Integrated visual displays that combine gesture with colour are nearly ubiquitous in the animal world, where they are shaped by sexual selection for their role in courtship and competition. However, few studies assess how multiple selection regimens operate on different components of these complex phenotypes on a macroevolutionary scale.
Here, we study this issue by assessing how both sexual and ecological selection work together to influence visual display complexity in the birds of paradise.
We first find that sexual dichromatism is highest in lekking species, which undergo more intense sexual selection by female choice, than non-lekking species. At the same time, species in which males directly compete with one another at communal display courts have more carotenoid-based ornaments and fewer melanin ornaments.
Meanwhile, display habitat influences gestural complexity. Species that dance in the cluttered understorey have more complex dances than canopy-displaying species.
Taken together, our results illustrate how distinct selection regimens each operate on individual elements comprising a complex display. This supports a modular model of display evolution, wherein the ultimate integrated display is the product of synergy between multiple factors that select for different types of phenotypic complexity.

1 INTRODUCTION

Animal displays are vital to mediating mate choice and competition. As a result, these behaviours are thought to contribute to the process of speciation and thus play a fundamental role in shaping global patterns of biodiversity (Grant & Grant, 2010; Price, 1998). Understanding how displays diverge in response to dynamic selection regimens is therefore a major goal in biology. Work to date indicates that signal design is the product of multiple selection regimens operating in tandem (Endler, 1987; Seddon, 2005). This also applies to complex displays, which consist of multiple signalling elements. Complex displays should evolve in a modular fashion, where each novel signal offers a new opportunity for one or more selection pressures to act (Hebets et al., 2016; Miles, Schuppe, Ligon, & Fuxjager, 2018). However, most work that examines multicomponent displays does so in single-species systems (e.g., Candolin, 1999; Pryke, Andersson, & Lawes, 2001; Smith et al., 2016; Stange, Page, Ryan, & Taylor, 2016), an approach that makes it difficult to understand the macroevolutionary consequences of modularity. There are relatively few studies that take such a broad approach to this topic (but see Seddon, 2005; Tobias et al., 2010), which leaves a gap in our understanding of how multiple drivers act together to shape signal divergence.

Some of the most widespread modular signals are integrated visual displays, which combine physical gestures with colour ornaments to communicate with signal receivers (Stuart-Fox & Ord, 2004). Such displays are nearly ubiquitous in the animal world, used by a wide range of invertebrates (Green & Patek, 2015; Hebets & Uetz, 2000), fishes (Basolo & Alcaraz, 2003; Milinski & Bakker, 1990) and tetrapods alike (Klomp, Stuart-Fox, Cassidy, Ahmad, & Ord, 2017; Miles, Cheng, & Fuxjager, 2017). Each component of an integrated display can convey distinct and isolated information to the receiver (Klomp et al., 2017; Kodric-Brown, 1989; Price, Earnshaw, & Webster, 2006), or otherwise be combined to supersede the effect of each component alone (Girard, Elias, & Kasumovic, 2015; Hebets & Uetz, 1999; Taylor & Ryan, 2013). As such, displays can become more elaborate either by introducing new signals to increase complexity, or by exaggerating existing elements (Hebets, Vink, Sullivan-Beckers, & Rosenthal, 2013; Lindsay, Houck, Giuliano, & Day, 2015). For example, sexual selection for colourful males encompasses a diverse range of evolutionary processes that generate dichromatism in different ways. Among the many possibilities are exaggerating the degree to which different melanins are deposited across the body (Bókony, Liker, Székely, & Kis, 2003; Galván, 2008), and/or increasing colour complexity by evolving novel metabolic pathways to process diet-derived carotenoids into new hues (Badyaev, Hill, & Weckworth, 2002; Goodwin, 1980; Ligon, Simpson, Mason, Hill, & McGraw, 2016). Because these different pigment origins for colour represent developmentally distinct pathways, they have the potential to act as individual components of the modular visual display (Hebets et al., 2016). Similarly, gestural signals might also undergo elaboration independent of colour ornaments because they are ontogenically distinct. If integrated visual displays are indeed modular, then each component should be independently shaped by a distinct selection regimen. Alternatively, signal components may evolve in a correlated manner, either by reinforcing or by constraining one another independent of selection for display complexity (Mason, Shultz, & Burns, 2014; Rowe, 1999).

Visual displays are primarily shaped by sexual selection, both via female choice and male–male competition. The former mechanism (intersexual selection) is the result of indirect competition among males for the opportunity to mate with choosy females, which results in the evolution of progressively elaborate displays (Andersson, 1994). Although most species undergo intersexual selection to some degree, the effects of female choice are at their most extreme in lekking species, which have an asymmetrical social mating system where a minority of males ever get to mate (Borgia, 1979; Payne, 1984; Widemo & Owensi, 1995). The underlying mechanisms of female choice have been a subject of debate for decades—be it for handicaps (Zahavi, 1975), motor skill and vigour (Byers, Hebets, & Podos, 2010), or material benefits (Alatalo, Lundberg, & Glynn, 1986; Gray, 1997)—but mechanism aside, a common consequence of female choice is increased display complexity (Hebets et al., 2013; Lindsay et al., 2015). At the same time, many species undergo differing degrees of sexual selection by direct male–male competition (intrasexual selection), wherein interactions among males determine access to territories and mating rights (Andersson, Pryke, Ornborg, Lawes, & Andersson, 2002; Ord, Blumstein, & Evans, 2001). Even among lekking species, the intensity of intrasexual selection is variable, occupying a continuum that spans all-out combat between males (Gosling, Petrie, & Rainy, 1987) to species where males at dispersed leks only occasionally interact (Ryder, Parker, Blake, & Loiselle, 2009). This means that some species evolve complex visual displays that are used both in courtship and in competition with other males. How do these complementary mechanisms of sexual selection, by female choice and male–male competition, interact to shape complex displays? One possibility is that inter- and intrasexual selection favour the exaggeration of different phenotypes and therefore act on different signal components. Alternatively, the same signals may evolve to serve both functions, which means that display complexity would reflect the strength of sexual selection (by both mechanisms) that a species undergoes.

Sexual selection, however, does not operate in unchecked isolation to drive display elaboration, as many constraints can impede this process (Wilkins, Seddon, & Safran, 2013). One common constraint is the signalling environment: to be evolutionarily stable, a signal must be reliably transmitted through the environment to convey information to the receiver (Endler, 1992). In this way, signal design is also subject to change based on how effectively it can be transmitted and perceived by the receiver, a phenomenon that has been explored extensively in studies of acoustic signalling (Seddon, 2005; Tobias et al., 2010). Signalling environment and habitat structure affect short-range visual displays as well, because increasing environmental “noise” such as light availability or visual range disruption, prompts the evolution of more detectable displays (Ord, Peters, Clucas, & Stamps, 2007) and/or more sensitive receivers (Bloch, Morrow, Chang, & Price, 2015). Habitats associated with increased visual clutter include the forest understorey, where dense herbaceous vegetation decreases visibility and light availability (Endler, 1987; Endler & Thery, 1996). Indeed, species with a preference for this habitat have evolved remarkable colour ornaments (Marchetti, 1993) and even strategically orient iridescent patches to maximize light transmittance (Schultz & Fincke, 2009). In a modular display framework, it should be possible for signal components to be differentially influenced by the signalling environment in combination with sexual selection.

