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Rômulo Mendonça Machado Carleial Evolution of Plumage Coloration

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Rômulo Mendonça Machado Carleial Evolution of Plumage Coloration Universidade Federal de Minas Gerais Programa de Pós-Graduação em Ecologia, Conservação e Manejo da Vida Silvestre Rômulo Mendonça Machado Carleial Evolution of plumage coloration and sexual dichromatism in the family Pittidae (Passeriformes:Tyranni) Belo Horizonte Minas Gerais – Brasil 2015 Rômulo Mendonça Machado Carleial Evolution of plumage coloration and sexual dichromatism in the family Pittidae (Passeriformes:Tyranni) Trabalho de dissertação apresentado ao Programa de Pós-Graduação em Ecologia, Conservação e Manejo da Vida Silvestre da Universidade Federal de Minas Gerais como requisito para a obtenção do título de Mestre. Orientador: Prof. Adriano Paglia Coorientadora: Prof.ª Marina Anciães Coorientador: Dr. Richard Prum Belo Horizonte Minas Gerais - Brasil 2015 Abstract The role of different selective pressures underpinning plumage evolution has occupied biologists for the past century. However, only recently have scientists incorporated avian visual models into the study of plumage colors. Pittas are very colorful passerines and offer a great opportunity to investigate the mechanisms behind plumage diversification and intensity in sexual dichomatism. We used a tetrahedral color space model to quantify plumage coloration and a color distance model to access the degree of sexual dichromatism in this family. We tested whether plumage metrics are influenced by ecological variables using Ornstein-Uhlenbeck models with different selective regimes. We also performed an ancestral reconstruction analysis to investigate the evolution of sexual dichromatism in the family. We found that plumage diversity in this group is better explained under a Brownian motion model but that migratory behavior has affected plumage evolution in the genus Pitta. Sexual dichromatism is the plesimorphic condition in pittas and more wider spread than previously reported. Ultra violet reflectance is more pronounced in males of sexually dichromatic species, although conspicuity has increased in both sexes. These findings suggest that reciprocal sexual selection has likely taken place in this group, and that evolution of plumage colors in pittas is complex and has involved more than one evolutionary mechanism. Key words: sexual selection, ultraviolet, tetrahedral color space, avian vision, pittas, migratory Introduction The importance of natural and sexual selection on the evolution of plumage coloration and sexual dichromatism has been part of intense debates among evolutionary biologists (Darwin 1871; Wallace 1889; Anderson 1994). Sexual dichromatism – the difference in coloration between males and females of the same species - occurs when both males and females experience different selective pressures, in many cases because of differences in parental investment (Cunningham and Birkhead 1998; Kimball and Ligon 1999; Amundsen 2000; Badyaev and Hill 2003). Sexual dichromatism has been more strongly associated with sexual selection on males for increased plumage elaboration, presumably because plumage ornaments are either attractive to females (inter- sexual selection) or increase male competitiveness against rivals (intra-sexual selection) (Darwin 1871; Anderson 1994). However, many ecological variables have been invoked to explain variation in sexual dichromatism: increase in predation risk at the nest has been associated with loss in female conspicuity (e.g.Wallace 1868; Soler and Moreno 2012); colder micro-climate and spatial separation of food resources in high altitudes has been associated with increase in male care and reduction in sexual dichromatism (Badyaev, 1997a; Badyaev and Ghalambor, 2001); migratory behavior is widely reported to affect sexual dichromatism, but with mixed results (e.g. Badyaev and Hill 2003; Friedman et al 2009; Dunn et al 2015); to cite a few. With an increase of studies evaluating plumage evolution, we are now aware that shifts towards sexual dichromatism or monochromatism can occur by either loss or gain in plumage ornamentation in both sexes (e.g. Burns 1998; Amundsen 2000; Siefferman and Hill 2005; Hoffman et al 2008, Dunn et al 2015). It is important then, to analyze male and female plumage separately (Badyaev and Hill 2003). Many of the earlier studies on plumage coloration failed to fully evaluate the extent of the complex interactions mentioned above, because they relied on methods that were based solely on human perspective (reviewed in Bennet et al 1994). However, avian visual system is very different from ours in many ways. Birds have tetrachromatic vision that is sensitive to ultraviolet and violet light (Chen and Goldsmith 1986; Hart 2001) and oil droplets in their cone receptors that narrows the absorption