Received: 28 November 2017 | Accepted: 10 January 2018

DOI: 10.1111/1365-2656.12824

RESEARCH ARTICLE

Synergistic selection regimens drive the evolution of display

complexity in birds of paradise

Meredith C. Miles | Matthew J. Fuxjager

Department of Biology, Wake Forest

University, Winston-Salem, NC, USA Abstract
1. Integrated visual displays that combine gesture with colour are nearly ubiquitous
Correspondence
Meredith C. Miles in the animal world, where they are shaped by sexual selection for their role in
Email: milemc16@wfu.edu courtship and competition. However, few studies assess how multiple selection
Funding information regimens operate on different components of these complex phenotypes on a
National Science Foundation, Grant/Award macroevolutionary scale.
Number: IOS-1655730
2. Here, we study this issue by assessing how both sexual and ecological selection
Handling Editor: Elizabeth Derryberry work together to influence visual display complexity in the birds of paradise.
3. 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 commu-
nal display courts have more carotenoid-based ornaments and fewer melanin
ornaments.
4. Meanwhile, display habitat influences gestural complexity. Species that dance in
the cluttered understorey have more complex dances than canopy-displaying
species.
5. 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.

KEYWORDS
animal communication, behavioural ecology, display habitat, evolutionary ecology, lek, sexual
selection, signal design

1 | I NTRO D U C TI O N to complex displays, which consist of multiple signalling elements.

Animal displays are vital to mediating mate choice and competi-
tion. 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 selec-
tion regimens is therefore a major goal in biology. Work to date indi-
cates that signal design is the product of multiple selection regimens
operating in tandem (Endler, 1987; Seddon, 2005). This also applies
Complex displays should evolve in a modular fashion, where each
novel signal offers a new opportunity for one or more selection pres-
sures to act (Hebets et al., 2016; Miles, Schuppe, Ligon, & Fuxjager,
2018). However, most work that examines multicomponent dis-
plays 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 rela-
tively few studies that take such a broad approach to this topic (but

J Anim Ecol. 2018;87:1149–1159. wileyonlinelibrary.com/journal/jane

© 2018 The Authors. Journal of Animal Ecology | 1149
© 2018 British Ecological Society

1150 | Journal of Animal Ecology
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 or-
naments 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 inte-
grated 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 com-
plexity, 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 dichroma-
tism in different ways. Among the many possibilities are exagger-
ating 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 poten-
tial 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 on-
togenically 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 re-
sults 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 fe-
male 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;
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MILES and FUXJAGER
Lindsay et al., 2015). At the same time, many species undergo dif-
fering 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 vari-
able, 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 vi-
sual 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 intrasex-
ual 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 isola-
tion 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 in-
formation to the receiver (Endler, 1992). In this way, signal design
is also subject to change based on how effectively it can be trans-
mitted 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 af-
fect short-­range visual displays as well, because increasing environ-
mental “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 herba-
ceous 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 dif-
ferentially 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) rep-
resent 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
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MILES and FUXJAGER Journal of Animal Ecology | 1151

& 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 dis-
play 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 spe-
cies 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 com-
plexity of integrated visual displays that comprise both colour and
gesture. If bird of paradise displays are indeed modular (i.e., multiple

F I G U R E 1 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]

1152 | Journal of Animal Ecology
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 vari-
ation in both gesture and colour. Finally, we examine how display
microhabitat influences signal design. By comparing how fundamen-
tal agents of evolution act on different signals, we aim to establish a
novel framework for understanding how synergistic selection regi-
mens facilitate the emergence of complex modular displays.
2 | M ATE R I A L S A N D M E TH O DS
2.1 | Experimental and statistical approach
We adopted a hypothesis-­driven approach to examine three indi-
ces 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 meth-
ods (Felsenstein, 1985) that account for non-­independence of com-
parative 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 con-
tinuous 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 con-
tinuous response variable (complexity scores), so we used phyloge-
netic 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).
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 in-
tersexual and intrasexual selection, as well as display habitat. This
information was derived using authoritative species accounts docu-
menting 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
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MILES and FUXJAGER
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 evolu-
tion (Borgia, 1979; Payne, 1984; Widemo & Owensi, 1995).
We next aimed to examine how degrees of sexual selection by di-
rect male–male competition predict differences in display complex-
ity. 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 al-
ternate 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 spe-
cies, 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 com-
plexity. 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 understo-
rey 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 qual-
itative 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”