In this study, we explore how multiple evolutionary pressures interact to shape complex visual display phenotypes in the birds of paradise (Passeriformes: Paradisaeidae; Figure 1). These “most beautiful and most wonderful of living things” (Wallace, 1869) represent the pinnacle of visual display evolution, exhibiting some of the gaudiest colour and most complex dances in the animal world. However, this family is not monolithic in its visual display complexity or social structures; although birds of paradise are known for their polygyny and elaborate displays, many species are monogamous and employ more modest visual signals or do not display at all (Frith & Beehler, 1998). Thus, the range of social mating systems in this family provides an excellent opportunity to investigate how female choice influences visual display evolution. Similarly, even lekking species in the family exhibit uncommon social diversity. For example, many bird of paradise leks are highly dispersed and males seldom interact with one another in a courtship context (Frith & Beehler, 1998; Irestedt, Jønsson, Fjeldså, Christidis, & Ericson, 2009). At the other extreme, the males of other species congregate daily and display at one another even when a female is not present. Moreover, this family is endemic to the humid forests of Wallacea, where it has remained since diverging from a crow-like ancestor approximately 10 million years ago (Jønsson et al., 2016). This eliminates many of the confounding environmental and biogeographic factors that can complicate our understanding of how displays diverge (Miles et al., 2017; Tobias et al., 2010), and makes understanding the effect of display environment more straightforward—even though each species inhabits a similar habitat, they display in different forest strata. All this, combined with an evolutionary context shaped by isolated island radiation, makes the birds of paradise the ideal study system for tackling the challenge of evolutionary synergy driving display diversity.

Here we investigate how multiple drivers each shape the complexity of integrated visual displays that comprise both colour and gesture. If bird of paradise displays are indeed modular (i.e., multiple evolutionary forces independently favour complexity of different signal components), then indices of different selection pressures should each predict directional variation in separate signals. Specifically, we hypothesize that sexual selection by female choice and male–male competition, as well as the signalling environment, will each predict the complexity of different display elements. As such, we first explore how proxies that reflect relative degrees of female choice and male–male competition predict species-wide variation in both gesture and colour. Finally, we examine how display microhabitat influences signal design. By comparing how fundamental agents of evolution act on different signals, we aim to establish a novel framework for understanding how synergistic selection regimens facilitate the emergence of complex modular displays.

2 MATERIALS AND METHODS

2.1 Experimental and statistical approach

We adopted a hypothesis-driven approach to examine three indices of visual display complexity: sexual dichromatism, carotenoid and melanin ornamentation, and gestural display complexity. In-depth descriptions of the methodology for each hypothesis follow in their respective sections, while here we describe the overall study design. To test how multiple proxies for selection pressure predict variation in our variables, we used phylogenetic comparative methods (Felsenstein, 1985) that account for non-independence of comparative datasets. Therefore, all analyses incorporate a published phylogeny that reflects our most up-to-date understanding of the avian radiation that includes birds of paradise (Figure 1; Jønsson et al., 2016). For each of our dependent variables, we first fit continuous trait models (Table S1) using the “fitContinuous” function in the r package geiger (Harmon, Weir, Brock, Glor, & Challenger, 2008) to determine appropriate branch length transformations to use in each analysis. All of our models use categorical predictors (indices of sexual selection intensity and display habitat) and a continuous response variable (complexity scores), so we used phylogenetic ANOVAs (Garland, Dickerman, Janis, & Jones, 1993) to test for associations between the two. Finally, we only report significant p-values that have been corrected to account for multiple testing (Holm, 1988).

Details are in the caption following the image — **Figure 1**
Open in figure viewer PowerPoint

Phylogeny of the birds of paradise from Jønsson et al. (2016), with gestural display complexity (outer ring) and dichromatism (inner ring) scores illustrated on a colour ramp. Blanks indicate species for which there was insufficient information to characterize display complexity. Illustrations depict males performing their complex integrated visual displays, with species selected that best represent the breadth of colour and display complexity found in the family [Colour figure can be viewed at wileyonlinelibrary.com]

2.2 Independent variables

In each of our models, we use categorical independent variables that reflect variation in the degree to which a species undergoes intersexual and intrasexual selection, as well as display habitat. This information was derived using authoritative species accounts documenting bird of paradise natural history (Frith & Beehler, 1998). We first aimed to explore how variation in intersexual selection pressure predicted differences in display complexity. To do this, we used a dichotomous classification of social mating system that distinguishes only between lekking and non-lekking species. We defined lekking species as those in which males mate with many females, and neither provide parental care nor maintain an all-purpose breeding territory (instead they maintain separate arenas for courtship displays, which can consist of either communal or dispersed courts; e.g., Borgia, 1979; Payne, 1984; Kirkpatrick, 1987; McDonald & Potts, 1994). This allowed us to approximately separate species undergoing moderate and extreme intersexual selection, as female choice drives lek evolution (Borgia, 1979; Payne, 1984; Widemo & Owensi, 1995).

We next aimed to examine how degrees of sexual selection by direct male–male competition predict differences in display complexity. Males that display in view of one another must compete directly for display space and time (and thus mating opportunities), and this competition is mediated by not only male–male display behaviour, but also even combat (Reynolds et al., 2009; Robel & Ballard, 1974; Widemo & Owensi, 1995). By contrast, male birds of paradise that display on a solitary court largely do not interact agonistically with other males on a regular basis (Frith & Beehler, 1998). Accordingly, we considered species in which males display close to one another (i.e. within visual range) to be undergoing more intense intrasexual selection, compared to species in which males only display alone. Note that no birds of paradise display cooperatively, which is an alternate social system in which female mate choice is contingent on coordinated displays between multiple males (McDonald & Potts, 1994). We therefore dichotomously categorized species as either displaying with other males, or exclusively alone. Notably, our two indices of sexual selection exhibit little overlap; of the 36 birds of paradise, 26 species have a lek mating system. Of those lekking species, 14 have dispersed leks where males display alone and 12 have communal display courts where 2–20 males display together. All non-lekking species except for one (Manucodia comrii) have solitary-displaying males.

Finally, we investigated how display habitat affects display complexity. Habitat structure can impose different challenges to signal transmission and perception by the receiver, particularly between open (low clutter) and closed (high clutter) habitats (Endler, 1992; Ord & Stamps, 2008; Tobias et al., 2010). All birds of paradise inhabit the closed humid tropical forest. However, species preferences for display courts are more variable, ranging from the dense understorey to canopy, where tree gaps are more common (Endler & Thery, 1996; Frith & Beehler, 1998). We classified species by the forest strata in which they display using a discrete index, because accounts of display habitat are supplied in metres for some species and qualitative terms (e.g., “high in the canopy,” “on the ground”) for others. This allowed for easy delineation of species described qualitatively, and we followed a previously published forest stratum classification for New Guinea birds to determine display habitat for quantitatively described species (Bell, 1982). Briefly, this system considers species ≤3 m from the forest floor to inhabit the understorey, ≥10 m from the forest floor to be in the canopy, and considers species between 3 and 10 m to be in the midstorey. However, due to the low number of midstorey-displaying species (n = 6) and the marked difference in vegetation structure between the understorey and all higher forest strata (Bell, 1982; Montgomery & Chazdon, 2001; Wright, 2002), we grouped midstorey and canopy species into a single “upper strata” category to compare to understorey counterparts. This dichotomous habitat classification still has biological relevance, as those species displaying in the mid- and upper stories seek out exposed perches at the forest edge or at a tree's crown, while species displaying in the understorey maintain display courts on or near the ground and among dense herbaceous vegetation (Frith & Beehler, 1998).

