Valcu. Extra Pair Paternity and Sexual Dimorphism in Birds

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Received: 19 October 2022 Revised: 1 February 2023 Accepted: 6 February 2023
DOI: 10.1111/jeb.14172
RESEARCH ARTICLE
Extra-pair paternity and sexual dimorphism in birds
Mihai Valcu | Cristina Valcu | Bart Kempenaers
Department of Behavioural Ecology

and Evolutionary Genetics, Max Planck Abstract
Institute for Ornithology, Seewiesen,
Differences in the strength of sexual selection between males and females can lead to
Germany
sexual dimorphism. Extra-pair paternity (EPP) can increase the variance in male repro-
Correspondence
ductive success and hence the opportunity for sexual selection. Previous research on
Bart Kempenaers, Department of
Behavioural Ecology and Evolutionary birds suggests that EPP drives the evolution of dimorphism in plumage colour and in
Genetics, Max Planck Institute for
body size. Because EPP increases the intensity of sexual selection in males, it should
Biological Intelligence, 82319 Seewiesen,
Germany. lead to increased dimorphism in species with larger or more colourful males, but de-
Email: bart.kempenaers@bi.mpg.de
creased dimorphism in species with larger or more colourful females. We explored the
Funding information covariation between EPP and sexual dimorphism in wing length and plumage coloura-
Max-Planck-Gesellschaft
tion in 401 bird species, while controlling for other, potentially confounding variables.
Wing length dimorphism was associated positively with the frequency of EPP, but also
with social polygamy, sex bias in parental behaviour and body size and negatively with
migration distance. The frequency of EPP was the only predictor of plumage colour
dimorphism. In support of our prediction, high EPP levels were associated with sexual
dichromatism, positively in species in which males are more colourful and negatively
in those in which females are more colourful. Contrary to our prediction, high EPP
rates were associated with increased wing length dimorphism in species with both
male-and female-biased dimorphism. The results support a role for EPP in the evolu-
tion of both size and plumage colour dimorphism. The two forms of dimorphism were
weakly correlated and predicted by different reproductive, social and life-history
traits, suggesting an independent evolution.
KEYWORDS
body size, plumage colouration, polygamy, promiscuity, sexual selection
1 | I NTRO D U C TI O N that sexual selection may be the main evolutionary driver of sexual
dimorphism and several studies have since shown that differences in
In many bird species males and females differ considerably, for ex- the strength of sexual selection between males and females can lead
ample, in size, plumage colouration, song or other secondary sexual to different forms of sexual dimorphism (Dunn et al., 2001; Owens
traits. In extreme cases, the phenotypic divergence between the & Hartley, 1998). The social mating system is a key indicator of the
sexes (i.e. sexual dimorphism) can even exceed the difference among intensity of sexual selection because it reflects variation in the social
species (Andersson, 1994). Darwin (1871) was the first to recognize mating success of males and females. Socially polygamous species,
Mihai Valcu and Cristina Valcu contributed equally to this work.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction
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© 2023 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology.
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wileyonlinelibrary.com/journal/jeb J Evol Biol. 2023;36:764–779.
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VALCU et al. 765
in which one sex experiences higher variation in mating success and of the social bond, migratory behaviour and latitude. To circumvent
higher competition for mates, and thus more intense sexual selection, the limited availability of data on the frequency of EPP and cover a
are typically more dimorphic, with the sex with the higher variance larger and phylogenetically more diverse sample of species, Dunn
in the number of social mates being larger (Dunn et al., 2001; Owens et al. (2001) used relative testis size as a proxy for EPP. The occur-
& Hartley, 1998; Székely et al., 2007) and more ornamented (Dale rence of extra-pair copulations leads to sperm competition (i.e. the
et al., 2015; Dunn et al., 2001, 2015). Because males and females competition between sperm from different males), which causes
breeding in monogamous pairs have the same number of mates and selection favouring increased sperm production and larger testis.
offspring and thus experience a similar intensity of sexual selection, Previous studies have shown positive associations between relative
no or only small sex differences are expected. Yet many socially mo- testis size and (1) the level of EPP (Moller & Briskie, 1995) and (2)
nogamous species show considerable sexual dimorphism in size (e.g. sexual dimorphism in plumage colour (Dunn et al., 2001, 1031 spe-
Phylloscopus fuscatus, Clement, 2020) and in plumage colouration cies, Dunn et al., 2015, 977 species). However, using relative testis
(i.e. dichromatism, e.g., Sialia mexicana, Guinan et al., 2020). size as a proxy for EPP can be problematic, because data on testis
Sexual selection can arise from competition for more or better size are often unreliable and using them in comparative analyses can
mates, both within and outside the social unit (Shuker, 2010). Hence, produce spurious results (Calhim & Birkhead, 2007).
one possible mechanism behind the evolution of sexual dimorphism Evidence for an association between EPP and sexual size di-
in socially monogamous species is sexual selection caused by vari- morphism across species is, conversely, limited. Owens and
ation in extra-pair siring success (Westneat et al., 1990). Extra-pair Hartley (1998) found no association between the proportion of
paternity (EPP) occurs when individuals engage in copulations out- broods with extra-pair young and sexual dimorphism in body mass,
side the pair bond, and can create a higher variance in male repro- whereas Dunn et al. (2001) reported a positive correlation between
ductive success and thus greater opportunity for sexual selection in relative testis size and sexual dimorphism in tail and wing length, but
males (Kempenaers & Schlicht, 2010). Research has shown that EPP not in body mass.