MILES and FUXJAGER
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 previ-
ously (Fuxjager et al., 2015; Lindsay et al., 2015; Miles et al., 2017).
This index uses published display descriptions to distinguish be-
tween 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 con-
sider these two wing displays to be unique gestures.
We define display complexity as the sum of discrete physical out-
puts 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 manoeu-
vres. We used published species accounts of display repertoires
(Frith & Beehler, 1998) augmented with information from later expe-
ditions (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 com-
plexity 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 mo-
tion). To eliminate bias, an individual blind to our hypotheses com-
puted all display complexity scores. Because complexity scoring is
based on human interpretation of the literature, a second individ-
ual (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
2
(R = .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
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Journal of Animal Ecology | 1153
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 effec-
tive proxy for quantifying avian coloration and making robust evo-
lutionary 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 in-
dividual 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 co-
lour 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 under-
standing 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 po-
tentially 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 out-
line above to determine whether each male plumage patch either
(1) incorporated carotenoid coloration, or (2) only expressed mela-
nin 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 total .
ncarotenoid
patches
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 re-
lated to the extent of colour generated by melanin (melanin pro-
portion = 1 – carotenoid proportion) in all species except Cicinnurus
regius. We therefore ran additional analyses using melanin propor-
tion as a dependent variable, but these data are not included in
figures due to redundancy. We also did not evaluate structural col-
oration, because it exists on a subtle continuum from matte feathers
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1154 | Journal of Animal Ecology MILES and FUXJAGER

(no structural colour), to glossy colours, to new colours introduced
altogether (Maia, D’Alba, & Shawkey, 2011). As such, it is nearly im-
possible to assess structural coloration through the lens of complex-
ity using handbook plates, as our index could not account for subtle
innovations in structural modifications.
3 | R E S U LT S
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 dichro-
matism (F1,34 = 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 (AICc = 197.35), sexual dichromatism scores are best
fit with a lambda transformation (AICc = 223.3, λ = 0.856), and kappa
processes underlie both carotenoid proportion (AICc = −25.28,
κ = 0.44) and melanin proportion (AICc = −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 spe-
cies had significantly higher dichromatism scores than non-­lekking
species (F1,34 = 24.628, p = .033, λ = 0.857). However, there was
no difference among lekking and non-­
lekking species for carot-
enoid proportion (F1,34 = 15.53, p = .100, κ = 0.44), melanin propor-
tion (F1,34 = 18.69, p = .100, κ = 0.15) or gestural complexity score
(F1,34 = 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; F1,34 = 17.610, p = .006, κ = 0.44). The re-
verse was true for melanin patch proportion, as solitary-­displaying

F I G U R E 2 Elements of visual display complexity as they vary among lekking (low intersexual selection pressure) and non-­lekking (high
intersexual selection) species (a); by the number of males displaying together (b), which indicates intrasexual selection pressure; and by
display habitat (c). Statistically significant differences are indicated with an asterisk (*), whereas non-­significant comparisons read n.s. Note
that because values were compared using phylogenetic ANOVA, what appear to be qualitative differences (as in carotenoid ornamentation
among lekking and non-­lekking species) are not always significant, because these trait differences are indistinguishable from discrepancies
produced by evolutionary history alone [Colour figure can be viewed at wileyonlinelibrary.com]

MILES and FUXJAGER
males had higher melanin proportion scores (F1,34 = 17.84, p = .008,
κ = 0.15). However, there was no such difference for dichromatism
(F1,34 = 2.024, p = .333, λ = 0.857) or gestural display complexity
scores (F1,34 = 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; F1,34 = 15.471, p = .005). Meanwhile, display stratum
does not explain variation in male coloration, either in total colour
complexity score (F = 1.591,34, p = .526, λ = 0.857) or in the relative
amount of carotenoid patches (F1,34 = 0.79, p = .526, κ = 0.44) or
melanin patches (F1,34 = 0.79, p = .526, κ = 0.15).
4 | D I S CU S S I O N
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 habi-
tat 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 dis-
plays therefore exhibit modularity (Hebets et al., 2016), because in-
dividual 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 evolution-
ary 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 dichro-
matism 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
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Journal of Animal Ecology | 1155
F I G U R E 3 Signal space schematic depicting how female choice
(red arrow), direct male–male competition (blue arrow) and display
habitat (orange arrow) each influence visual displays in birds of
paradise. The four plotted points correspond to four representative
species that exemplify these effects: (1) Manucodia chalybatus, a
non-­lekking species that displays alone in the canopy, is sexually
monochromatic and performs a relatively simple display, (2) male
Astrapia rothschildi, which display in the canopy at a solitary lek,
are highly sexually dichromatic, (3) Paradisaea rubra gather in large
numbers to display in canopy leks and employ numerous carotenoid
ornaments, and (4) Parotia carolae have the most complex dance
routines of all, performing in groups of up to 6 on their forest floor
leks [Colour figure can be viewed at wileyonlinelibrary.com]
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 respon-
sible 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 ex-
treme are also those species where males have evolved more plum-
age 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 sex-
ual 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 or-
naments 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 gen-
erated by diet-­derived carotenoid pigments (Goodwin, 1980). This