2.3 Gesture complexity scores

To characterize gestural complexity of each species, we followed a literature-based numerical scoring index that has been used previously (Fuxjager et al., 2015; Lindsay et al., 2015; Miles et al., 2017). This index uses published display descriptions to distinguish between unique motor components of a display. For example, many species perform a wing display, but some pump the whole wing with the pectoralis and supracoracoideus muscles, whereas others extend only the wrist using carpal extensors and flexors; and yet others still will incorporate both gestures into their display. Therefore, we consider these two wing displays to be unique gestures.

We define display complexity as the sum of discrete physical outputs incorporated into a species’ gestural display repertoire (as in Fuxjager et al., 2015; Lindsay et al., 2015; Miles et al., 2017). In this way, display complexity scores are computed by awarding a species 1 point for every unique physical manoeuvre it performs as part of the total dance routine. By adhering to a priori delineations of each gesture (Table S1), we were able to avoid double-counting manoeuvres. We used published species accounts of display repertoires (Frith & Beehler, 1998) augmented with information from later expeditions (del Hoyo, Elliott, & Sargatal, 1999; Laman & Scholes, 2012) to describe and categorize individual gestures for each taxa. Tallying presence (1 point) or absence (0 points) of each gesture in a species, and then adding the total score, results in the species gestural complexity score (Table S2). As such, a total score of 0 denotes a species that performs no gestural displays whatsoever, and higher scores denote species with more complex display repertoires. Because this study's focus concerns display complexity and not elaboration, we do not account for qualitative differences in gesture performance across species (thus, two species that perform the bow gesture each receive a score of 1, regardless of the depth and speed of the motion). To eliminate bias, an individual blind to our hypotheses computed all display complexity scores. Because complexity scoring is based on human interpretation of the literature, a second individual (similarly blind to the study motives) independently recomputed complexity scores to ensure that our methodology was repeatable. Indeed, we had a strong correlation between the two sets of scores (R² = .987, p < .0001).

2.4 Quantifying coloration

We quantified sexual dichromatism using a published score-based index based on human observation (Gray, 1996; Ornelas, González, & Espinosa de los Monteros, 2009). We chose to use this index over measures of plumage brightness (e.g., quantifying position in tetrahedral colour space; Stoddard & Prum, 2008), because our index more closely characterizes complexity, or the number of novel components added to the display (Hebets et al., 2013; Miles et al., 2017). Although humans and birds do not perceive the same range of colours, previous work shows that human vision is a valid and effective proxy for quantifying avian coloration and making robust evolutionary inferences (Seddon, Tobias, Eaton, Ödeen, & Byers, 2010).

As such, we adapted methodology from Ornelas et al. (2009) to compute dichromatism across species. Briefly, using highly accurate handbook plates as a reference (del Hoyo et al., 1999), we divided each bird into 15 distinct plumage regions (Figure S1) and had an individual blind to our study aims compare males and females of each species. Then, each male plumage region was scored based on its similarity or difference from the female—similar regions received a score of 0; regions in which a colour was qualitatively different but shared a fundamental pigment or structural basis received a score of 1; and regions that introduced a new mode of coloration received a score of 2. Again following Ornelas et al. (2009), we classified colour mode using a conservative system where we considered blacks, browns and tans, as well as dilute yellows (“buff”) and red-browns (“rufous”) to be melanin-based, which is consistent with our understanding of avian coloration generated from both eumelanins and phaeomelanins (Hill & McGraw, 2006). Saturated yellows, oranges and reds we considered to be carotenoid-based (Cardoso & Mota, 2008; Ligon et al., 2016). Structural coloration can exist on plumage with either pigment, generating colour in the violet-blue-teal range on melanin pigment and green when combined with carotenoids (Maia, Rubenstein, & Shawkey, 2016), so we considered colours in the violet-green range to be structural (Figure S1). The result of this indexing method is a score for each species (Table S2) that can potentially range from 0 (sexually monomorphic) to 30 (every plumage region changes colour mechanism). As above, all colour data were gathered by an individual blind to the study objectives. To validate repeatability of the dichromatism index, a second individual (again blind to our hypotheses) independently corroborated the scoring process. Both scores were highly correlated (R² = .983, p < .0001).

We further probed visual signal diversity by examining pigment origins of male coloration. To do this, we followed the scheme outline above to determine whether each male plumage patch either (1) incorporated carotenoid coloration, or (2) only expressed melanin pigment (only one species, Cicinnurus regius, has unpigmented plumage regions). We then calculated the proportion of carotenoid patches relative to the total number of plumage regions $urn:x-wiley:00218790:media:jane12824:jane12824-math-0001$ . This results in a proportion between 0 and 1, where species that score near 1 use carotenoid-based colours on a greater number of plumage patches compared to the majority melanin species that score closer to 0. Carotenoid proportion therefore is inversely related to the extent of colour generated by melanin (melanin proportion = 1 – carotenoid proportion) in all species except Cicinnurus regius. We therefore ran additional analyses using melanin proportion as a dependent variable, but these data are not included in figures due to redundancy. We also did not evaluate structural coloration, because it exists on a subtle continuum from matte feathers (no structural colour), to glossy colours, to new colours introduced altogether (Maia, D'Alba, & Shawkey, 2011). As such, it is nearly impossible to assess structural coloration through the lens of complexity using handbook plates, as our index could not account for subtle innovations in structural modifications.

3 RESULTS

We found there to be high diversity in both gesture complexity and dichromatism scores across the birds of paradise (Figure 1), and there was no correlation between gesture complexity and sexual dichromatism (F_1,34 = 0.1287, R² = .0263, p = .722). When fitting a series of continuous trait models to each variable (Table S3), we found that each one was best fit by Brownian motion (BM) or a modification thereof. Specifically, gestural complexity scores appear to evolve under full BM (AIC_c = 197.35), sexual dichromatism scores are best fit with a lambda transformation (AIC_c = 223.3, λ = 0.856), and kappa processes underlie both carotenoid proportion (AIC_c = −25.28, κ = 0.44) and melanin proportion (AIC_c = −21.11, κ = 0.15). For each of these dependent variables, we therefore supplied trees with the appropriate branch length transformation to statistical models.

We first found that sexual dichromatism changed among species with different social mating systems (Figure 2a), where lekking species had significantly higher dichromatism scores than non-lekking species (F_1,34 = 24.628, p = .033, λ = 0.857). However, there was no difference among lekking and non-lekking species for carotenoid proportion (F_1,34 = 15.53, p = .100, κ = 0.44), melanin proportion (F_1,34 = 18.69, p = .100, κ = 0.15) or gestural complexity score (F_1,34 = 14.671, p = .114).

Next, species in which multiple males display at a single court had significantly more male carotenoid ornaments than those that display alone (Figure 2b; F_1,34 = 17.610, p = .006, κ = 0.44). The reverse was true for melanin patch proportion, as solitary-displaying males had higher melanin proportion scores (F_1,34 = 17.84, p = .008, κ = 0.15). However, there was no such difference for dichromatism (F_1,34 = 2.024, p = .333, λ = 0.857) or gestural display complexity scores (F_1,34 = 1.822, p = .180).

Finally, species that display in the forest understorey had greater gestural complexity scores than those that dance in upper strata (Figure 2c; F_1,34 = 15.471, p = .005). Meanwhile, display stratum does not explain variation in male coloration, either in total colour complexity score (F = 1.59_1,34, p = .526, λ = 0.857) or in the relative amount of carotenoid patches (F_1,34 = 0.79, p = .526, κ = 0.44) or melanin patches (F_1,34 = 0.79, p = .526, κ = 0.15).