can even have a larger effect on the opportunity for selection than Taken together, previous studies clearly support a role for EPP in
variation in pairing status or in the quality of the social mate, at least driving the evolution of plumage colour dimorphism in birds, but to
in some species (Webster et al., 1995, 2007). EPP has been found what degree EPP also contributes to the evolution of size dimorphism
in 82% of 401 bird species investigated so far, suggesting that it is a remains less clear. Here, we investigate the link between EPP and sex-
common mating strategy (Valcu et al., 2021). EPP could lead to sexual size and plumage colour dimorphism in birds. First, we use spa-
ual dimorphism, for example, if females gain direct or indirect bene- tially explicit models which account for variation in EPP levels within
fits from choosing larger or more colourful extra-pair mates (female the species' breeding range (Valcu et al., 2021) to produce robust EPP
choice), or if male success in gaining EPP is size-or colour-dependent estimates for 401 avian species. We then explore the association be-
(male–male competition) (Dunn et al., 2001). tween sexual size and plumage colour dimorphism and the proportion
Although the evolutionary causes of EPP are still debated of EP broods and EP offspring. Natural and social selection can also
(Forstmeier et al., 2014), the hypothesis that EPP drives the evo- contribute to variation in sexual dimorphism along with sexual selec-
lution of sexual dimorphism is supported by both within-and tion (Dale et al., 2015; Dunn et al., 2015; Soler & Moreno, 2012). Thus,
between-
species analyses. Within several species, male extra- factors such as migration (Friedman et al., 2009; Simpson et al., 2015)
pair siring success correlated positively with male plumage co- or parental roles (Fairbairn et al., 2007) can also lead to sexual dimor-
louration (Albrecht et al., 2009; Balenger et al., 2009; Sheldon phism. We therefore control for potentially confounding variables in-
& Ellegren, 1999; Sundberg & Dixon, 1996; Wells et al., 2015; cluding the social mating system (Dale et al., 2015; Dunn et al., 2001,
Yezerinac & Weatherhead, 1997), and with body size (Akçay 2015; Owens & Hartley, 1998; Székely et al., 2007), parental contri-
& Roughgarden, 2007, but see Hsu et al., 2015, Kempenaers bution to incubation and offspring provisioning (Dunn et al., 2001;
et al., 1992). There is also experimental evidence for some species Owens & Hartley, 1998; Sonerud et al., 2014), migratory behaviour
that females choose extra-pair partners based on plumage coloura- (Friedman et al., 2009; Kissner et al., 2003; Simpson et al., 2015),
tion (Whittingham & Dunn, 2016, Baldassarre & Webster, 2013, but cooperative breeding (Dale et al., 2015; Du Plessis et al., 1995;
see Delhey, Peters, Johnsen, et al., 2007). Rubenstein & Lovette, 2009) and body size (Dale et al., 2007, 2015;
Comparative analyses confirmed a link between EPP and sexual Székely et al., 2007; Webb & Freckleton, 2007), as well as for the phy-
dimorphism in plumage colouration. An early study on 55 species logenetic relatedness between species.
reported a positive correlation between dimorphism in plumage In most species, sexual dimorphism in body size (Székely
colouration and the proportion of extra-pair offspring, after con- et al., 2007) or plumage colouration (Dale et al., 2015; Dunn
trolling for the level of polygyny, developmental mode and colonial- et al., 2015) is male-biased. This is a direct consequence of the in-
ity (Møller & Birkhead, 1994). Later studies confirmed that sexual tersexual differences in gametic investment (anisogamy), which pro-
plumage dimorphism is positively associated with the frequency duces greater fitness benefits of mating with multiple partners and
of EPP (73 species, Owens & Hartley, 1998, 186 species, Thibault stronger sexual selection in males (Bateman's principle). However, a
et al., 2022, 202 species, Lifjeld et al., 2019) after controlling for the small number of species display female-biased sexual dimorphism,
division of parental care between males and females, the duration often associated with polyandry (Lindenfors et al., 2003; Székely
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766 VALCU et al.
et al., 2000, 2004), high male contribution to parental care (Jönsson Ericsson backbone using the maxCladeCred function in phangorn 2.5.5
& Alerstam, 1990; Sonerud et al., 2014) or the occurrence of aerial (Schliep, 2011). We then used this consensus phylogeny to impute the
male displays (Szekely et al., 2006; Székely et al., 2004). Although missing wing length data for four species based on the data already
some of the processes leading to sexual dimorphism, such as com- available for the other species in the dataset and the species' own body
petition for social mates or parental care, may act similarly on males mass. Wing length dimorphism was computed as the difference be-
and females, others, including EPP (Kempenaers & Schlicht, 2010) tween the ln-transformed average wing length of males and females.
