JOURNAL OF AVIAN BIOLOGY www.avianbiology.org Journal of Avian Biology 1 –––––––––––––––––––––––––––––––––––––––– © 2019 The Authors. Journal of Avian Biology © 2019 Nordic Society Oikos Subject Editor: Alexandre Roulin Editor-in-Chief: Jan-Åke Nilsson Accepted 26 May 2019 2019: e02041 doi: 10.1111/jav.02041 doi: 10.1111/jav.02041 00 1–8 Black plumage is expected to absorb and retain more heat and provide better protection against UV radiation compared with lighter plumages. Black plumage is common in species of the genera Turdus and Platycichla that inhabit highlands across different regions of the world. Considering this geographical recurrent pattern we tested the hypothesis that black plumage in these two genera has evolved as a co-adaptive response to inhabiting highlands, reconstructing ancestral character states for plumage and altitudinal distribution using maximum-likelihood methods, and a Pagel’s multistate discrete method. For these analyses, we used a phylogeny based on mitochondrial and nuclear DNA regions that included 60 of the 66 recognized species in the genera Turdus and Platycichla. We found that black-plumage coloration evolved independently on eight occasions within these two genera, and species with black plumage occur more often at highlands. Our results support the hypothesis that black-plumage is adaptative in highlands; but, studies in other bird groups with black- plumage inhabiting at the same elevations will provide evidence for this adaptive hypothesis or if the evolution of black-plumage in other groups is explained by other evolutionary forces. Keywords: black color, color evolution, comparative analysis, highland birds, Passeriformes, UV defense Introduction The climatic conditions prevailing at highlands (> 2500 m a.s.l.) impose several con- straints to those species that colonize and inhabit high mountain habitats. At these elevations low temperatures, low atmospheric pressure and oxygen levels, and high solar radiation often function as barriers, limiting the number of species that adapt to these conditions (Körner 2007, Keller et al. 2013). A fair amount of studies have focused on breathing rates (Ramirez et al. 2007, Storz et al. 2010, Ivy and Scott 2015), body morphology (Price 1991, Landmann and Winding 1995, Bears  et  al. 2008), cold tolerance (Swanson and Liknes 2006, Swanson and Garland 2009), mass change (Bears et al. 2008) or change in plumage color (Friedman and Remeŝ 2017, Delhey 2018, Galván et al. 2018, Medina et al. 2018), to understand the adaptive response of birds to highland environments. Is black plumage an adaptation to high elevations in a cosmopolitan bird genus? Luis Sandoval and Gilbert Barrantes L. Sandoval (https://orcid.org/0000-0002-0793-6747) ✉ (biosandoval@hotmail.com) and G. Barrantes, Escuela de Biología, Univ. de Costa Rica, San Pedro, San José, Costa Rica. Article 2 The evolution of plumage coloration is the consequence of the combined effect of sexual and natural selection and the effect of each of these evolutionary forces varies among species and between sexes, since each of these forces may affect differently the individual reproduction in each spe- cies (Hill 1991, Bennett et al. 1994). For instance, species in which concealment is important, plumage coloration matches the surroundings, or the coloration of other spe- cies (Bortolotti 2006). This is the case of ptarmigans whose plumage change seasonally to match the background (Madge and McGowan 2002), or cuckoos whose plumage mimic that of hawk predators (Gluckman and Mundy 2013, Trnka and Grim 2013). In many other species, there are striking differences in plumage coloration between sexes, in which females are usually cryptic and males have bright and sometimes extravagant plumages as a result of sexual selec- tion (e.g. Paradisaeidae, Pipridae, Cotingidae; Andersson 1994, Zahavi and Zahavi 1997, Bortolotti 2006, Dale et al. 2015). Despite that evolutionary causes of plumage color- ation have received much attention (Darwin 1871, Wallace 1889, Huxley 1942, Mayr 1942, Cowless  et  al. 1967), the effect of high mountain environmental conditions on the evolution of plumage coloration has