spectra, which is believed to reduce the overlap between pigments, increasing the number of hues they can discern (Govardovskii 1983; Vorobyev et al 1998; Vorobyev 2003). Birds are also believed to process achromatic signals independently (Vorobyev and Osorio 1998; Kelber et al. 2003; Jones and Osorio 2004; Endler and Mielke 2005). It is of summary relevance then, that birds signaling should be analyzed under an avian visual model. The tetrahedral color space model (Goldsmith 1990; Endler and Mielke 2005; Endler et al. 2005; Stoddard and Prum 2008) was developed in order to fulfill this predicament, by incorporating avian cone type sensitivities into the equivalent of a human chromaticity space. Each vertex of the tetrahedral represents one of the four birds’ retinal cone types namely uv or violet sensitive (uv/v), short-wavelength- sensitive or blue (s), medium-wavelength-sensitive or green (m), and long-wavelength-sensitive or red (l). Each color has a unique set of relative stimulation values for these cones and therefore a unique position in the avian color space. In this study we examine plumage evolution in the family Pittidae. Pittas are passerines of the suborder Tyranni, mainly distributed in tropical Australasian and Asiatic forests, with two species occurring in tropical Africa. They are currently divided in three genera (Pitta, Erythropitta and Hydrornis) with around 30 species. However, new studies have been raising some subspecies to species level, which would increase this number to more than 40 (Rheindt and Eaton 2010; Irestedt et al 2013). Pittas are small to medium size, usually terrestrial, birds with its diet being constituted mainly by worms and other invertebrates (Erritzoe 2003; Chowdhury et al 2013). The species altitudinal distribution ranges from lowlands to up to 2200m, with altitudinal shift believed to occur in some species (Erritzoe 2003). In all species investigated so far, the mating system is monogamy with bi-parental care, and both sexual dichromatism and monochromatism are present in the family. Migratory behavior occurs in some species of the genus Pitta, although this number may be underestimated, since pittas movements are poorly understood (Erritzoe 2003). It has been suggested that migrant species in the genus Pitta are duller than their sedentary conspecifics, because either migratory behavior constrained plumage evolution or genetic drift in small, sedentary populations promoted plumage diversification (Irestedt et al 2006). However, this hypothesis has never been objectively tested. Pittas are astonishingly colorful birds (Figure 1), which makes them a promising group for the study of plumage evolution. Although they are known as “jewel thrushes” and are popular among bird watchers (Erritozoe 2003), little is known about their ecology and behavior (but see Donald et al 2009). It remains to be investigated whether the great color diversity in this group is a product of adaptive evolution to different ecological conditions or if it has been shaped by other evolutionary mechanisms, such as sexual selection. Therefore, our objectives in this study were to: (1) describe male and female pittas plumage coloration under an avian visual model; (2) quantify sexual dichromatism for each species; (3) test several existing hypotheses regarding evolution of plumage coloration and sexual dichromatism in relation to ecological variables; (4) investigate the correlation between overall plumage contrast and degree of sexual dichromatism and (5) investigate differences in plumage conspicousness between males and females. We hypothesized that birds occupying higher elevations would be duller than birds which are lowland specialists, because of scarcity of resources at higher elevations (Badyaev 1997a; Badyaev and Ghalambor 2001). For an instance, certain plumage hues can be environmentally constrained, such as the majority of carotenoid-based colors, since its metabolic precursors can be only obtained through diet (reviewed in Hill and McGraw 2006b). We also expect ground nesting birds to be more cryptic than birds that preferentially nest on trees, because predation risk is likely to be higher at ground level (e.g.Wallace 1868; Soler and Moreno 2012). It is also likely that species inhabiting islands should have less color diversity because islands tend to hold smaller populations than the mainland and small populations are less able to respond to changes in conditions, due to its smaller genetic variation (Kimura and Ohta 1969). Finally, we also expect that overall plumage contrast would increase with sexual dichromatism, because if the intensity of the latter is a good estimator of sexual selection, it would be logical to assume that selection would favor conspicuousness if it helps males attract females. A strong correlation between males and females color span would suggest
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