and cooperative breeding (Hauber & Lacey, 2005) can act preferen- Computed this way, wing length dimorphism is close to zero in mono-
tially on one sex. Since EPP increases the variance in reproductive morphic species, positive when males are larger than females and
success and sexual selection only in males, different predictions can negative when females are larger than males. Consequently, strong
be formulated for its effect on sexual dimorphism in species with dimorphism in wing length corresponds to both large positive values in
male-biased (larger or more colourful males) or female-biased (larger species with male-biased dimorphism, and large negative values in spe-
or more colourful females) dimorphism. Thus, in species with male- cies with female-biased dimorphism. Similar measures of dimorphism
biased dimorphism, the added sexual selection on males caused by have been previously used in comparative analysis (Dunn et al., 2001),
EPP should further increase sexual dimorphism, while in species with but correlations of these variables with some life-history traits are dif-
female-biased dimorphism, EPP could have a compensatory effect, ficult to interpret and may be misleading (Figure 1). Consider a predic-
leading to lower sexual dimorphism. This prediction has received lit- tor variable that is positively correlated with the sex difference in wing
tle attention so far, due both to the relatively low representation of length irrespective of which is the larger sex. If the dataset is balanced
species with female-biased dimorphism and to the limited availabil- and the effect is similar in species with male-and female-biased dimor-
ity of EPP data from wild populations of these species. A final aim of phism, the measured effect will be close to zero (Figure 1a). The meas-
the paper, is therefore to investigate how sexual selection in general, ured effect will be positive either if the effect is stronger in species
and EPP in particular, drives sexual size and plumage colour dimor- with male-biased dimorphism or if these species are more prevalent
phism in species with male-biased or female-biased dimorphism. in the dataset (e.g. Figure 1d), and negative if the effect is stronger in
species with female-biased dimorphism or if these species are over-
represented in the dataset. A positive correlation between a predic-
2 | M ATE R I A L S A N D M E TH O DS tor variable and the measure of wing length dimorphism described
above would imply that this variable takes large values in species with
2.1 | Measures of sexual dimorphism in size and strong male-biased dimorphism and small values in those with female-
plumage colour biased dimorphism, but this may not be the case (e.g. Figure 1d). To
obtain biologically meaningful results in species with either male-or
2.1.1 | Wing length dimorphism female-
biased dimorphism, we explored the association between
sexual dimorphism and EPP with models which included the abso-
We used wing length dimorphism as a primary measure for sexual lute wing length dimorphism as the dependent variable (Figure 1b,e).
size dimorphism. Wing length is a more suitable index of body size To detect putative differences between species with either male-or
compared to other size measurements such as tarsus and bill length, female-biased dimorphism (e.g. Figure 1c,f) we subsequently included
which are under stronger functional selection, or body mass, which interaction terms with the direction of the dimorphism in the models
shows strong seasonal and even diurnal variation (Székely et al., 2004, (see below). In our dataset, absolute wing length dimorphism ranged
2007). Moreover, reliable measurements of female body mass are dif- between 0 and 0.11 (corresponding to a size difference of about 12%).
ficult to obtain during the reproductive season, because female mass Sixty-eight species showed a female-biased dimorphism, and 333 spe-
varies greatly before and after egg laying (Székely et al., 2007). As a cies had a male-biased dimorphism (Figure 2).
result, sexual dimorphism in body mass has higher dispersion than
sexual dimorphism in wing length, both at species and at family level
(Székely et al., 2007). Wing length is therefore typically preferred over 2.1.2 | Body mass dimorphism
body mass for measuring body size dimorphism (Dale et al., 2007;
Krüger, 2005; Székely et al., 2007). Average wing length (mm) for Despite the known limitations of the variable, size dimorphism has
males and females was obtained mostly from (Dale et al., 2007, for often been computed based on body mass (Dunn et al., 2001, 2015;
additional data sources see Supplement Data). Because imputation Owens & Hartley, 1998). To enable the comparison of our results
of missing data is generally preferred to the omission of missing data with previous studies, we used body mass dimorphism as a second-
and because including phylogenetic information improves imputation ary measure of size dimorphism. Average body mass (g) for males and
performance (Penone et al., 2014), we estimated missing wing length females was obtained mostly from (Dunning, 2007, for additional
values by phylogenetic imputation with the package Rphylopars (v data sources see Supplement Data). We estimated missing body
0.2.12; Goolsby et al., 2017), using the Pagel's lambda model of trait mass values for seven species by imputation, as described above for
evolution (Pagel, 1997). To do this, we built a consensus phylogeny wing length values. We computed body mass dimorphism similarly
using 1000 trees (sampled from Birdtree.org (Jetz et al., 2012)) with to wing length dimorphism, as the absolute difference between the
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VALCU et al. 767
F I G U R E 1 Illustration of correlations between sexual dimorphism and a hypothetical explanatory variable x. For two simulated datasets,
sexual dimorphism was computed either as the difference in trait value between males and females (a, d) or as the absolute value of the
difference in trait value between the sexes (b, e). Blue dots represent species with male-biased dimorphism and red dots represent species
with female-biased dimorphism. The first dataset contains an equal number of species with male-and female-biased dimorphism (a–c), while
the second contains a larger number of species with male-biased dimorphism (d–f ). Effect sizes for species with male-and female-biased
dimorphism were similar in the first dataset (a–c) but different in the second (d–f ). Measuring sexual dimorphism as the absolute value of the
difference in trait value between males and females allows to investigate potential interactions with the direction of the dimorphism (c, f).
ln-transformed average body mass of males and females. Body mass colour elaboration is close to zero in monochromatic species, and
dimorphism ranged between 0 and 0.34; 128 species had a female- low in species in which males and females have different colours
biased dimorphism and 273 species had a male-biased dimorphism. with similar levels of elaboration. The sex difference in colour elabo-
ration varied between 0 and 292 (indigo bunting Passerina cyanea).