been overlooked (McNaught and Owens 2002, Galeotti et al. 2003, Badyaev and Young 2004). In birds (e.g. Turdidae and Thraupidae), insects (e.g. flies and butterflies) and reptiles, there is a remarkable pattern wherein species that inhabit highlands have black or more melanized body coloration (Isler and Isler 1999, Clement and Hathway 2000, Ellers and Boggs 2002, 2004, Collar 2005, Pool and Aquadro 2007, Parkash  et  al. 2008, 2010, Wittkopp  et  al. 2011). Although this pattern has been reported multiple times, to our best knowledge the relation- ship between black coloration and highland occupancy in birds have not been studied using a comparative phyloge- netic approach; although this method has been used to study the effect of other habitats in bird coloration (Delhey 2018, Galván et al. 2018). It is well known that coloration of some bird species correlates with some climatic conditions (e.g. precipitation or temperature; Delhey  et  al. 2019, Romano  et  al. 2019). For example, in deserts populations of some bird species have lighter plumage coloration compared with popula- tions inhabiting more humid environments (Gloger’s rule; Gloger 1833, Serventy 1971, Delhey 2018); though many species inhabiting deserts have black-plumages (Ward et al. 2002). The lighter plumage presumably reduces heat transfer (Mayr 1963), but several hypotheses have been proposed to explain the adaptation of black-plumage to desertic environ- ments (Serventy 1971; see Ward  et  al. 2002 for a review): resistance to abrasion, protection against feather-degradation by bacteria, protection against UV radiation, reduction of skin heat stress, reduction of metabolic costs by allowing birds activity at dawn and dusk when temperatures decrease drastically, social signaling and night camouflage (Zink and Remsen 1986, Ward  et  al. 2002, Burtt and Ichida 2004, Goldstein et al. 2004, Lodei 2013). In cold highland environments, many bird species have also black plumage contradicting the Gloger’s Rule that expect more species with dark plumage in warmer regions (Serventy 1971, Ward et al. 2002), but agreeing with the Bogert’s rule (Bogert 1949, Clusella Trullas  et  al. 2007, Gaston  et  al. 2008), which proposes that darker color improves thermo- regulation efficacy in cold conditions. The energetic cost of thermoregulation increases in birds as the difference between body temperature and ambient temperature increases (Calder and King 1974, Keller et al. 2013, Stager et al. 2015), and its effect is expected to be more severe at high elevations. Two conditions reduce the thermoregulation cost in birds: 1) hypothermia and torpor in which birds by lowering their body temperature reduce their thermal gradient, and 2) the use of an external heat source (e.g. solar radiation), which reduces the metabolic cost of maintaining the body tempera- ture constant, particularly when ambient temperature is very low. Birds with dark coloration presumably absorb and retain more heat, and protect themselves more effectively against UV radiation than those birds with lighter plumages (Heppner 1970, Walsberg 1983, Bittner  et  al. 2002, Goldstein  et  al. 2004, Bortolotti 2006). Considering the higher cost of main- taining body temperature constant and the negative effect of UV radiation in highland environments, we hypothesize that dark plumage should evolve more frequently in highlands than at lower elevations. In this study, our main objective is to reconstruct the evo- lution of plumage color and altitudinal distribution in two sister genera Turdus and Platycichla to test the hypothesis that black-plumage has evolved as an adaptation to inhabit highlands. We mapped the evolution of black-plumage evo- lution onto the phylogeny of the genus Turdus (Voelker et al. 2007) and examined whether evolutionary changes in black coloration are associated with occupancy of highland environments. We predicted that if black-plumage is an adaptation to inhabit cold highlands as Bogerts’ Rule pre- dict, thrushes with black-plumage evolved from lowlands species with lighter plumages. But, if black-plumage is not an adaptation to inhabit cold highlands, thrush species with