4 DISCUSSION

By breaking down complex visual displays into their constituent parts, we dissect the diverse evolutionary pressures that shape the complexity of the display’s individual components. We first show that lekking species (which undergo extreme levels of intersexual selection) are more sexually dichromatic than non-lekking species, without respect to the pigment origin of male coloration. In other words, species undergoing a stronger level of sexual selection by female choice are more dichromatic, compared to species subject to a more moderate degree of intersexual selection. Meanwhile, species in which multiple males display together have more red and yellow ornaments (and less apparent melanin coloration) than those that display alone. Because males that display together engage in direct competition for display space and dispersed males do not, this means that aggregate displayers should be experiencing a stronger degree of intrasexual selection. Therefore, our data suggest that shifting intrasexual selection pressure is associated with changes in carotenoid ornamentation. Finally, we find an association between display habitat and gestural display complexity, where species that signal in the forest understorey have more complex dances than those that signal in the canopy and midstorey. This implies that habitat does indeed influence gestural display complexity. Altogether, these findings point to three distinct evolutionary drivers operating in tandem to guide divergence in three different components of an integrated visual display phenotype (Figure 3). Bird of paradise displays therefore exhibit modularity (Hebets et al., 2016), because individual signal components are modified independently despite their function to the integrated visual display. This implies that the total complexity of integrated displays is the result of multiple evolutionary forces acting synergistically, or in tandem, rather than any one operating in isolation.

One of the most interesting insights from our data is that the bright plumage of male birds of paradise evolved in response to sexual selection by both female choice and male–male competition operating on different colours. Indeed, we find that overall dichromatism is associated with increasing intersexual selection pressure, while aggregate display dynamics predict a shift from melanin- to carotenoid-based coloration. Why would two indices of sexual selection predict different types of colour ornament shifts? One answer may lie in dichromatic “innovations”, as males with a rare colour pattern can experience elevated mating success (Hughes, Houde, Price, & Rodd, 2013). A similar mechanism could be responsible here, as lekking species are more sexually dichromatic (i.e., the males have more putative novel colours) than non-lekking species. In other words, the species for which female choice is at its most extreme are also those species where males have evolved more plumage ornaments relative to females. Alternatively, female choice may still operate on specific colours in birds of paradise, but this might vary in direction among species. This idea is supported by the fact that plumage can be highly labile (Omland & Lanyon, 2000), and sexual traits persist due to parallel changes in both the male signalling phenotype and female preference for that signal (Servedio, 2016). Indeed, effective colour signals used in mate choice are found in melanin (Siefferman & Hill, 2003), carotenoid (Friedman, McGraw, & Omland, 2014) and structural colours alike (Keyser, 2000).

Meanwhile, birds of paradise undergoing intense direct male–male competition tend to have more carotenoid-based ornaments and fewer melanin patches. This suggests that red and yellow ornaments may function in direct male–male competition, possibly because carotenoid-based ornaments act as an evolutionarily stable mediator of male–male interactions due to their tendency to serve as an honest signal (Ligon et al., 2016; Pryke & Andersson, 2003). In passerines like birds of paradise, these colours are exclusively generated by diet-derived carotenoid pigments (Goodwin, 1980). This means that generating red and yellow ornaments relies not only on an individual's ability to acquire food, but also on converting dietary forms into usable pigments along numerous metabolic pathways (Cardoso & Mota, 2008; Ligon et al., 2016). As a result, carotenoid colours sometimes function as condition-dependent badges used to negotiate male–male competition (Peek, 1972; Pryke & Andersson, 2003). This may also not be the case, however, as carotenoid coloration is not the only route to a condition-dependent ornament. For example, both melanin and structural coloration can also be honest signals due to condition dependence (Roulin, 2016; Siefferman & Hill, 2003), so we cannot rule out the possibility that these alternate modes may also play some role.

Birds of paradise are perhaps best known for their bizarre courtship dances, but our indices of sexual selection do not predict any variation in gestural display complexity scores. This does not mean that gesture is unimportant to mate choice in birds of paradise, of course; for these species, gesture appears to be a foundational element of mate choice, with females closely observing and even probing displaying males before deciding to copulate or visit another display court (Frith & Beehler, 1998; Laman & Scholes, 2012; Scholes, 2008). One explanation for our data is that female birds of paradise likely evaluate gesture on some other qualitative basis, perhaps of motor skill or vigour (Byers et al., 2010), which may influence phenotypic patterning of individual gesture exaggeration and/or coordination instead of complexity. Studies in other avian taxa support this point of view, showing that fraction-of-a-second differences in gestural performance indeed influence female mate choice (Barske, Schlinger, Wikelski, & Fusani, 2011; Manica, Macedo, Graves, & Podos, 2016; Schuppe & Fuxjager, 2018).

We also find that gestural complexity is best explained by display habitat, where males displaying in the forest understorey perform more complex dance routines than those that display in the upper strata. This phenomenon is likely rooted in the complex interactions between signal production, transmission and perception by the receiver, as sexual selection can only act on signals that can be reliably propagated through the environment (Endler, 1992). Although few studies investigate the effect of signalling environment on gesture, previous work shows that anoles similarly overcome visual “noise” in a wind-disturbed habitat by introducing new gestures to their display (Ord et al., 2007). In this case, a broad range of environmental factors may inhibit signal perception. Among dense (understorey) or open (upper strata) display microhabitats, potential sources of ecological pressure for increased complexity may include physical breakup of the scene by foliage (Endler, 1993; Théry, 2001), restricted light availability (White, Zeil, & Kemp, 2015) and/or visual distance from the signaller (Fleishman, 1992). Alternatively, the difference in gestural complexity across display habitats may be a product of physiological and/or morphological constraints associated with dancing on different perching substrates; while most understorey species display on the ground or on vertical perches, canopy-displaying species exclusively use larger perches. How does evolution proceed in the face of these environmental challenges? Using more gestures is only one potential solution to signalling in a challenging environment; alternative routes include enhancing highly directional iridescent ornaments (White et al., 2015), or even modifying the signalling environment itself to maximize light transmission to the display court (Uy & Endler, 2004). Indeed, both of these traits are common in birds of paradise, although they are shared by understorey and canopy displayers alike (Frith & Beehler, 1998).

Importantly, bird of paradise displays are multimodal as well as complex, incorporating many non-visual cues that could also function as redundant messages (Rowe, 1999). For example, most species call extensively before dancing, often using a different perch specifically for vocalizing. Some birds of paradise incorporate tactile and even olfactory signalling into their displays as well, which further expands the opportunities for sexual selection to elaborate the signal (Frith & Beehler, 1998). Therefore, the integrated visual display itself is yet another component embedded in a larger multimodal courtship display, which may evolve in surprising ways. For example, colour and gesture complexity appear to evolve independently (rather than by transfer from one signal to another Mason et al., 2014). However, visual display complexity may still interact differently with other multimodal signals.

5 CONCLUSIONS

Altogether, these results offer novel insight into the macroevolutionary pattern of visual display design: different signal components can be simultaneously and independently influenced by multiple core evolutionary processes, which interact to produce the ultimate integrated visual display. This highlights the remarkable potential of diverse selection regimens, often viewed as discrete operators, to instead function independently on a single signal component, while still interacting with other processes to shape overall complexity. The result is an integrated display that conveys more information than the sum of its constituent signals—and, in the case of extraordinary bird of paradise visual displays, exemplifies the diversifying potential of animal behaviour.

