1 Plumage convergence in tyrant flycatchers: A 2 tetrachromatic view 3 4 A thesis submitted to the Department of Biological Science of the 5 Universidad de los Andes in partial fulfillment of the requirements for the 6 degree of Bachelor of Science in Biology 7 8 9 María Alejandra Meneses-Giorgi 10 Laboratorio de Biología Evolutiva de Vertebrados 11 Departamento de Ciencias Biológicas 12 Universidad de los Andes 13 14 Advisor: 15 Daniel Cadena, PhD 16 Full Professor 17 Departamento de Ciencias Biológicas 18 Universidad de los Andes 19 20 21 ABSTRACT 22 Convergent evolution is the process through which different evolutionary lineages 23 independently evolve similar features. Phenotypic convergence has been linKed 24 with selective pressures including predation and competitive interactions. Social 25 mimicry may lead to convergent evolution when interactions with conspecifics and 26 heterospecifics drive evolution towards similar phenotypes. Several hypotheses 27 accounting for convergence based on mechanisms of social mimicry exist, but 28 evaluations of how similar species are given the visual system of receptors has 29 been ostensibly missing from tests of such hypotheses. We used phylogenetic 30 methods, plumage reflectance measurements of six species of tyrant flycatchers 31 (Passeriformes, Tyrannidae) with strikingly similar plumage patterns, and models 32 of avian vision to evaluate the efficacy of visual deception and therefore the 33 plausibility of hypotheses potentially accounting for plumage convergence involving 34 mimicry. We found plumage similarity resulted from convergence and may have 35 been favored by selective pressures exerted by predation because putative models 36 and mimics species were indistinguishable by visually oriented raptors. We reject 37 social mimicry hypotheses as an explanation for the aparent similarity between one 38 of the putative model species and putative mimics because deception seems 39 unlikely given the visual system of passerines visual system. Nonetheless, 40 plumage convergence may have been favored by competitive interactions with 41 other putative model species or with other smaller species of passerines. 42 Experiments and behavioral observations are necessary to better characterize 43 social interactions among our study species and to test predictions of alternative 44 hypotheses posed to account for mimicry. 45 46 RESUMEN 47 La evolución convergente es el proceso mediante el cual diferentes linajes 48 evolutivos independientemente evolucionan características similares. La evolución 49 convergente ha sido relacionada con presiones de selección como la depredación 50 y las interacciones de competencia. El mimetismo social puede llevar a evolución 51 convergente cuando las interacciones competitivas con individuos coespecíficos y 52 heteroespecíficos impulsan la evolución hacia fenotipos similares. Existen varias 53 hipótesis que dan cuenta de la convergencia dado el mimetismo social, pero 54 estimaciones de qué tanto se parecen las especies involucradas dado el sistema 55 visual de especie receptoras han estado ausentes de los trabajos que evalúan 56 dichas hipótesis. En este estudio usamos métodos filogenéticos, medidas de 57 reflectancia de seis especies de tiránidos (Passeriformes, Tyrannidae) que 58 presentan plumajes similares y modelos visuales de aves para evaluar la eficacia 59 del engaño visual y, por ende, la plausibilidad de hipótesis que plantean que la 60 convergencia en el plumaje ha surgido por mimetismo social. Encontramos que la 61 similitud en el plumaje es producto de convergencia, que pudo ser favorecida por 62 la presión de selección ejercida por los depredadores pues las especies modelo e 63 imitadoras hipotéticas son indistinguibles para aves rapaces que se orientan 64 visualmente. Rechazamos las hipótesis de mimetismo social como una explicación 65 de la aparente similitud entre una de las especies modelo y los imitadores 66 hipotéticos debido a que el engaño es poco probable dado el modelo visual de los 67 Passeriformes. Sin embargo, la convergencia en el plumaje pudo haber sido 68 favorecida por interacciones competitivas con la otra especie modelo putativa o 69 con otras especies passeriformes más pequeñas. Es necesario hacer 70 experimentos y observaciones de comportamiento para caracterizar mejor las 71 interacciones sociales entre nuestras especies de estudio y para probar 72 predicciones de hipótesis alternativas planteadas para explicar el mimetismo. 73 74 Keywords: Convergence, coloration, social mimicry, visual models, interespecific 75 social dominance mimicry. 