black-plumage are expected to have evolved from a lowland species with black-plumage. Material and methods Scoring plumage and altitude distribution We obtained the information on thrush species plumage from descriptions of species and illustrations (Clement and Hathway 2000, Collar 2005). We classified species’ plum- age into three categories: black, brown and grey. We assigned birds to a particular category if the plumage of a particular color (e.g. black) covers > 50% of the body, including the dorsal parts (dorsum of birds is more exposed to solar radia- tion and coloration on it is expected to have little influence of sexual selection, since in thrushes vocalizations play the main role for mating; Vargas-Castro et al. 2012, 2015). In species 3 in which females have lighter plumage than males (Clement and Hathway 2000, Collar 2005), we used only the male col- oration in our analysis. The altitudinal distribution of each species was obtained from Clement and Hathway (2000) and Collar (2005) and references therein, and from unpub- lished records of the authors. The distribution of the species included in Collar (2005) could be updated with recent eBird data and is possible to visually compare both distributions visiting each thrush species web page in Handbook of the birds of the world alive at . The altitudinal distribution is reported as a range in these references, but for the analyses of the species included in this study, we used the lower, the upper and the midpoint of each species dis- tribution. We used lower and upper distribution limits to test whether extreme altitudinal distributions influence the plumage color. However, we chose the mid distribution point as the best indicator for each-species altitudinal distribution, because abundance tends to peak around the center of the altitudinal distribution for many bird species (Clement and Hathway 2000). Ancestral state reconstruction and comparative analysis We used the molecular phylogeny of thrushes published by Voelker  et  al. (2007) which includes 60 of the 66 rec- ognized species in the genera Turdus and Platycichla, and several subspecies and individuals per species and subspecies (Voelker  et  al. 2007, Melo  et  al. 2010). This phylogeny is based on mitochondrial (cytochrome b and ND2) and nuclear DNA regions (RAG1, beta fibrinogen intron 5, aconitase 1 intron 10 and myoglobin intron 2). We eliminated from the ancestral state reconstruction and comparative analysis all subspecies that have the same plumage color. Additionally, we eliminated individuals of the same species and subspe- cies that were in the same clade, so that we ended with a tree that included 65 taxa (Fig. 1). In the case of T. olivaceus the relationship between subspecies and their taxonomic status is unclear (Voelker et al. 2007, Melo et al. 2010); and for that reason we used in our analysis those subspecies with different plumage pattern included in different clades. We reconstructed ancestral character states for plumage using the maximum-likelihood method in Mesquite ver. 3.02 (Maddison and Maddison 2015). We used Markov k-state one parameter model for the maximum-likelihood analysis, which assumes an equal rate of change of charac- ters, as in previous studies of discrete ancestral state charac- ter reconstructions (Schluter et al. 1997, Price et al. 2009, Odom et al. 2013). To reconstruct the altitudinal distribu- tion of the species we used the square-change parsimony method in Mesquite ver. 3.02 weighted by branch length. This method assumes that large evolutionary changes, in this case altitudinal distribution, occur more likely in lon- ger branches; but, this method minimizes the evolutionary changes by dividing the the sum of squared changes between the branch lengths (Nunn 2011). Additionally, this method provides values equivalent to the maximum likelihood estimate under Brownian motion (Schluter  et  al. 1997, Maddison and Maddison 2000, Nunn 2011). We tested if black-plumage coloration in thrushes occurs more often in species that inhabit high elevations using a phylogenetic regression with a mixture of discrete (non- black = 0, and black plumage = 1; dependent