The difference in colour elaboration correlates well with other meas-
2.1.3 | Difference in colour elaboration ures of plumage dimorphism, for example, with sexual dichromatism
(Dale et al., 2015, Pearson's r = 0.85, n = 232) and with dichromatism
We scored colour elaboration following Carballo et al. (2020). We in hue (Dunn et al., 2015, Pearson's r = 0.64, n = 197).
compiled digital images of colour plates from del Hoyo et al. (2017)
and extracted colour values from nine body patches (nape, crown,
forehead, throat, upper breast, lower breast, shoulder, wing and 2.1.4 | Sexual dichromatism
tail, illustrated in Figure S1) using colorZapper v.1.4.6 (Valcu &
Dale, 2014) as in Dale et al. (2015). The method has been validated To capture the plumage colour dimorphism of species in which males
with spectrometric measurements of museum specimens (Dale and females have similar levels of elaboration but different colours,
et al., 2015; Delhey et al., 2019) and is commonly used in compara- we also computed sexual dichromatism (SDC) as the sum of the
tive analyses of plumage colouration and dimorphism (e.g. Carballo Euclidean distances in CIELAB space between homologous patches
et al., 2020; Dale et al., 2015; Miller et al., 2018; Webb et al., 2016). in males and females. As the difference between male and female
We computed colour elaboration for each plumage patch and each plumage colouration increases, SDC values become increasingly
sex according to Carballo et al. (2020), as the Euclidean distance in positive, independent of how elaborated the plumage colouration is,
CIELAB space between the patch and the centroid of the given patch or which of the sexes is more colourful. SDC values varied between
across species. Because in small datasets the centroid can be sen- 0 and 478 (scarlet tanager Piranga olivacea).
sitive to the presence of species with highly elaborate colours, we
chose as reference the centroid of the subset with the lower col-
our elaboration among the male and the female of each species. We 2.1.5 | Difference in colour diversity
computed the colour elaboration of each species and sex as the sum
of the distances obtained for the nine patches. Similar to the dimor- Because the variation of plumage colouration within patches is not
phism in body size, the sex difference in colour elaboration was then captured when plumage colouration is averaged for each patch, we
defined as the absolute difference between the colour elaboration also computed the colour diversity of each sex and species, as the
of the male and the female of a given species. The sex difference in average Euclidian distance in CIELAB space between a random 90%
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768 VALCU et al.
F I G U R E 2 Sex dimorphism in wing length (a, c, e) and sex difference in colour elaboration (b, d, f) for species with a different mating
system (a, b), parental contribution to incubation (c, d) and parental contribution to offspring provisioning (e, f). Colours denote the
frequency of extra-pair paternity expressed as the proportion of extra-pair broods.
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VALCU et al. 769
of the image pixels and the centroid of the image. We used 90% of frequency of EP offspring from 390 species and the frequency
the image pixels to introduce a small measurement error and thus of EP broods from 386 species (a total of 401 species from 91
avoid null values for species in which males and females are depicted families, representing 4% of the extant species and 47% of the
by a single image. We then defined sexual difference in colour diver- extant avian families). The dataset covered all 11 zoogeographi-
sity as the absolute difference between the colour diversity of the cal realms (Valcu et al., 2021).
male and the female of a given species. Values varied between 0 and c. Parental role asymmetry was scored for two components of
15.7 (Australian golden whistler Pachycephala pectoralis). parental care: incubation and offspring provisioning. Similar to
dimorphism, we initially did not differentiate between predom-
inant male and female care, and therefore assigned scores of 0
2.2 | Potential predictors of sexual dimorphism to species with relatively equal contributions, 1 to species with
mostly male or female care and 2 to species with male or female-
a. Social polygamy. Data on the social mating system were ob- only care. We subsequently accounted for the sex with a higher
tained from the species accounts in Birds of the World (Billerman investment in parental care in separate models (see below).
et al., 2020, sections “Breeding” and ‘Behaviour’, access date Scores are mostly based on information from the Birds of the
6/5/2021). The social mating system was classified as social World (Billerman et al., 2020, for additional data sources see
monogamy, polygyny, polyandry or polygynandry. Species be- Supplement Data). The dataset included, for the respective cat-
longing to multiple categories were assigned to intermediate egories, 148/29/224 species (incubation) and 351/35/15 species
categories based on the modifier ‘occasional’ (<5% of breeding (offspring provisioning).
attempts) and ‘regular’ (5–50% of breeding attempts), or when d. Cooperative breeding was scored as 0 (absent), 1 (occasional) or 2
these categories were explicitly specified. We scored the de- (present) based on data obtained from Cockburn (2006), updated
gree of social polygamy based on the type of mating system, on based on recent literature (see Supplement Data). The dataset
a 6-level scale from 0 to 5 as follows: 0 (‘monogamy’, ‘monog- included, for the respective categories, 275/37/89 species.
amy with occasional or regular polygynandry’, ‘polygynandry e. The median migration distance (km) of the species was obtained
with regular monogamy’, ‘polygynandry’), 1 (‘monogamy with from Dufour et al. (2020).
occasional polyandry or polygyny’), 2 (‘monogamy with regular f. Phylogeny. To control for non-independence due to shared an-
polyandry or polygyny’), 3 (‘polyandry or polygyny with regular cestry, we built a consensus phylogeny based on the posterior
monogamy’), 4 (‘polyandry or polygyny with occasional monog- distributions available from Birdtree.org (Jetz et al., 2012) and
amy’) and 5 (‘polyandry or polygyny’). We assigned ‘polygynan- used it to create a phylogenetic covariance matrix, as described
dry’ the same score as ‘monogamy’, because males and females in Valcu et al. (2021). This covariance matrix was included in the
of polygynandrous species experience comparable variation in Bayesian models.
