854 | DOI
[62] Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists, Biological Reviews, Volume 85 (2010), pp. 935-956 | DOI
[63] Complex Distribution of Avian Color Vision Systems Revealed by Sequencing the SWS1 Opsin from Total DNA, Molecular Biology and Evolution, Volume 20 (2003) no. 6, pp. 855-861 | DOI
[64] Pollinating birds differ in spectral sensitivity, Journal of Comparative Physiology A, Volume 196 (2010) no. 2, pp. 91-96 | DOI
[65] Spectral reflectance and directional properties of structural coloration in bird plumage, Journal of Experimental Biology, Volume 205 (2002) no. 14, pp. 2017-2027 | DOI
[66] A review of the evolution of animal colour vision and visual communication signals, Vision Research, Volume 48 (2008) no. 20, pp. 2042-2051 | DOI
[67] Biological Evolution and Statistical Physics, Lecture Notes in Physics, Springer Berlin Heidelberg, Berlin, Heidelberg, (2002) | DOI
[68] 515 million years of structural colour, Journal of Optics A: Pure and Applied Optics, Volume 2 (2000) no. 6 | DOI
[69] Incorporating Clade Identity in Analyses of Phylogenetic Community Structure: An Example with Hummingbirds, The American Naturalist, Volume 176 (2010) no. 5, pp. 573-587 | DOI
[70] Color evolution in the hummingbird genuscoeligena, Evolution, Volume 64 (2010) no. 2, pp. 324-335 | DOI
[71] Lek Behavior of the Plovercrest (Stephanoxis lalandi, Trochilidae), The Wilson Journal of Ornithology, Volume 124 (2012) no. 1, pp. 106-112 | DOI
[72] Anatomy, physics, and evolution of structural colors. In: Bird Coloration, Vol- ume 1: Mechanisms and Measurements. Ed. by Geoffrey E. Hill and Kevin J. McGraw. Vol. 1. 2 vols. Bird Coloration, Harvard University Press, (2006), 640 pages
[73] The birds of Ecuador: status, distribution and taxonomy. 2001. 880 pp., Cornell University Press, Ithaca, NY, (2001), 640 pages
[74] A sexually selected character displacement in flycatchers reinforces premating isolation, Nature, Volume 387 (1997) no. 6633, pp. 589-592 | DOI
[75] Experimental trait mismatches uncover specificity of evolutionary links between multiple signaling traits and their interactions in hummingbirds*, Evolution, Volume 73 (2019) no. 3, pp. 436-451 | DOI
[76] It's not just what you have, but how you use it: solar-positional and behavioural effects on hummingbird colour appearance during courtship, Ecology Letters, Volume 21 (2018) no. 9, pp. 1413-1422 | DOI
[77] Two ways to display: male hummingbirds show different color-display tactics based on sun orientation, Behavioral Ecology, Volume 29 (2018) no. 3, pp. 637-648 | DOI
[78] Aggressive and Courtship Displays of the Male Anna's Hummingbird, The Condor, Volume 84 (1982) no. 2, pp. 208-225 | DOI
[79] Diagnosis and observations of a hybrid hummingbird (Metallura tyrianthina x Aglaiocercus kingi) in the Eastern Andes of Colombia, Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, Volume 39 (2015) no. 153, pp. 481-490 | DOI
[80] Ecology and evolution of lek mating behavior in the long-tailed hermit hummingbird, Ornithological Monographs, Volume iii–78 (1979) | DOI
[81] Evolution of Avian Plumage Color in a Tetrahedral Color Space: A Phylogenetic Analysis of New World Buntings, The American Naturalist, Volume 171 (2008) no. 6, pp. 755-776 | DOI
[82] rptR: repeatability estimation and variance decomposition by generalized linear mixed‐effects models, Methods in Ecology and Evolution, Volume 8 (2017) no. 11, pp. 1639-1644 | DOI
[83] Neotropical birds: ecology and conservation. Vol. 3, University of Chicago Press, (1996)
[84] Hummingbird flight: Sustaining the highest mass-specific metabolic rates among vertebrates, Experientia, Volume 48 (1992) no. 6, pp. 565-570 | DOI
[85] Species interactions and the structure of complex communication networks, Proceedings of the National Academy of Sciences, Volume 111 (2014) no. 3, pp. 1020-1025 | DOI
[86] Signal design and perception inhypocnemisantbirds: evidence for convergent evolution via social selection, Evolution, Volume 63 (2009) no. 12, pp. 3168-3189 | DOI
[87] New multidimensional functional diversity indices for a multifaceted framework in functional ecology, Ecology, Volume 89 (2008) no. 8, pp. 2290-2301 | DOI
[88] Natural photonics, Physics World, Volume 17 (2004) no. 2, pp. 35-39 | DOI
[89] Reproducible research in the study of biological coloration, Animal Behaviour, Volume 106 (2015), pp. 51-57 | DOI
[90] Brilliant camouflage: photonic crystals in the diamond weevil, Entimus imperialis, Proceedings of the Royal Society B: Biological Sciences, Volume 279 (2012) no. 1738, pp. 2524-2530 | DOI
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