variable) and continuous characters (lower, upper and midpoint altitudinal distribution values; independent variable). We used the func- tion ‘compar.gee’ of the library ‘ape’ in R, with a binomial family to run a logistic regression analysis corrected by the phylogenetic relationship between species. Data deposition Data available from the Dryad Digital Repository: < http:// dx.doi.org/10.5061/dryad.mm4qb48 > (Sandoval and Barrantes 2019). Results Fourteen Turdus species have black-plumage based on our classification method. The reconstruction of the coloration of thrushes using maximum likelihood indicated that black coloration evolved from a brown ancestor at the basal node (rate = 0.18; –log likelihood = 69.55; Fig. 1a), and black- plumage evolved independently on eight occasions. In four cases the black-plumage evolved as basal in a clade, and within these clades, seven species maintained the black- plumage, but five species lost the black-plumage and evolved to another plumage (Fig. 1). In the other four occasions (once at the north of Europe, once in south of Africa and twice in South America) black-plumage evolved from a black/gray ancestor (Fig. 1). Squared-change parsimony reconstruc- tion of the altitudinal origin of all thrushes indicated that the genus evolved from an ancestor inhabiting approximately 1413 m a.s.l. (SE = 387 m, confidence intervals: 639–2186 m a.s.l.; Fig. 1). From the 11 species with midpoint elevation higher than 2000 m a.s.l., six species (T. kessleri, T. rufitorques, T. nigrescens, T. infuscatus, T. plebejus and T. merula) evolved between 920 and 1536 m a.s.l. (Fig. 1). The other five species (T. serranus, T. chiguanco, T. fuscator, T. olivaceus smithi and T. olivaceus abyssinicus) evolved above 2000 m a.s.l. (Fig. 1). Black plumage was correlated with altitudinal distribution in thrushes (Fig. 2). The black plumage was associated with higher elevations, in the lower (slope esti- mate ± SE = 0.0016 ± 0.0005, t = 3.26, df = 26.94, p = 0.003), upper (slope estimate ± SE = 0.0012 ± 0.0003, t = 3.67, df = 26.94, p = 0.001) and midpoint of the altitudinal distribu- tion of thrush species (slope estimate ± SE = 0.0022 ± 0.0005, t = 4.15, df = 26.94, p < 0.001). Discussion The black-plumage in the genus Turdus is more common in highland species, and its evolution correlates with the 4 Figure 1. Maximum-likelihood reconstruction using a Markov k-state one parameter model with equal characters change rate for black- plumage color. Black circles: black-plumage color. White circles: brown plumage color. Dark grey circles: grey plumage color; light grey circles: multiple plumage color. Proportional likelihood of ancestral states characters are indicated by the color distribution inside the circles. Number inside of the figure represent the altitudinal distribution in meters (rounded to the closed number) of the ancestors of actual species according to the altitudinal reconstruction. 5 occupancy of highlands. Black-plumage evolved indepen- dently multiple times from different ancestors within the genus and most of these events occurred at middle eleva- tion. The multiple times that black-plumage thrushes colo- nized highlands support the adaptive response to the climatic conditions such as low temperatures and high levels of UV radiations, prevailing at high elevation (Walsberg 1983, Goldstein  et  al. 2004, Bortolotti 2006). In cold habitats black-plumage could favor thermoregulation by increasing absorption of solar radiation (Bittner et al. 2002), reducing the energy cost of maintaining the body temperature con- stant especially when the ambient temperature is very low. The melanin pigment in black feathers could also function as a UV radiation screen (Bechtel 1978), which increases rapidly with elevation (Bechtel 1978). This pigment absorbs more effectively the UV radiation than other pig- ments (Bergman 1982, Brenner and Hearing 2008). These two functions of black-plumage are not mutually exclusive and likely both have influenced the recurrent evolution of black plumage in highland thrushes than at other elevations. However, direct evidence comparing the thermoregulation effect and UV radiation