1156 | Journal of Animal Ecology
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 color-
ation 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 court-
ship 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 an-
other 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, per-
haps of motor skill or vigour (Byers et al., 2010), which may influence
phenotypic patterning of individual gesture exaggeration and/or co-
ordination 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 com-
plex 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 sig-
nalling 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 sig-
naller (Fleishman, 1992). Alternatively, the difference in gestural
complexity across display habitats may be a product of physiolog-
ical and/or morphological constraints associated with dancing on
different perching substrates; while most understorey species dis-
play on the ground or on vertical perches, canopy-­displaying spe-
cies exclusively use larger perches. How does evolution proceed in
the face of these environmental challenges? Using more gestures
13652656, 2018, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2656.12824 by Welsh Assembly Government, Wiley Online Library on [23/06/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MILES and FUXJAGER
is only one potential solution to signalling in a challenging envi-
ronment; 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 under-
storey 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 func-
tion as redundant messages (Rowe, 1999). For example, most species
call extensively before dancing, often using a different perch specif-
ically for vocalizing. Some birds of paradise incorporate tactile and
even olfactory signalling into their displays as well, which further ex-
pands 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 court-
ship display, which may evolve in surprising ways. For example, co-
lour 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 | CO N C LU S I O N S
Altogether, these results offer novel insight into the macroevolu-
tionary 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 extraor-
dinary bird of paradise visual displays, exemplifies the diversifying
potential of animal behaviour.
AC K N OW L E D G E M E N T S
The work was funded by NSF grant IOS-­1655730 to M.J.F. The au-
thors have no conflicts of interest to declare.
AU T H O R S ’ C O N T R I B U T I O N S
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 AC C E S S I B I L I T Y
Data from this study are available online at the Dryad Digital R
­ epository:
https://doi.org/10.5061/dryad.9m47pj0 (Miles & Fuxjager, 2018).