ACKNOWLEDGEMENTS

The work was funded by NSF grant IOS-1655730 to M.J.F. The authors have no conflicts of interest to declare.

AUTHORs’ CONTRIBUTIONS

M.C.M. and M.J.F. conceived of and designed the study, analysed the data and wrote the manuscript. Both authors gave final approval of the study for publication.

DATA ACCESSIBILITY

Data from this study are available online at the Dryad Digital Repository: https://doi.org/10.5061/dryad.9m47pj0 (Miles & Fuxjager, 2018).

Supporting Information

REFERENCES

Alatalo, R. V., Lundberg, A., & Glynn, C. (1986). Female pied flycatchers choose territory quality and not male characteristics. Nature, 323, 152–153. https://doi.org/10.1038/323152a0
10.1038/323152a0
Web of Science®Google Scholar
Andersson, M. B. (1994). Sexual selection. Princeton, NJ: Princeton University Press.
10.1515/9780691207278
CASGoogle Scholar
Andersson, S., Pryke, S. R., Ornborg, J., Lawes, M. J., & Andersson, M. (2002). Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird. The American Naturalist, 160, 683–691.
10.1086/342817
PubMedWeb of Science®Google Scholar
Badyaev, A. V., Hill, G. E., & Weckworth, B. V. (2002). Species divergence in sexually selected traits: Increase in song elaboration is related to decrease in plumage ornamentation in finches. Evolution, 56, 412–419. https://doi.org/10.1111/j.0014-3820.2002.tb01350.x
10.1111/j.0014-3820.2002.tb01350.x
PubMedWeb of Science®Google Scholar
Barske, J., Schlinger, B. A., Wikelski, M., & Fusani, L. (2011). Female choice for male motor skills. Proceedings of the Royal Society B: Biological Sciences, 278, 3523–3528. https://doi.org/10.1098/rspb.2011.0382
10.1098/rspb.2011.0382
PubMedWeb of Science®Google Scholar
Basolo, A. L., & Alcaraz, G. (2003). The turn of the sword: Length increases male swimming costs in swordtails. Proceedings of the Royal Society B: Biological Sciences, 270, 1631–1636. https://doi.org/10.1098/rspb.2003.2388
10.1098/rspb.2003.2388
PubMedWeb of Science®Google Scholar
Bell, H. (1982). A bird community of lowland rainforest in New Guinea. I. Composition and density of the avifauna. Emu, 82, 24. https://doi.org/10.1071/MU9820024
10.1071/MU9820024
Web of Science®Google Scholar
Bloch, N. I., Morrow, J. M., Chang, B. S. W., & Price, T. D. (2015). SWS2 visual pigment evolution as a test of historically contingent patterns of plumage color evolution in warblers. Evolution, 69, 341–356. https://doi.org/10.1111/evo.12572
10.1111/evo.12572
PubMedWeb of Science®Google Scholar
Bókony, V., Liker, A., Székely, T., & Kis, J. (2003). Melanin-based plumage coloration and flight displays in plovers and allies. Proceedings of the Royal Society of London B: Biological Sciences, 270, 2491–2497. https://doi.org/10.1098/rspb.2003.2506
10.1098/rspb.2003.2506
PubMedWeb of Science®Google Scholar
Borgia, G. (1979). Sexual selection and the evolution of mating systems. In M. S. Blum, & N. A. Blum (Eds.), Sexual selection and reproductive competition in insects (pp. 19–80). New York, NY: Academic Press.
10.1016/B978-0-12-108750-0.50008-2
Google Scholar
Byers, J., Hebets, E., & Podos, J. (2010). Female mate choice based upon male motor performance. Animal Behaviour, 79, 771–778. https://doi.org/10.1016/j.anbehav.2010.01.009
10.1016/j.anbehav.2010.01.009
Web of Science®Google Scholar
Candolin, U. (1999). Male-male competition facilitates female choice in sticklebacks. Proceedings of the Royal Society B: Biological Sciences, 266, 785–789. https://doi.org/10.1098/rspb.1999.0706
10.1098/rspb.1999.0706
Web of Science®Google Scholar
Cardoso, G. C., & Mota, P. G. (2008). Speciational evolution of coloration in the genus Carduelis. Evolution, 62, 753–762. https://doi.org/10.1111/j.1558-5646.2008.00337.x
10.1111/j.1558-5646.2008.00337.x
PubMedWeb of Science®Google Scholar
del Hoyo, J., Elliott, A., & Sargatal, J. (1999). Handbook of the birds of the world, vol. 5. Barcelona, Spain: Lynx Edicions.

Google Scholar
Endler, J. A. (1987). Predation, light intensity and courtship behaviour in Poecilia reticulata (Pisces: Poeciliidae). Animal Behaviour, 35, 1376–1385. https://doi.org/10.1016/S0003-3472(87)80010-6
10.1016/S0003-3472(87)80010-6
Web of Science®Google Scholar
Endler, J. A. (1992). Signals, signal conditions, and the direction of evolution. The American Naturalist, 139, S125–S153. https://doi.org/10.1086/285308
10.1086/285308
Web of Science®Google Scholar
Endler, J. A. (1993). The color of light in forests and its implications. Ecological Monographs, 63, 1–27. https://doi.org/10.2307/2937121
10.2307/2937121
Web of Science®Google Scholar
Endler, J. A., & Thery, M. (1996). Interacting effects of lek placement, display behavior, ambient light, and color patterns in three neotropical forest-dwelling birds. The American Naturalist, 148, 421–452. https://doi.org/10.1086/285934
10.1086/285934
Web of Science®Google Scholar
Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125, 1–15. https://doi.org/10.1086/284325
10.1086/284325
Web of Science®Google Scholar
Fleishman, L. J. (1992). The influence of the sensory system and the environment on motion patterns in the visual displays of anoline lizards and other vertebrates. The American Naturalist, 139, S36. https://doi.org/10.1086/285304
10.1086/285304
Web of Science®Google Scholar
Friedman, N. R., McGraw, K. J., & Omland, K. E. (2014). Evolution of carotenoid pigmentation in caciques and meadowlarks (Icteridae): Repeated gains of red plumage coloration by carotenoid C4-oxygenation. Evolution, 68, 791–801. https://doi.org/10.1111/evo.12304
10.1111/evo.12304
CASPubMedWeb of Science®Google Scholar
Frith, C. B., & Beehler, B. M. (1998). The birds of paradise. Oxford, UK: Oxford University Press.