absorption in close-related species with black-plumage and other color-plumage in highlands is needed to quantitatively test the function of black-plumage coloration. In most species of highland thrushes, males are black, while females are light black (Clement and Hathway 2000, Collar 2005). This sexual dichromatism could be the effect of females selecting darker males (sexual selection), or that males are more exposed to radiation during acoustic dis- plays (sexual selection/natural selection). Displaying males of several bird species tend to be in more open areas because they use exposed perches to vocalize and transmit better and farther their acoustic signals (Krams 2001, Mathevon et al. 2005, Sandoval et al. 2015). The most probable elevation for the origin of thrush spe- cies was between 1000 and 2000 m a.s.l., since the ancestral species for all analyzed species (after the altitudinal recon- struction) showed an ancestral middle distribution of 1413 m a.s.l. From this elevation different thrush species colonized lowlands and highlands on several occasions, according to the actual distribution of the species tha inhabit below and above the original ancestral distribution. Especifically for highland species, we found five colonization events in America, one in Europe and two in Africa. For example, T. plebejus an American highland species (2162 m a.s.l. in the middle spe- cies distribution point) evolved from an ancestor with a mid- dle elevation distribution (ca 1611 m a.s.l.). Also, T. olivaceus smithi an African highland species (2450 m a.s.l. in the middle species distribution point) evolved from an African ancestor with a middle elevation distribution (ca 1643 m a.s.l.). These events of colonization were likely associated with the uplift of mountains in those continents or increasing warmer weather after the last glaciations. Both of these factors have been pre- sumably important for highland colonization in other bird species (Cook 1974, Weir 2006, Barrantes 2009). However, to associate the origin of these species directly with geologi- cal and climatic events would require a different approach that incorporates the time scale and the study of geological events in each continent, which is beyond the scope of this investigation. The latitudinal distribution of the thrush species could be a confounding factor for our results (Clement and Hathway 2000, Collar 2005), because low ambient temperature is presumably an important factor in the evolution of black Figure 2. Logistic regression of the relationship between the altitu- dinal distribution using the lower, higher and middle distribution per thrush species (each dot) and the occurrence of black-plumage. 6 plumage in thrushes, and at higher latitudes the tempera- ture is lower than at equatorial latitudes at the same altitude (Freeman 2017). It is then expected that if black-plumage coloration is the result of adaptation to low temperatures, species with high latitudinal distributions would have black- plumage coloration independently of the altitude. However, this appears to be not the case, since from the six European and Eurasian thrush species occupying northern latitudes only two have black-plumage (Clement and Hathway 2000, Collar 2005, Supplementary material Appendix 1). Additionally, several of the thrush species occupying north- ern latitudes have complete (all individuals from a species migrate to non-reproductive areas without geographical overlap in both distributions) or partial (all individuals from one species migrate to non-reproductive areas, but repro- ductive and non-reproductive areas overlap geographically) latitudinal migrations (Clement and Hathway 2000, Collar 2005). Thereby, during the winter when ambient temperature lowers at higher latitudes, individuals are wintering in warmer areas; thus, these species have not had the pressure to evolve black-plumage coloration to cope with cold temperatures as seems to be the case for tropical highland species that inhabit cold environments year-round (Clement and Hathway 2000, Collar 2005). In conclusion, we found that black-plumage coloration evolved independently on eight occasions in