76 77 INTRODUCTION 78 Convergent evolution, the process through which two or more distinct lineages 79 independently acquire similar traits, reveals that the paths of evolution are not 80 infinite, but may be rather restricted. Convergence may happen rapidly or over the 81 course of millions of years either by random drift or more likely because a given 82 phenotypic trait is repeatedly favored by natural selection in a particular 83 environment (Endler, 1986; Losos et al., 1998). Likewise, convergence may also 84 occur due to biases in the production of phenotypic variation such as shared 85 developmental constraints (Brakefield, 2006; Losos et al., 1998; Price & Pavelka, 86 1996). A well-studied form of convergent evolution is mimicry, in which one species 87 (the mimic) evolves to resemble another species (the model), often to deceive a 88 third species (the receptor; McGhee, 2012). 89 90 There are numerous examples of phenotypic convergence among birds (Cody & 91 Brown, 1970; Davies & Welbergen, 2008; Jønsson et al., 2016; Laiolo, 2017; 92 Leighton et al., 2018; Lopes et al., 2017; Prum, 2014; Stoddard, 2012), and several 93 scientists have proposed hypothesis to explain this phenomenon in the context of 94 mimicry (Barnard, 1979, 1982; Diamond, 1982; Moynihan, 1968; Prum, 2014; 95 Prum & Samuelson, 2012, 2016). Among leading ideas proposed to account for 96 phenotypic convergence in birds, the social mimicry hypothesis (Moynihan, 1968) 97 posits that convergent similarity in traits like coloration and plumage patterns may 98 evolve to promote efficient communication maintaining cohesion both among 99 conspecifics and heterospecifics in mixed-species flocks. A variant of this 100 hypothesis posits that rather than maintaining cohesion of mixed flocks, social 101 mimicry serves mainly as an antipredatory adaptation because predation 102 eliminates conspicuous or atypical individuals from populations, thereby promoting 103 phenotypic uniformity (Barnard, 1979). How atypical an animal is in this context 104 must be examined relative to the background (Gomez & Théry, 2007); if a predator 105 considers a whole mixed-species flock as the background, then any species 106 forming a distinct minority within it may be a preferred prey, resulting in a selective 107 pressure favoring homogeneity (Mueller, 1971). Therefore, the efficacy of social 108 mimicry to reduce predation (Barnard, 1979) depends on the extent to which 109 predators may perceive mixed flocks as homogeneous, which ultimately relies on 110 the acuity of their visual system. 111 112 An alternative explanation for mimicry not focusing on predation but still 113 considering social interactions suggests that mimicry may serve two purposes: (1) 114 mimics may escape attack from model species of larger body size, and (2) mimics 115 may deceive species of smaller size and scare them off without further effort 116 (Diamond, 1982). Along the same lines, Prum & Samuelson (2012) further 117 proposed the Interspecific Social Dominance Mimicry (ISDM) hypothesis, which 118 posits that, given interference competition, smaller species evolve to mimic larger, 119 ecologically dominant competitors, to deceive them and thereby avoid attacks. For 120 this mechanism to be plausible, individuals of the mimic species must be confused 121 by individuals of the model species as if they were conspecific based on pictorial 122 cues like shape, color and plumage patterns regardless of differences in body size 123 (Leighton et al., 2018; Prum, 2014; Prum & Samuelson, 2012, 2016). Therefore, 124 the efficacy of this form of mimicry critically depends on the visual system of model 125 species. 126 127 Explicit consideration of the efficacy of visual deception given avian visual models 128 has been ostensibly missing from analyses, limiting our ability to assess the 129 plausibility of various hypotheses posed to account for mimicry. Birds have visual 130 pigments enabling them to acquire information from red, green and blue 131 wavelengths (like humans), but they are also capable of acquiring information from 132 ultraviolet wavelengths with an additional pigment. Also, each of the avian 133 pigments is paired with a particular pigmented oil droplet type, which results in 134 better spectral discrimination relative to other vertebrates (Cuthill et al., 2000). The 135 ability to distinguish colors varies among birds, however, with a pronounced 136 difference in the absorbance peak of the ultraviolet sensitive (UVS-type) cones 137 present in Passeriformes and Psittaciformes, and the violet sensitive (VS-type) 138 cones present in all other non-passerines including raptors (Håstad et al., 2005). 139 Thus, a crucial question one must answer to gauge support for hypotheses 140 attempting to account for mimicry is whether phenotypic similarities between 141 species perceived by humans are sufficient to deceive birds including predators, 142 competitors,