Google Scholar
Fuxjager, M. J., Eaton, J., Lindsay, W. R., Salwiczek, L. H., Rensel, M. A., Barske, J., … Schlinger, B. A. (2015). Evolutionary patterns of adaptive acrobatics and physical performance predict expression profiles of androgen receptor – but not oestrogen receptor – in the forelimb musculature (ed W Hopkins). Functional Ecology, 29, 1197–1208. https://doi.org/10.1111/1365-2435.12438
10.1111/1365-2435.12438
PubMedWeb of Science®Google Scholar
Galván, I. (2008). The importance of white on black: Unmelanized plumage proportion predicts display complexity in birds. Behavioral Ecology and Sociobiology, 63, 303–311. https://doi.org/10.1007/s00265-008-0662-9
10.1007/s00265-008-0662-9
Web of Science®Google Scholar
Garland, T., Dickerman, A. W., Janis, C. M., & Jones, J. A. (1993). Phylogenetic analysis of covariance by computer simulation. Systematic Biology, 42, 265–292. https://doi.org/10.1093/sysbio/42.3.265
10.1093/sysbio/42.3.265
Web of Science®Google Scholar
Girard, M. B., Elias, D. O., & Kasumovic, M. M. (2015). Female preference for multi-modal courtship: Multiple signals are important for male mating success in peacock spiders. Proceedings of the Royal Society B: Biological Sciences, 282, 20152222. https://doi.org/10.1098/rspb.2015.2222
10.1098/rspb.2015.2222
CASPubMedWeb of Science®Google Scholar
Goodwin, T. W. (1980). The biochemistry of the carotenoids. Dordrecht, the Netherlands: Springer. https://doi.org/10.1007/978-94-009-5860-9
10.1007/978-94-009-5860-9
Google Scholar
Gosling, L. M., Petrie, M., & Rainy, M. E. (1987). Lekking in topi: A high cost, specialist strategy. Animal Behaviour, 35, 616–618. https://doi.org/10.1016/S0003-3472(87)80296-8
10.1016/S0003-3472(87)80296-8
Web of Science®Google Scholar
Grant, B. R., & Grant, P. R. (2010). Songs of Darwin's finches diverge when a new species enters the community. Proceedings of the National Academy of Sciences of the United States of America, 107, 20156–20163. https://doi.org/10.1073/pnas.1015115107
10.1073/pnas.1015115107
CASPubMedWeb of Science®Google Scholar
Gray, D. A. (1996). Carotenoids and sexual dichromatism in North American passerine birds. The American Naturalist, 148, 453–480. https://doi.org/10.1086/285935
10.1086/285935
Web of Science®Google Scholar
Gray, E. M. (1997). Female red-winged blackbirds accrue material benefits from copulating with extra-pair males. Animal Behavior, 53, 625–639. https://doi.org/10.1006/anbe.1996.0336
10.1006/anbe.1996.0336
Web of Science®Google Scholar
Green, P. A., & Patek, S. N. (2015). Contests with deadly weapons: Telson sparring in mantis shrimp (Stomatopoda). Biology Letters, 11, 20150558. https://doi.org/10.1098/rsbl.2015.0558
10.1098/rsbl.2015.0558
CASPubMedWeb of Science®Google Scholar
Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E., & Challenger, W. (2008). GEIGER: Investigating evolutionary radiations. Bioinformatics, 24, 129–131. https://doi.org/10.1093/bioinformatics/btm538
10.1093/bioinformatics/btm538
CASPubMedWeb of Science®Google Scholar
Hebets, E. A., Barron, A. B., Balakrishnan, C. N., Hauber, M. E., Mason, P. H., & Hoke, K. L. (2016). A systems approach to animal communication. Proceedings of the Royal Society B: Biological Sciences, 283, 20152889. https://doi.org/10.1098/rspb.2015.2889
10.1098/rspb.2015.2889
PubMedWeb of Science®Google Scholar
Hebets, E. A., & Uetz, G. W. (1999). Female responses to isolated signals from multimodal male courtship displays in the wolf spider genus Schizocosa (Araneae: Lycosidae). Animal Behaviour, 57, 865–872. https://doi.org/10.1006/anbe.1998.1048
10.1006/anbe.1998.1048
CASPubMedWeb of Science®Google Scholar
Hebets, E. A., & Uetz, G. W. (2000). Leg ornamentation and the efficacy of courtship display in four species of wolf spider (Araneae: Lycosidae). Behavioral Ecology and Sociobiology, 47, 280–286. https://doi.org/10.1007/s002650050667
10.1007/s002650050667
Web of Science®Google Scholar
Hebets, E. A., Vink, C. J., Sullivan-Beckers, L., & Rosenthal, M. F. (2013). The dominance of seismic signaling and selection for signal complexity in Schizocosa multimodal courtship displays. Behavioral Ecology and Sociobiology, 67, 1483–1498. https://doi.org/10.1007/s00265-013-1519-4
10.1007/s00265-013-1519-4
Web of Science®Google Scholar
Hill, G. E., & McGraw, K. J. (2006). Bird coloration: Mechanisms and measurements. Cambridge, MA: Harvard University Press.
10.4159/9780674273818
Google Scholar
Holm, S. (1988). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65–70.

Google Scholar
Hughes, K. A., Houde, A. E., Price, A. C., & Rodd, F. H. (2013). Mating advantage for rare males in wild guppy populations. Nature, 503, 108–110. https://doi.org/10.1038/nature12717
10.1038/nature12717
CASPubMedWeb of Science®Google Scholar
Irestedt, M., Jønsson, K. A., Fjeldså, J., Christidis, L., & Ericson, P. G. (2009). An unexpectedly long history of sexual selection in birds-of-paradise. BMC Evolutionary Biology, 9, 235. https://doi.org/10.1186/1471-2148-9-235
10.1186/1471-2148-9-235
CASPubMedWeb of Science®Google Scholar
Jønsson, K. A., Fabre, P.-H., Kennedy, J. D., Holt, B. G., Borregaard, M. K., Rahbek, C., & Fjeldså, J. (2016). A supermatrix phylogeny of corvoid passerine birds (Aves: Corvides). Molecular Phylogenetics and Evolution, 94, 87–94. https://doi.org/10.1016/j.ympev.2015.08.020
10.1016/j.ympev.2015.08.020
PubMedWeb of Science®Google Scholar
Keyser, A. J. (2000). Structurally based plumage coloration is an honest signal of quality in male blue grosbeaks. Behavioral Ecology, 11, 202–209. https://doi.org/10.1093/beheco/11.2.202
10.1093/beheco/11.2.202
Web of Science®Google Scholar
Kirkpatrick, M. (1987). Sexual selection by female choice in polygynous animals. Annual Review of Evology Systematics, 18, 43–70. https://doi.org/10.1146/annurev.es.18.110187.000355
10.1146/annurev.es.18.110187.000355
Web of Science®Google Scholar
Klomp, D. A., Stuart-Fox, D., Cassidy, E. J., Ahmad, N., & Ord, T. J. (2017). Color pattern facilitates species recognition but not signal detection: A field test using robots. Behavioral Ecology, 218, 1556–1563.

Google Scholar
Kodric-Brown, A. (1989). Dietary carotenoids and male mating success in the guppy: An environmental component to female choice. Behavioral Ecology and Sociobiology, 25, 393–401. https://doi.org/10.1007/BF00300185
10.1007/BF00300185
Web of Science®Google Scholar
Laman, T., & Scholes, E. (2012). Birds of paradise: Revealing the world's most extraordinary birds. Washington, DC: National Geographic Books.