the genus Turdus and species with black-plumage occurred more often at highlands. Highland Turdus species evolved from a middle elevation ancestor and from there eight independent lin- eages colonized the highlands. However, not in all species that colonized the highlands evolved the black-plumage coloration. Acknowledgements – We thank Gary Voelker for allow us to access to the Turdus phylogenetic tree. We also thank Daniel Cadena, Pierre- Paul Bitton and two anonymous reviewers for all the valuables comments to a draft of this manuscript. Funding – This study was funded by Vicerrectoría de Investigación, Univ. de Costa Rica. Author contributions – Both conceived the idea of the study and wrote the manuscript. The first author performed the analyses. References Andersson, M. 1994. Sexual selection. – Princeton Univ. Press. Badyaev, A. V. and Young, R. L. 2004. Complexity and integration in sexual ornamentation: an example with carotenoid and melanin plumage pigmentation. – J. Evol. Biol. 17: 1317–1327. Barrantes, G. 2009. The role of historical and local factors in determining species composition of the highland avifauna of Costa Rica and western Panamá. – Rev. Biol. Trop. 57: 333–346. Bears, H., Drever, M. C. and Martin, K. 2008. Comparative morphology of dark-eyed juncos Junco hyemalis breeding at two elevations: a common aviary experiment. – J. Avian Biol. 39: 152–162. Bechtel, H. B. 1978. Color and pattern in snakes (Reptilia, Serpentes). – J. Herpet. 12: 521–532. Bennett, A. T. D., Cuthill, I. C. and Norris, K. J. 1994. Sexual selection and the mismeasure of color. – Am. Nat. 144: 848–860. Bergman, G. 1982. Why are the wings of Larus f. fuscus so dark? – Ornis Fenn. 59: 77–83. Bittner, T. D., King, R. B. and Kerfin, J. M. 2002. Effects of body size and melanism on the thermal biology of garter snakes (Thamnophis sirtalis). – Copeia 2002: 477–482. Bogert, C. M. 1949. Thermoregulation in reptiles, a factor in evolution. – Evolution 3: 195–211. Bortolotti, G. R. 2006. Natural selection and coloration: protection, concealment, advertisement or deception? – In: Hill, G. E. and McGraw, K. J. (eds), Bird coloration: function and evolution. Harvard Univ. Press, pp. 3–35. Brenner, M. and Hearing, V. J. 2008. The protective role of melanin against UV damage in human skin. – Photochem. Photobiol. 84: 539–549. Burtt, E. H. Jr. and Ichida, J. M. 2004. Gloger’s rule, feather- degrading bacteria and color variation among Song Sparrows. – Condor 106: 681–686. Calder, W. A. and King, J. R. 1974. Thermal and caloric relations of birds. – Avian Biol. 4: 259–413. Clement, P. and Hathway, R. 2000. Thrushes. – Christopher Helm. Clusella Trullas, S., van Wyk, J. H. and Spotila, J. R. 2007. Thermal melanism in ectotherms. – J. Therm. Biol. 32: 235–245. Collar, N. J. 2005. Family Turdidae (Thrushes). – In: del Hoyo, J., Elliott, A. and Christie, D. (eds), Handbook of the birds of the world, Vol. 10. Cuckoo-shrikes to thrushes. Lynx Edicions, pp. 514–807. Cook, R. E. 1974. Origin of the highland avifauna of Southern Venezuela. – Syst. Biol. 23: 257–264. Cowles, R. B., Hamilton, W. J. and Heppner, F. 1967. Black pigmentation: adaptation for concealment or heat conservation? – Science 158: 1340–1341. Dale, J., Dey, C. J., Delhey, K., Kempenaers, B. and Valcu, M. 2015. The effects of life history and sexual selection on male and female plumage colouration. – Nature 527: 367–370. Darwin, C. 1871. The descent of man, and selection in relation to sex. – Murray. Delhey, K. 2018. Darker where cold and wet: Australian birds follow their own version of Gloger’s rule. – Ecography 41: 673–683. Delhey, K., Dale, J., Valcu, M. and Kempenaers, B. 2019. Reconciling ecogeographical rules: rainfall and temperature predict global colour variation in the largest bird radiation. – Ecol. Lett. doi:10.1111/ele.13233. Ellers, J. and Boggs, C. L. 2002. The evolution of wing color in Colias butterflies: heritability, sex linkage and population divergence. – Evolution 56: 836–840. Ellers, J. and Boggs, C. L. 2004. Evolutionary genetics of dorsal wing colour in Colias butterflies. – J. Evol. Biol. 17: 752–758. Freeman, B. G. 2017. Little evidence for Bergmann’s rule body size clines in passerines along tropical elevational gradients. – J. Biogeogr. 