social mating success and intensity of sexual selection, similarly
to monogamous species.
b. Extra-pair paternity was defined according to Valcu et al. (2021), 2.3 | Data analyses
as parentage occurring outside a social unit (pair or group) and
quantified as (1) the proportion of offspring in a population sired We used R version 4.1.2 (R Core Team, 2020) for statistical analysis.
by males outside the social unit (EP offspring) and (2) the propor- We ran hierarchical Bayesian models with the R package brms version
tion of broods or clutches containing at least one EP offspring or 2.16.3 (Bürkner, 2017) as described previously (Valcu et al., 2021).
extra-pair sired egg (EP broods). Lekking and promiscuous species Briefly, we investigated the relationship between sexual dimorphism
were not included, because they do not form pair bonds. Based and EPP using Bayesian phylogenetic Gaussian mixed models. Each
on EPP data from 401 bird species, we previously modelled the model included phylogeny as a random factor. We ran separate mod-
variation in the frequency of EPP within the species' breeding els for each of the two measures of the frequency of EPP (proportion
ranges using spatially explicit Bayesian models which accounted of EP offspring and proportion of EP broods). For each model, we ran
for the specific ecological context of each population. We then 5 chains of 5000 iterations (2500 warm-up iterations) and extracted
used these models to predict the proportion of EP broods and EP posterior distributions for all parameters, as in Valcu et al. (2021).
offspring for new locations covering the entire breeding range All models achieved convergence, with R-hat values of 1 or close
of each of the species (Valcu et al., 2021). The predicted pro- to 1 for all predictors (Gelman & Rubin, 1992). To test whether EPP
portions of EP broods and EP offspring reflect the geographical relates differently to sexual dimorphism in species with male-biased
variation of these variables within the species' breeding range vs. female-biased dimorphism, we updated the model by includ-
due to location (latitude, distance to breeding range boundary) ing the interaction between the proportion of EP broods and the
and environmental factors (seasonality) (Valcu et al., 2021). Here, direction of dimorphism. We report posterior means, the standard
we computed species values as the median proportion of EP deviation of the posterior distributions and the two-sided 95% cred-
offspring and EP broods predicted for each species (for details ible intervals of the posterior means (95% CI), as well as the prob-
see Valcu et al. (2021)). The dataset included estimates of the ability of direction (PD). PD is comparable to the frequentist p-value
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770 VALCU et al.
(Makowski et al., 2019), whereby PD values of 0.5 and 1 correspond

to p-values of 1 and 0, respectively (also reported).
We ln-transformed migration distance, wing length and body
mass to normalize their distributions. Dependent variables, continu-
ous predictors (wing length, body mass, EPP and migration distance)
and ordered factors (social polygamy, parental role asymmetry and
cooperative breeding) were scaled by subtracting the mean and di-
viding by the standard deviation. The partial correlation between
predictors varied between −0.22 (between cooperative breeding
and migration distance) and 0.43 (between social polygamy and sex
bias in offspring provisioning).
3 | R E S U LT S
First, we describe how different reproductive, social and life-history

traits explain between-species variation in sexual size dimorphism
(3.1.) and in plumage colour dimorphism (3.2.). We then explore how
the observed relationships vary between species with male-biased
or female-biased dimorphism (3.3.).
3.1 | Predictors of sexual size dimorphism
The results of the Bayesian phylogenetic models show that sexual

F I G U R E 3 Predictors of sex dimorphism in wing length and sex
dimorphism in wing length is associated positively with social po- difference in colour elaboration (model details in Tables S1 and S2).
lygamy, the proportion of EP broods, sex bias in incubation and
offspring provisioning and wing length, and negatively with migra- frequency of EPP, whereby species with a higher proportion of EP
tion distance (Figure 3; Table S1). Size-monomorphic species were broods differed more strongly in colour. The fixed factors explained
smaller, were more likely socially monogamous, had a low frequency 6% of the variance, while phylogeny explained 63%.
of EPP, migrated longer distances and males and females of these The difference in colour elaboration was strongly correlated with
species had a relatively equal contribution to incubation and off- both dichromatism (r = 0.86) and with the difference in colour diver-
spring provisioning. Species with higher levels of dimorphism in wing sity (r = 0.62). The effects of all predictors were similar when using
length were larger, had higher levels of polygamy and EPP, migrated dichromatism or the difference in colour diversity as measures of
shorter distances and one of the sexes had a comparatively higher plumage dimorphism (Figure S2b, Tables S4, S5). Results were also
parental investment. Cooperative behaviour had little effect on di- similar when using the proportion of EP offspring as a measure of
morphism in wing length. The fixed factors explained 25% of the the frequency of EPP (Figure S3, Tables S6, S7).
2
variance (marginal R ), while phylogeny explained 60%. Given the consistency of the results, we performed subsequent
Dimorphism in body mass and wing length were strongly cor- analyses using wing length dimorphism as a proxy for size dimor-
related (r = 0.61). When using sexual dimorphism in body mass as the phism, the sex difference in colour elaboration as a proxy for plum-
dependent variable, the direction of all predictors was consistent, age colour dimorphism and the proportion of EP broods as a measure
but the effect sizes were generally lower with the notable excep- of the frequency of EPP.
tion of body size which had a stronger effect (Figure S2a, Table S3).