MILES and FUXJAGER
ORCID
Meredith C. Miles http://orcid.org/0000-0002-7307-0195
Matthew J. Fuxjager https://orcid.org/0000-0003-0591-6854
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
Andersson, M. B. (1994). Sexual selection. Princeton, NJ: Princeton
University Press.
Andersson, S., Pryke, S. R., Ornborg, J., Lawes, M. J., & Andersson, M.
(2002). Multiple receivers, multiple ornaments, and a trade-­off be-
tween agonistic and epigamic signaling in a widowbird. The American
Naturalist, 160, 683–691.
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
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
Basolo, A. L., & Alcaraz, G. (2003). The turn of the sword: Length in-
creases male swimming costs in swordtails. Proceedings of the
Royal Society B: Biological Sciences, 270, 1631–1636. https://doi.
org/10.1098/rspb.2003.2388
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
Bloch, N. I., Morrow, J. M., Chang, B. S. W., & Price, T. D. (2015). SWS2 vi-
sual 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
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
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.
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
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
Cardoso, G. C., & Mota, P. G. (2008). Speciational evolution of color-
ation in the genus Carduelis. Evolution, 62, 753–762. https://doi.
org/10.1111/j.1558-5646.2008.00337.x
del Hoyo, J., Elliott, A., & Sargatal, J. (1999). Handbook of the birds of the
world, vol. 5. Barcelona, Spain: Lynx Edicions.
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
Endler, J. A. (1992). Signals, signal conditions, and the direction of
evolution. The American Naturalist, 139, S125–S153. https://doi.
org/10.1086/285308
Endler, J. A. (1993). The color of light in forests and its implications.
Ecological Monographs, 63, 1–27. https://doi.org/10.2307/2937121
Endler, J. A., & Thery, M. (1996). Interacting effects of lek placement, dis-
play behavior, ambient light, and color patterns in three neotropical
13652656, 2018, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2656.12824 by Welsh Assembly Government, Wiley Online Library on [23/06/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Journal of Animal Ecology | 1157
forest-­dwelling birds. The American Naturalist, 148, 421–452. https://
doi.org/10.1086/285934
Felsenstein, J. (1985). Phylogenies and the comparative method. The
American Naturalist, 125, 1–15. https://doi.org/10.1086/284325
Fleishman, L. J. (1992). The influence of the sensory system and the en-
vironment on motion patterns in the visual displays of anoline lizards
and other vertebrates. The American Naturalist, 139, S36. https://doi.
org/10.1086/285304
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
Frith, C. B., & Beehler, B. M. (1998). The birds of paradise. Oxford, UK:
Oxford University Press.
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
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
Garland, T., Dickerman, A. W., Janis, C. M., & Jones, J. A. (1993).
Phylogenetic analysis of covariance by computer simula-
tion. Systematic Biology, 42, 265–292. https://doi.org/10.1093/
sysbio/42.3.265
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
Goodwin, T. W. (1980). The biochemistry of the carotenoids. Dordrecht, the
Netherlands: Springer. https://doi.org/10.1007/978-94-009-5860-9
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
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
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
Gray, E. M. (1997). Female red-­winged blackbirds accrue material bene-
fits from copulating with extra-­pair males. Animal Behavior, 53, 625–
639. https://doi.org/10.1006/anbe.1996.0336
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
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
Hebets, E. A., Barron, A. B., Balakrishnan, C. N., Hauber, M. E., Mason,
P. H., & Hoke, K. L. (2016). A systems approach to animal commu-
nication. Proceedings of the Royal Society B: Biological Sciences, 283,
20152889. https://doi.org/10.1098/rspb.2015.2889
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
Hebets, E. A., & Uetz, G. W. (2000). Leg ornamentation and the effi-
cacy of courtship display in four species of wolf spider (Araneae:

1158 | Journal of Animal Ecology
Lycosidae). Behavioral Ecology and Sociobiology, 47, 280–286. https://
doi.org/10.1007/s002650050667
Hebets, E. A., Vink, C. J., Sullivan-Beckers, L., & Rosenthal, M. F. (2013).
The dominance of seismic signaling and selection for signal com-
plexity in Schizocosa multimodal courtship displays. Behavioral
Ecology and Sociobiology, 67, 1483–1498. https://doi.org/10.1007/
s00265-013-1519-4
Hill, G. E., & McGraw, K. J. (2006). Bird coloration: Mechanisms and mea-
surements. Cambridge, MA: Harvard University Press.
Holm, S. (1988). A simple sequentially rejective multiple test procedure.
Scandinavian Journal of Statistics, 6, 65–70.
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
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
Jønsson, K. A., Fabre, P.-H., Kennedy, J. D., Holt, B. G., Borregaard,
M. K., Rahbek, C., & Fjeldså, J. (2016). A supermatrix phy-
logeny of corvoid passerine birds (Aves: Corvides). Molecular
Phylogenetics and Evolution, 94, 87–94. https://doi.org/10.1016/
j.ympev.2015.08.020
Keyser, A. J. (2000). Structurally based plumage coloration is an hon-
est signal of quality in male blue grosbeaks. Behavioral Ecology, 11,
202–209. https://doi.org/10.1093/beheco/11.2.202
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
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.
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
Laman, T., & Scholes, E. (2012). Birds of paradise: Revealing the world’s most
extraordinary birds. Washington, DC: National Geographic Books.
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
Lindsay, W. R., Houck, J. T., Giuliano, C. E., & Day, L. B. (2015).
Acrobatic courtship display coevolves with brain size in manak-
ins (Pipridae). Brain, Behavior and Evolution, 85, 29–36. https://doi.
org/10.1159/000369244
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
Maia, R., Rubenstein, D. R., & Shawkey, M. D. (2016). Selection, con-
straint, and the evolution of coloration in African starlings. Evolution,
70, 1064–1079. https://doi.org/10.1111/evo.12912
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.
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
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
13652656, 2018, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2656.12824 by Welsh Assembly Government, Wiley Online Library on [23/06/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MILES and FUXJAGER
McDonald, D. B., & Potts, W. K. (1994). Cooperative display and relat-
edness among males in a lek-­mating bird. Science, 266, 1030–1032.
https://doi.org/10.1126/science.7973654
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
Miles, M. C., & Fuxjager, F. J. (2018). Data from: Synergistic selection reg-
imens drive the evolution of display complexity in birds of paradise.
Dryad Digital Repository, https://doi.org/10.5061/dryad.9m47pj0
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
Milinski, M., & Bakker, T. C. M. (1990). Female sticklebacks use male col-
oration in mate choice and hence avoid parasitized males. Nature,
344, 330–333. https://doi.org/10.1038/344330a0
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[270
7:FSCAAL]2.0.CO;2
Omland, K. E., & Lanyon, S. M. (2000). Reconstructing plum-
age 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
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
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
Ord, T. J., & Stamps, J. A. (2008). Alert signals enhance animal communi-
cation 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
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
Payne, R. B. (1984). Sexual selection, lek and arena behavior, and sex-
ual size dimorphism in birds. Ornithological Monographs, 33, iii–52.
https://doi.org/10.2307/40166729
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
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
Price, J. J., Earnshaw, S. M., & Webster, M. S. (2006). Montezuma oro-
pendolas 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
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
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