44: 502–510. Friedman, N. R. and Remeŝ, V. 2017. Ecogeographical gradients in plumage coloration among Australasian songbird clades. – Global Ecol. Biogeogr. 26: 261–274. Galeotti, P., Rubolini, D., Dunn, P. O. and Fasola, M. 2003. Colour polymorphism in birds: causes and functions. – J. Evol. Biol. 16: 635–646. 7 Galván, I., Rodríguez-Martínez, S. and Carrascal, L. M. 2018. Dark pigmentation limits thermal niche position in birds. – Funct. Ecol. 32: 1531–1540. Gaston, K. J., Chown, S. L. and Evans, K. L. 2008. Ecogeographical rules: elements of a synthesis. – J. Biogeogr. 35: 483–500. Gloger, C. W. L. 1833. Das Abändern der Vögel durch Einfluss des Klimas. – Breslau. Gluckman, T. L. and Mundy, N. I. 2013. Cuckoos in raptors’ clothing: barred plumage illuminates a fundamental principle of Batesian mimicry. – Anim. Behav. 86: 1165–1181. Goldstein, G., Flory, K. R., Browne, B. A., Majid, S., Ichida, J. M. and Burtt, E. H. 2004. Bacterial degradation of black and white feathers. – Auk 121: 656–659. Heppner, F. 1970. The metabolic significance of differential absortion of radiant energy by black and white birds. – Condor 72: 50–59. Hill, G. E. 1991. Plumage coloration is a sexually selected indicator of male quality. – Nature 350: 337–339. Huxley, J. S. 1942. Evolution, the modern synthesis. – Allen and Unwin. Isler, M. L. and Isler, P. R. 1999. The Tanagers: natural history, distribution and identification. – Smithsonian. Ivy, C. M. and Scott, G. R. 2015. Control of breathing and the circulation in high-altitude mammals and birds. – Comp. Biochem. Physiol. A 186: 66–74. Keller, I., Alexander, J. M., Holderegger, R. and Edwards, P. J. 2013. Widespread phenotypic and genetic divergence along altitudinal gradients in animals. – J. Evol. Biol. 26: 2527–2543. Körner, C. 2007. The use of ‘altitude’ in ecological research. – Trends Ecol. Evol. 22: 569–574. Krams, I. 2001. Perch selection by singing chaffinches: a better view of surroundings and the risk of predation. – Behav. Ecol. 12: 295–300. Landmann, A. and Winding, N. 1995. Guild organization and morphology of high-elevation granivorous and insectivorous birds: convergent evolution in an extreme environment. – Oikos 73: 237–250. Lodei, T. 2013. Alternation of clear-cut colour patterns in Corvus crow evolution accords with learning-dependent social selection against unusual-looking conspecifics. – Ibis 155: 632–634. Maddison, W. P. and Maddison, D. R. 2000. MacClade: analysis of phylogeny and character evolution. – Sinauer Assoc. Maddison, W. P. and Maddison, D. R. 2015. Mesquite: a modular system for evolutionary analysis, ver. 3.02. – Available at: . Accessed 1 March 2015. Madge, S. and McGowan, P. 2002. Pheasants, partridge and grouse. – Princeton Univ. Press. Mathevon, N., Dabelsteen, T. and Blumenrath, S. H. 2005. Are high perches in the blackcap Sylvia atricapilla song or listening posts? A sound transmission study. – J. Acoustic Soc. Am. 117: 442–449. Mayr, E. 1942. Systematics and the origin of species. – Columbia Univ. Press. Mayr, E. 1963. Animal species and evolution. – Harvard Univ. Press. McNaught, M. K. and Owens, I. P. F. 2002. Interspecific variation in plumage colour among birds: species recognition or light environment? – J. Evol. Biol. 15: 505–514. Medina, I., Newton, E., Kearney, M. R., Mulder, R. A., Porter, W. P. and Stuart-Fox, D. 2018. Reflection of near-infrared light confers thermal protection in birds. – Nat. Commun. 9: 3610. Melo, M, Bowie, R. C. K., Voelker, G., Dallimer, M., Collar, N. J. and Jones, P. J. 2010. Multiple lines of evidence support the recognition of a very rare bird species: the Príncipe thrush. – J. Zool. 282: 120–129. Nunn, C. L. 2011. The comparative approach in evolutionary anthropology and biology. – Univ. Chicago Press. Odom, K. J., Hall, M. L., Riebel, K., Omland, K. E. and Langmore, N. E. 2013. Female song is widespread and ancestral in songbirds. – Nat. Commun. 5: 3379. Parkash, R., Rajpurohit, S. and Ramniwas, S. 2008. Changes in body melanisation and desiccation resistance in highland vs. lowland populations of D. melanogaster. – J. Insect Physiol. 