Results were similar when using the proportion of EP offspring as a
measure of the frequency of EPP (Figure S3, Table S6). 3.3 | Sex-bias in size and plumage dimorphism
Among the 401 species of our sample, the species with male-biased
3.2 | Predictors of sexual dimorphism in plumage dimorphism outnumber those with female-biased dimorphism 4.9-
colouration fold in the case of wing length dimorphism and 1.6-fold in the case
of the sex difference in colour elaboration. The average dimorphism
The effects of most predictors on the difference in colour elabora- in wing length was similar in species with male-biased and female-
tion were small and had low PD values (Figure 3; Table S1). The only biased dimorphism (Figure 2a; Table S8). However, species with
clear predictor of the sex difference in colour elaboration was the male-biased colour elaboration were more dimorphic than species
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VALCU et al. 771
F I G U R E 4 The frequency of extra-

pair paternity in species with male-and
female-biased dimorphism in wing length
(a) and plumage colour elaboration (b)
(model details in Tables S10 and S11), and
interactions between the proportion of
broods with extra-pair paternity and the
direction of sex dimorphism in wing length
(c) and difference in plumage colour
elaboration (d) (male-biased vs. female-
biased) (model details in Tables S12
and S13).
with female-biased colour elaboration (Figure 2b; Table S9). Species care is provided predominantly or exclusively by one sex display a
with either male-biased wing length dimorphism or colour elabo- bias in dimorphism in wing length towards the opposite sex, that is,
ration had higher levels of EPP than species with either female- female-biased in species with male care and male-biased in species
biased wing length dimorphism or colour elaboration (Figure 4a,b; with female care (Figure 2c,e). The results also confirmed that nei-
Tables S10, S11). ther predominant male nor predominant female care are correlated
To discriminate between the effect of social polygyny (stronger with the sex difference in colour elaboration (incubation: Tables S20,
sexual selection on males) and social polyandry (stronger selection S21, offspring provisioning: Tables S24, S25).
on females), we ran the original models on two subsets of species We predicted that the frequency of EPP should correlate pos-
which included monogamous species and species with different de- itively with sexual dimorphism in species with male-biased dimor-
grees of either (1) polygyny or (2) polyandry. The results show that phism and negatively in species with female-
biased dimorphism
polyandry and polygyny have similar positive effects on dimorphism because EPP increases the intensity of sexual selection only in
in wing length (Tables S14, S15). Polyandry and polygyny had ef- males. The model including the interaction between the propor-
fects of opposite signs on the sex difference in colour elaboration tion of EP broods and the direction of dimorphism confirmed that
(positive for the former and negative for the latter). However, both the proportion of EP broods was positively associated with plum-
effects were small and had low PD values (Tables S16, S17). age dimorphism in species with male-
biased colour elaboration,
Similarly, to discriminate between species in which parental care but negatively in species with female-
biased colour elaboration
is undertaken predominantly by either males or females, we ran the (Figure 4d; Table S13). However, the association between sexual size
original models on two subsets of species which included species dimorphism and the frequency of EPP was positive in species with
with bi-parental care and species with either (1) predominantly male both male-and female-biased dimorphism in wing length (Figure 4c;
or (2) predominantly female incubation (Tables S18–S21) or offspring Table S12).
provisioning (Tables S22–S25). The results confirmed that predom-
inant male or predominant female parental care are positively cor-
related with dimorphism in wing length. The effect of predominant 4 | D I S C U S S I O N
male incubation on wing length dimorphism was not supported sta-
tistically (Table S18) but was based on a sample of only 8 species Sexual dimorphism evolves primarily as a consequence of sex
with predominant male incubation. Thus, species in which parental role asymmetry and reflects the adaptations of the sexes to their
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772 VALCU et al.
reproductive roles (Fairbairn et al., 2007). However, dimorphism in if males engage in aerial acrobatic displays to attract extra-p air
different traits may only weakly correlate (Székely et al., 2007). For females (Székely et al., 2000, 2004), or if females indirectly ben-
example, in our study, the correlation between sexual size dimor- efit from producing smaller male offspring and therefore choose
phism and dichromatism was only rSpearman = 0.18, suggesting that smaller extra-p air partners (Mueller, 1989; Sonerud et al., 2014).
different mechanisms are responsible for the evolution of these dif- So far, the association between EPP and body size dimorphism
ferent forms of dimorphism. Because traits under sexual selection has received limited support. An early study found no evidence
can also be under viability or fecundity selection, the actual form of a link between body mass dimorphism and the frequency of
and extent of sexual dimorphism can only be understood within the EP broods (Owens & Hartley, 1998). Dunn et al. (2001) later con-
broader frame of social selection (West-Eberhard, 1983). Previous firmed that relative testis size, a strong correlate of the frequency
studies have already provided evidence that different forms of di- of EPP (Moller & Briskie, 1995), was not associated with body mass
morphism are associated with different reproductive and life-history dimorphism, but showed that it was positively associated with di-
traits (Dunn et al., 2001; Owens & Hartley, 1998). Our results con- morphism in wing and tail length. In line with these results, we
firm that dimorphism in wing length and colour elaboration are as- found limited evidence for an association between the proportion
sociated with different reproductive, social and life-history traits, of EP broods and sexual dimorphism in body mass, but strong
and may thus evolve independently, as a consequence of different evidence for a positive association with wing length dimorphism
selective pressures. Moreover, our results strongly support a role (Figure 3).