Google Scholar
Ligon, R. A., Simpson, R. K., Mason, N. A., Hill, G. E., & McGraw, K. J. (2016). Evolutionary innovation and diversification of carotenoid-based pigmentation in finches. Evolution, 70, 2839–2852. https://doi.org/10.1111/evo.13093
10.1111/evo.13093
CASPubMedWeb of Science®Google Scholar
Lindsay, W. R., Houck, J. T., Giuliano, C. E., & Day, L. B. (2015). Acrobatic courtship display coevolves with brain size in manakins (Pipridae). Brain, Behavior and Evolution, 85, 29–36. https://doi.org/10.1159/000369244
10.1159/000369244
PubMedWeb of Science®Google Scholar
Maia, R., D'Alba, L., & Shawkey, M. D. (2011). What makes a feather shine? A nanostructural basis for glossy black colours in feathers. Proceedings of the Royal Society B: Biological Sciences, 278, 1973–1980. https://doi.org/10.1098/rspb.2010.1637
10.1098/rspb.2010.1637
PubMedWeb of Science®Google Scholar
Maia, R., Rubenstein, D. R., & Shawkey, M. D. (2016). Selection, constraint, and the evolution of coloration in African starlings. Evolution, 70, 1064–1079. https://doi.org/10.1111/evo.12912
10.1111/evo.12912
PubMedWeb of Science®Google Scholar
Manica, L. T., Macedo, R. H., Graves, J. A., & Podos, J. (2016). Vigor and skill in the acrobatic mating displays of a Neotropical songbird. Behavioral Ecology, 28, 164–173.
10.1093/beheco/arw143
Web of Science®Google Scholar
Marchetti, K. (1993). Dark habitats and bright birds illustrate the role of the environment in species divergence. Nature, 362, 149–152. https://doi.org/10.1038/362149a0
10.1038/362149a0
Web of Science®Google Scholar
Mason, N. A., Shultz, A. J., & Burns, K. J. (2014). Elaborate visual and acoustic signals evolve independently in a large, phenotypically diverse radiation of songbirds. Proceedings of the Royal Society B: Biological Sciences, 281, 20140967. https://doi.org/10.1098/rspb.2014.0967
10.1098/rspb.2014.0967
PubMedWeb of Science®Google Scholar
McDonald, D. B., & Potts, W. K. (1994). Cooperative display and relatedness among males in a lek-mating bird. Science, 266, 1030–1032. https://doi.org/10.1126/science.7973654
10.1126/science.7973654
CASPubMedWeb of Science®Google Scholar
Miles, M. C., Cheng, S., & Fuxjager, M. J. (2017). Biogeography predicts macro-evolutionary patterning of gestural display complexity in a passerine family. Evolution, 71, 1406–1416. https://doi.org/10.1111/evo.13213
10.1111/evo.13213
PubMedWeb of Science®Google Scholar
Miles, M. C., & Fuxjager, F. J. (2018). Data from: Synergistic selection regimens drive the evolution of display complexity in birds of paradise. Dryad Digital Repository, https://doi.org/10.5061/dryad.9m47pj0

Google Scholar
Miles, M. C., Schuppe, E. R., Ligon, R. M., & Fuxjager, M. J. (2018). Macroevolutionary patterning of woodpecker drums reveals how sexual selection elaborates signals under constraint. Proceedings of the Royal Society B, 285, 20172628. https://doi.org/10.1098/rspb.2017.2628
10.1098/rspb.2017.2628
PubMedWeb of Science®Google Scholar
Milinski, M., & Bakker, T. C. M. (1990). Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature, 344, 330–333. https://doi.org/10.1038/344330a0
10.1038/344330a0
Web of Science®Google Scholar
Montgomery, R. A., & Chazdon, R. L. (2001). Forest structure, canopy architecture, and light transmittance in tropical wet forests. Ecology, 82, 2707–2718. https://doi.org/10.1890/0012-9658(2001)082[2707:FSCAAL]2.0.CO;2
10.1890/0012-9658(2001)082[2707:FSCAAL]2.0.CO;2
Web of Science®Google Scholar
Omland, K. E., & Lanyon, S. M. (2000). Reconstructing plumage evolution in orioles (Icterus): Repeated convergence and reversal in patterns. Evolution, 54, 2119–2133. https://doi.org/10.1111/j.0014-3820.2000.tb01254.x
10.1111/j.0014-3820.2000.tb01254.x
CASPubMedWeb of Science®Google Scholar
Ord, T. J., Blumstein, D. T., & Evans, C. S. (2001). Intrasexual selection predicts the evolution of signal complexity in lizards. Proceedings of the Royal Society B: Biological Sciences, 268, 737–744. https://doi.org/10.1098/rspb.2000.1417
10.1098/rspb.2000.1417
CASPubMedWeb of Science®Google Scholar
Ord, T. J., Peters, R. A., Clucas, B., & Stamps, J. A. (2007). Lizards speed up visual displays in noisy motion habitats. Proceedings of the Royal Society B: Biological Sciences, 274, 1057–1062. https://doi.org/10.1098/rspb.2006.0263
10.1098/rspb.2006.0263
PubMedWeb of Science®Google Scholar
Ord, T. J., & Stamps, J. A. (2008). Alert signals enhance animal communication in “noisy” environments. Proceedings of the National Academy of Sciences of the United States of America, 105, 18830–18835. https://doi.org/10.1073/pnas.0807657105
10.1073/pnas.0807657105
CASPubMedWeb of Science®Google Scholar
Ornelas, J. F., González, C., & Espinosa de los Monteros, A. (2009). Uncorrelated evolution between vocal and plumage coloration traits in the trogons: A comparative study. Journal of Evolutionary Biology, 22, 471–484. https://doi.org/10.1111/j.1420-9101.2008.01679.x
10.1111/j.1420-9101.2008.01679.x
CASPubMedWeb of Science®Google Scholar
Payne, R. B. (1984). Sexual selection, lek and arena behavior, and sexual size dimorphism in birds. Ornithological Monographs, 33, iii–52. https://doi.org/10.2307/40166729
10.2307/40166729
Google Scholar
Peek, F. W. (1972). An experimental study of the territorial function of vocal and visual display in the male red-winged blackbird (Agelaius phoeniceus). Animal Behaviour, 20, 112–118. https://doi.org/10.1016/S0003-3472(72)80180-5
10.1016/S0003-3472(72)80180-5
Web of Science®Google Scholar
Price, T. (1998). Sexual selection and natural selection in bird speciation. Philosophical Transactions of the Royal Society B: Biological Sciences, 353, 251–260. https://doi.org/10.1098/rstb.1998.0207
10.1098/rstb.1998.0207
Web of Science®Google Scholar
Price, J. J., Earnshaw, S. M., & Webster, M. S. (2006). Montezuma oropendolas modify a component of song constrained by body size during vocal contests. Animal Behaviour, 71, 799–807. https://doi.org/10.1016/j.anbehav.2005.05.025
10.1016/j.anbehav.2005.05.025
Web of Science®Google Scholar
Pryke, S. R., & Andersson, S. (2003). Carotenoid-based epaulettes reveal male competitive ability: Experiments with resident and floater red-shouldered widowbirds. Animal Behaviour, 66, 217–224. https://doi.org/10.1006/anbe.2003.2193
10.1006/anbe.2003.2193
Web of Science®Google Scholar
Pryke, S. R., Andersson, S., & Lawes, M. J. (2001). Sexual selection of multiple handicaps in the red-collared widowbird: Female choice of tail length but not carotenoid display. Evolution, 55, 1452–1463. https://doi.org/10.1111/j.0014-3820.2001.tb00665.x
10.1111/j.0014-3820.2001.tb00665.x
CASPubMedWeb of Science®Google Scholar
Reynolds, S. M., Christman, M. C., Uy, J. A. C., Patricelli, G. L., Braun, M. J., & Borgia, G. (2009). Lekking satin bowerbird males aggregate with relatives to mitigate aggression. Behavioral Ecology, 20, 410–415. https://doi.org/10.1093/beheco/arn146
10.1093/beheco/arn146
Web of Science®Google Scholar
Robel, R. J., & Ballard, W. B. (1974). Lek social organization and reproductive success in the greater prairie chicken. Integrative and Comparative Biology, 14, 121–128.