MILES and FUXJAGER
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
Robel, R. J., & Ballard, W. B. (1974). Lek social organization and reproduc-
tive success in the greater prairie chicken. Integrative and Comparative
Biology, 14, 121–128.
Roulin, A. (2016). Condition-­d ependence, pleiotropy and the hand-
icap principle of sexual selection in melanin-­ b ased coloura-
tion. Biological Reviews, 91, 328–348. https://doi.org/10.1111/
brv.12171
Rowe, C. (1999). Receiver psychology and the evolution of multicompo-
nent signals. Animal Behaviour, 58, 921–931. https://doi.org/10.1006/
anbe.1999.1242
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 mat-
ing 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
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
Schultz, T. D., & Fincke, O. M. (2009). Structural colours create a flash-
ing 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
Schuppe, E. R., & Fuxjager, M. J. (2018). High-­speed displays encod-
ing motor skill trigger increased territorial aggression in downy
woodpeckers. Functional Ecology, 32, 450–460. https://doi.
org/10.1111/1365-2435.12993
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
Seddon, N., Tobias, J. A., Eaton, M., Ödeen, A., & Byers, B. E. (2010).
Human vision can provide a valid proxy for avian perception of sex-
ual dichromatism. The Auk, 127, 283–292. https://doi.org/10.1525/
auk.2009.09070
Servedio, M. R. (2016). Geography, assortative mating, and the ef-
fects of sexual selection on speciation with gene flow. Evolutionary
Applications, 9, 91–102. https://doi.org/10.1111/eva.12296
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
Smith, K. R., Cadena, V., Endler, J. A., Porter, W. P., Kearney, M. R., &
Stuart-Fox, D. (2016). Colour change on different body regions pro-
vides 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
Stange, N., Page, R. A., Ryan, M. J., & Taylor, R. C. (2016). Interactions
between complex multisensory signal components result in unex-
pected mate choice responses. Animal Behaviour, 134, 239–247.
Stoddard, M. C., & Prum, R. O. (2008). Evolution of avian plumage
color in a tetrahedral color space: A phylogenetic analysis of new
13652656, 2018, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2656.12824 by Welsh Assembly Government, Wiley Online Library on [23/06/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Journal of Animal Ecology | 1159
world buntings. The American Naturalist, 171, 755–776. https://doi.
org/10.1086/587526
Stuart-Fox, D. M., & Ord, T. J. (2004). Sexual selection, natural selec-
tion 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
Taylor, R. C., & Ryan, M. J. (2013). Interactions of multisensory compo-
nents perceptually rescue Tungara frog mating signals. Science, 341,
273–274. https://doi.org/10.1126/science.1237113
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
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.
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
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.
White, T. E., Zeil, J., & Kemp, D. J. (2015). Signal design and courtship pre-
sentation coincide for highly biased delivery of an iridescent butterfly
mating signal. Evolution, 69, 14–25. https://doi.org/10.1111/evo.12551
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
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
Wright, J. J. (2002). Plant diversity in tropical forests: A review of mech-
anisms of species coexistence. Oecologia, 130, 1–14. https://doi.
org/10.1007/s004420100809
Zahavi, A. (1975). Mate selection-­ A selection for a handi-
cap. Journal of Theoretical Biology, 53, 205–214. https://doi.
org/10.1016/0022-5193(75)90111-3
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How to cite this article: Miles MC, Fuxjager MJ. Synergistic
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