54: 1050–1056. Parkash, R., Sharma, V. and Kalra, B. 2010. Correlated changes in thermotolerance traits and body color phenotypes in montane populations of Drosophila melanogaster: analysis of within- and between-population variations. – J. Zool. 280: 49–59. Pool, J. E. and Aquadro, C. F. 2007. The genetic basis of adaptive pigmentation variation in Drosophila melanogaster. – Mol. Ecol. 16: 2844–2851. Price, T. 1991. Morphology and ecology of breeding warblers along an altitudinal gradient in Kashmir, India. – J. Anim. Ecol. 60: 643–664. Price, J. J., Lanyon, S. M. and Omland, K. E. 2009. Losses of female song with changes from tropical to temperate breeding in the New World blackbirds. – Proc. R. Soc. B 276: 1971–1980. Ramirez, J.-M., Folkhow, L. P. and Blix, A. S. 2007. Hypoxia toler- ance in mammals and birds: from the wilderness to the clinic. – Annu. Rev. Physiol. 69: 113–143. Romano, A., Séchaud, R., Hirzel, A. H. and Roulin, A. 2019. Climate-driven convergent evolution of plumage colour in a cosmopolitan bird. – Global Ecol. Biogeol. 28: 496–507. Sandoval, L. and Barrantes, G. 2019. Data from: is black plumage an adaptation to high elevations in a cosmopolitan bird genus? – Dryad Digital Repository, . Sandoval, L., Dabelsteen, T. and Mennill, D. J. 2015. Transmission characteristics of solo songs and duets in a neotropical thicket habitat specialist bird. – Bioacoustics 24: 289–306. Schluter, D., Price, T., Mooers, A. Ø. and Ludwig, D. 1997. Likelihood of ancestor states in adaptive radiation. – Evolution 51: 1699–1711. Serventy, D. L. 1971. Biology of desert birds. – Avian Biol. 1: 287–339. Stager, M., Pollock, H. S., Benham, P. M., Sly, N. D., Brawn, J. D. and Cheviron, Z. A. 2015. Disentangling environmental drivers of metabolic flexibility in birds: the importance of tem- perature extremes versus temperature variability. – Ecography 39: 787–795. Storz, J. F., Scott, G. R. and Cheviron, Z. A. 2010. Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. – J. Exp. Biol. 213: 4125–4136. Swanson, D. L. and Liknes, E. T. 2006. A comparative analysis of thermogenic capacity and cold tolerance in small birds. – J. Exp. Biol. 209: 466–474. Swanson, D. L. and Garland, T. 2009. The evolution of high summit metabolism and cold tolerance in birds and its impact on present-day distributions. – Evolution 63: 184–194. Trnka, A. and Grim, T. 2013. Color plumage polymorphism and predator mimicry in brood parasites. – Front. Zool. 10: 25. 8 Vargas-Castro, L. E., Sánchez, N. V. and Barrantes, G. 2012. Repertoire size and element sharing in the song of the Clay colored Thrush Turdus grayi. – Wilson J. Ornit. 124: 446–453. Vargas-Castro, L. E., Sánchez, N. V. and Barrantes, G. 2015. Song plasticity over time and vocal learning in clay-colored thrushes. – Anim. Cogn. 18: 1113–1123. Voelker, G., Rohwer, S., Bowie, R. C. K. and Outlaw, D. C. 2007. Molecular systematics of a speciose, cosmopolitan songbird genus: defining the limits of, and relationships among, the Turdus thrushes. – Mol. Phylogenet. Evol. 42: 422–434. Wallace, A. R. 1889. Darwinism: an exposition of the theory of natural selection with some of its applications. – Macmillan Publishers. Walsberg, G. E. 1983. Avian ecological energetics. – Avian Biol. 7: 161–220. Ward, J. M., Blount, J. D., Ruxton, G. D. and Houston, D. C. 2002. The adaptive significance of dark plumage for birds in desert environments. – Ardea 90: 311–323. Weir, J. T. 2006. Divergent timing and patterns of species accumu- lation in lowland and highland neotropical birds. – Evolution 60: 842–855. Wittkopp, P. J., Smith-Winberry, G., Arnold, L. L., Thompson, E. M., Cooley, A. M., Yuan, D. C., Song, Q. and McAllister, B. F. 2011. Local adaptation for body color in Drosophila americana. – Heredity 106: 592–602. Zahavi, A. and Zahavi, A. 1997. The handicap principle. A missing piece of Darwin’s puzzle. – Oxford Univ. Press. Zink, R. M. and Remsen, J. V. 1986. Evolutionary processes and patterns of geographic variation in birds. – Curr. Ornithol. 4: 1–69. Supplementary material (available online as Appendix jav- 02041 at < www.avianbiology.org/appendix/jav-02041 >). Appendix 1.