Google Scholar
Roulin, A. (2016). Condition-dependence, pleiotropy and the handicap principle of sexual selection in melanin-based colouration. Biological Reviews, 91, 328–348. https://doi.org/10.1111/brv.12171
10.1111/brv.12171
PubMedWeb of Science®Google Scholar
Rowe, C. (1999). Receiver psychology and the evolution of multicomponent signals. Animal Behaviour, 58, 921–931. https://doi.org/10.1006/anbe.1999.1242
10.1006/anbe.1999.1242
CASPubMedWeb of Science®Google Scholar
Ryder, T. B., Parker, P. G., Blake, J. G., & Loiselle, B. A. (2009). It takes two to tango: Reproductive skew and social correlates of male mating success in a lek-breeding bird. Proceedings of the Royal Society B: Biological Sciences, 276, 2377–2384. https://doi.org/10.1098/rspb.2009.0208
10.1098/rspb.2009.0208
PubMedWeb of Science®Google Scholar
Scholes, E. (2008). Evolution of the courtship phenotype in the bird of paradise genus Parotia (Aves: Paradisaeidae): Homology, phylogeny, and modularity. Biological Journal of the Linnean Society, 94, 491–504. https://doi.org/10.1111/j.1095-8312.2008.01012.x
10.1111/j.1095-8312.2008.01012.x
Web of Science®Google Scholar
Schultz, T. D., & Fincke, O. M. (2009). Structural colours create a flashing cue for sexual recognition and male quality in a Neotropical giant damselfly. Functional Ecology, 23, 724–732. https://doi.org/10.1111/j.1365-2435.2009.01584.x
10.1111/j.1365-2435.2009.01584.x
Web of Science®Google Scholar
Schuppe, E. R., & Fuxjager, M. J. (2018). High-speed displays encoding motor skill trigger increased territorial aggression in downy woodpeckers. Functional Ecology, 32, 450–460. https://doi.org/10.1111/1365-2435.12993
10.1111/1365-2435.13010
Web of Science®Google Scholar
Seddon, N. (2005). Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds. Evolution, 59, 200–215. https://doi.org/10.1111/j.0014-3820.2005.tb00906.x
10.1111/j.0014-3820.2005.tb00906.x
PubMedWeb of Science®Google Scholar
Seddon, N., Tobias, J. A., Eaton, M., Ödeen, A., & Byers, B. E. (2010). Human vision can provide a valid proxy for avian perception of sexual dichromatism. The Auk, 127, 283–292. https://doi.org/10.1525/auk.2009.09070
10.1525/auk.2009.09070
Web of Science®Google Scholar
Servedio, M. R. (2016). Geography, assortative mating, and the effects of sexual selection on speciation with gene flow. Evolutionary Applications, 9, 91–102. https://doi.org/10.1111/eva.12296
10.1111/eva.12296
PubMedWeb of Science®Google Scholar
Siefferman, L., & Hill, G. E. (2003). Structural and melanin coloration indicate parental effort and reproductive success in male eastern bluebirds. Behavioral Ecology, 14, 855–861. https://doi.org/10.1093/beheco/arg063
10.1093/beheco/arg063
Web of Science®Google Scholar
Smith, K. R., Cadena, V., Endler, J. A., Porter, W. P., Kearney, M. R., & Stuart-Fox, D. (2016). Colour change on different body regions provides thermal and signalling advantages in bearded dragon lizards. Proceedings of the Royal Society B: Biological Sciences, 283, 20160626. https://doi.org/10.1098/rspb.2016.0626
10.1098/rspb.2016.0626
Web of Science®Google Scholar
Stange, N., Page, R. A., Ryan, M. J., & Taylor, R. C. (2016). Interactions between complex multisensory signal components result in unexpected mate choice responses. Animal Behaviour, 134, 239–247.
10.1016/j.anbehav.2016.07.005
Web of Science®Google Scholar
Stoddard, M. C., & Prum, R. O. (2008). Evolution of avian plumage color in a tetrahedral color space: A phylogenetic analysis of new world buntings. The American Naturalist, 171, 755–776. https://doi.org/10.1086/587526
10.1086/587526
PubMedWeb of Science®Google Scholar
Stuart-Fox, D. M., & Ord, T. J. (2004). Sexual selection, natural selection and the evolution of dimorphic coloration and ornamentation in agamid lizards. Proceedings of the Royal Society B: Biological Sciences, 271, 2249–2255. https://doi.org/10.1098/rspb.2004.2802
10.1098/rspb.2004.2802
PubMedWeb of Science®Google Scholar
Taylor, R. C., & Ryan, M. J. (2013). Interactions of multisensory components perceptually rescue Tungara frog mating signals. Science, 341, 273–274. https://doi.org/10.1126/science.1237113
10.1126/science.1237113
CASPubMedWeb of Science®Google Scholar
Théry, M. (2001). Forest light and its influence on habitat selection. In K. E. Linsenmair, A. J. Davis, B. Fiala, & M. R. Speight (Eds.), Tropical forest canopies: Ecology and management (pp. 251–261). Dordrecht, the Netherlands: Kluwer Academic Publishers. https://doi.org/10.1007/978-94-017-3606-0
10.1007/978-94-017-3606-0_20
Google Scholar
Tobias, J. A., Aben, J., Brumfield, R. T., Derryberry, E. P., Halfwerk, W., Slabbekoorn, H., & Seddon, N. (2010). Song divergence by sensory drive in amazonian birds. Evolution, 64, 2820–2839.
10.1111/j.1558-5646.2010.01067.x
PubMedWeb of Science®Google Scholar
Uy, J. A. C., & Endler, J. A. (2004). Modification of the visual background increases the conspicuousness of golden-collared manakin displays. Behavioral Ecology, 15, 1003–1010. https://doi.org/10.1093/beheco/arh106
10.1093/beheco/arh106
Web of Science®Google Scholar
Wallace, A. R. (1869). The Malay Archipelago: The land of the orang-utan and the bird of paradise; a narrative of travel, with studies of man and nature. North Chelmsford, MA: Courier Corporation.

Google Scholar
White, T. E., Zeil, J., & Kemp, D. J. (2015). Signal design and courtship presentation coincide for highly biased delivery of an iridescent butterfly mating signal. Evolution, 69, 14–25. https://doi.org/10.1111/evo.12551
10.1111/evo.12551
PubMedWeb of Science®Google Scholar
Widemo, F., & Owensi, I. P. F. (1995). Lek size, male mating skew and the evolution of lekking. Nature, 373, 148–151. https://doi.org/10.1038/373148a0
10.1038/373148a0
CASWeb of Science®Google Scholar
Wilkins, M. R., Seddon, N., & Safran, R. J. (2013). Evolutionary divergence in acoustic signals: Causes and consequences. Trends in Ecology and Evolution, 28, 156–166. https://doi.org/10.1016/j.tree.2012.10.002
10.1016/j.tree.2012.10.002
PubMedWeb of Science®Google Scholar
Wright, J. J. (2002). Plant diversity in tropical forests: A review of mechanisms of species coexistence. Oecologia, 130, 1–14. https://doi.org/10.1007/s004420100809
10.2307/1940675
PubMedWeb of Science®Google Scholar
Zahavi, A. (1975). Mate selection-A selection for a handicap. Journal of Theoretical Biology, 53, 205–214. https://doi.org/10.1016/0022-5193(75)90111-3
10.1016/0022-5193(75)90111-3
CASPubMedWeb of Science®Google Scholar

Citing Literature

Volume87, Issue4

Special Feature: Linking organismal functions, life history strategies and population performance

July 2018

Pages 1149-1159

Synergistic selection regimens drive the evolution of display complexity in birds of paradise

Abstract

1 INTRODUCTION

2 MATERIALS AND METHODS