for extra-pair mating in both the evolution of size and plumage We predicted that EPP should lead to higher dimorphism in spe-
dimorphism. cies with male-biased dimorphism but lower dimorphism in species
with female-biased dimorphism because EPP mainly increases the
variance in male reproductive success. Contrary to this prediction,
4.1 | Extra-pair paternity and sexual higher frequencies of EPP were associated with higher levels of
size dimorphism wing length dimorphism, in both species with male-and female-
biased dimorphism in wing length (Figure 4c). Thus, although species
In birds, large body size can confer an advantage in the competi- with female-biased size dimorphism had overall lower levels of EPP
tion for mates and other resources, reduce predation risk or in- (Figure 4a), within this lower range, higher levels of EPP were associ-
crease survival in harsh environments through better temperature ated with higher levels of size dimorphism (Figure 4c). In our dataset,
regulation and higher resilience to variation in resource abundance species with female-biased wing length dimorphism are more often
(Blanckenhorn, 2005). However, large body size also entails costs, socially polyandrous (18% vs. 5% in species with male-biased dimor-
for example, related to high energy requirements for maintenance, phism), and females of polyandrous species show steeper Bateman
flight and reproduction, reduced agility, temperature regulation or gradients (Fromonteil et al., 2023; Kvarnemo & Simmons, 2013;
late reproduction (Blanckenhorn, 2005). Small body size can facili- Parker & Birkhead, 2013). In socially polyandrous species EPP can
tate flight agility in predators (Mueller, 1989; Sonerud et al., 2014) be a by-product of the mating system because females use extra-
and in species in which males exhibit acrobatic displays (Székely pair copulations as a strategy to acquire additional care-giving males
et al., 2000, 2004). Body size is therefore driven by multiple factors (Emlen et al., 1998; Krietsch et al., 2022; Safari & Goymann, 2018).
such as climate (Olson et al., 2009), distribution and predictability In this case, larger females could have an advantage in the competi-
of resources (Olson et al., 2009) and the intensity of sexual selection for males. Higher levels of EPP could also lead to higher female-
tion (Blanckenhorn, 2000). Sexual size dimorphism evolves primar- biased size dimorphism in species in which males engage in aerial
ily as a consequence of sex-bias in the strength of sexual selection acrobatic displays to attract extra-pair females if a smaller body size
through intrasexual competition for mates, but mate choice, inter- has a competitive advantage for males. In raptors, in which males
sexual niche divergence and adaptation to different parental roles undertake the larger part of offspring provisioning, females may also
can also lead to size dimorphism (Dunn et al., 2001; Fairbairn, 1997) choose smaller extra-pair partners because smaller body size facili-
(see Section 4.3). Evolutionary changes in the direction of size di- tates efficient hunting and is therefore a desirable trait to pass on to
morphism most often involve changes in male body size, probably their male offspring (Sonerud et al., 2014).
because male growth is more plastic than female growth, while fe-
male size is both more heritable and under stronger fecundity selec-
tion (Kalmbach & Benito, 2007; Lindenfors et al., 2003). Across bird 4.2 | Extra-pair paternity and sexual dimorphism in
species, males are more often the larger sex (this study; Friedman & plumage colouration
Remeš, 2016).
Larger size could represent an advantage for males seeking Plumage colouration has multiple functions, ranging from camou-
extra-p air copulations, either if they engage in physical compe- flage, temperature control and species recognition to mate choice
tition for females or if it helps them provide direct or indirect and signalling of social status and condition. Colouration fulfils
benefits which are sought after by females (Blanckenhorn, 2000). similar roles in males and females (Nolazco et al., 2021) and medi-
However, smaller size could also be an advantage, for example, ates both mate choice and intrasexual competition for resources,
|
VALCU et al. 773
either related to reproduction or not (Tobias et al., 2012). However, higher frequencies of EPP were associated with larger differences in
elaborate plumage colouration can also have drawbacks for exam- plumage colour elaboration in species with male-biased plumage di-
ple related to physiological costs of production and maintenance, morphism, and with smaller differences in those with female-biased
a trade-
off with immune function or increased predation risk dimorphism (Figure 4d). When males are the more colourful sex, se-
(Delhey, Peters, & Kempenaers, 2007). The evolution of plumage lection on males to become more colourful to increase extra-pair
colouration is thus driven by a variety of factors such as climate siring success, or selection on female crypsis to facilitate extra-pair
(Delhey et al., 2019; Friedman & Remeš, 2017), vegetation (Delhey copulations, can lead to larger differences between males and fe-
et al., 2019; Friedman & Remeš, 2017), life history (Dale et al., 2015; males in colour elaboration. Conversely, when females are the more
Delhey et al., 2021) and the intensity of sexual selection (Dale colourful sex, similar mechanisms would result in smaller differences
et al., 2015; Thibault et al., 2022). Sexual dimorphism in plumage in colour elaboration between the sexes.
colouration is believed to evolve primarily as a consequence of sex- After controlling for a strong phylogenetic effect, extra-pair mat-
bias in the strength of sexual selection, through mate choice (Dunn ing emerges as the only driver of plumage colour dimorphism, with
et al., 2001, 2015; Møller & Birkhead, 1994; Owens & Hartley, 1998; little or no contribution of other reproductive or life-history traits
Thibault et al., 2022). However, other factors causing different in- (see Section 4.4). Technical limitations in the biologically meaning-
tensities of selection on plumage colour in males and females (e.g. ful quantification of plumage colour dimorphism (see Section 4.5)
diet, habitat or parental roles) can also potentially lead to plumage could explain why the fixed factors (marginal R 2) explained only 6%
dimorphism (see Section 4.4). of the variance in the difference in colour elaboration as compared
EPP has long been recognized as an important predictor of plum- to 25% of the variance in wing length dimorphism. However, the
age dimorphism (Møller & Birkhead, 1994; Owens & Hartley, 1998; multivariate model explained a substantial 51% (conditional R 2) of
Thibault et al., 2022). In support of these previous results, we found the overall variance in the difference in colour elaboration, similar
that the proportion of EP broods was the single predictor of the dif- to the 58% explained from the overall variance in wing length di-
ference in colour elaboration between the sexes (Table S1). Female morphism. Plumage colour is determined by various mechanisms
choice for extra-
pair partners may intensify sexual selection in and previous research has shown that melanin-, carotenoid-, and
males, and this could lead to the evolution of more colourful males, structurally-based dimorphism show different patterns of covaria-
and hence to higher plumage colour dimorphism (Dunn et al., 2001; tion with different aspects of sexual and parental behaviour (Owens
Owens & Hartley, 1998; Thibault et al., 2022). Alternatively, more & Hartley, 1998). Fully understanding the evolution of plumage di-
elaborate male colouration could also evolve through increased morphism may thus require further study of each of these forms of
competition between males for extra-pair mating opportunities, if plumage dimorphism.
plumage colour signals male dominance (Santos et al., 2011). Effects
of inter-or intrasexual competition on male plumage colouration
are difficult to discriminate experimentally and are non-mutually 4.3 | Other evolutionary drivers of sexual
exclusive because plumage colouration can indicate both male qual- size dimorphism
ity to choosy females and male status to competing males (Lyon &
Montgomerie, 2012). There are however indications against the If a larger (or smaller) body size has a competitive advantage in the
latter mechanism, at least in some species in which females resist sex with higher competition for mates, this should lead to greater
extra-pair copulations. For example, in the mallard (Anas platy- sexual size dimorphism in socially polygamous species (Dunn
rhynchos), access to extra-pair females is gained primarily through et al., 2001; Owens & Hartley, 1998). Conversely, because males
competition between males, but extra-pair siring success was not and females of socially monogamous species experience relatively
associated with male dominance or with male phenotype in this equal strength of sexual selection, these species are expected to
species (Cunningham, 2003; Kreisinger et al., 2010). An alternative be monomorphic. Comparative studies have, indeed, shown that
hypothesis proposes that higher levels of EPP would lead to the evo- intense mating competition can explain dimorphism in body mass
lution of cryptic colouration in females if female crypsis facilitates (Dunn et al., 2001; Owens & Hartley, 1998; Székely et al., 2007),
engagement in extra-pair copulations while avoiding retaliation of wing length (Dunn et al., 2001; Székely et al., 2007, 2000), tarsus
the social partner in the form of physical aggression, withdrawal length (Székely et al., 2007), tail length (Dunn et al., 2001; Székely
of parental care or divorce (Lifjeld et al., 2019). While our analysis et al., 2007) and bill length (Székely et al., 2007). Our results are in
cannot discriminate between these hypotheses, there is evidence full agreement with these findings in showing that socially monoga-
that increased sexual selection can lead to plumage colour dimor- mous species are more likely size monomorphic, while species with
phism both through increased plumage colour elaboration in males increasing degrees of polygamy display increasingly strong dimor-
(Dale et al., 2015; Møller & Birkhead, 1994; Thibault et al., 2022) phism in wing length (Figure 3) and in body mass (Figure S2). In the
and through reduced plumage colour elaboration in females (Dale suborder Charadrii, male-biased dimorphism has increased following
et al., 2015; Lifjeld et al., 2019). evolutionary changes towards socially polygynous mating systems,
In support of our prediction that EPP should have opposite ef- while female-biased dimorphism has increased after transitions to-
fects depending on the direction of the dimorphism, we found that wards socially polyandrous mating systems (Lindenfors et al., 2003).
|
774 VALCU et al.
Our results corroborate this pattern showing that across spe- were scored together) (Du Plessis et al., 1995). Dunn et al. (2001)
cies, high mating competition among males (polygyny) predicts categorized cooperative behaviour as one of six mating systems (106
strong male-biased size dimorphism and high mating competition of 1031 species) and found that species breeding cooperatively had
among females (polyandry) predicts female-biased size dimorphism lower dimorphism in wing, tail and body mass compared to species
(Tables S14, S15, Figure 2a,b). with other breeding systems. A later study showed that among 45
Sexual size dimorphism is also associated with parental role species of African starlings with male-biased dimorphism in wing
asymmetry, whereby species in which males and females have a length, cooperative behaviour was associated with lower wing length
relatively equal contribution to parental care are more monomor- dimorphism (Rubenstein & Lovette, 2009). Although the direction
phic, while increased investment in parental care of one of the sexes of the effect concurred with these previous results, we found poor
leads to higher dimorphism in wing length (Figure 3) and in body statistical support for a link between cooperative behaviour and di-
mass (Figure S2). It has previously been shown that sex-bias in provi- morphism in wing length. This could reflect the limited availability
sioning leads to dimorphism in body mass (Owens & Hartley, 1998), of EPP data in species of the Afrotropical realm, where cooperative
while female-only incubation was associated with dimorphism in tail breeding is most common (Cockburn, 2006). Alternatively, the nega-
and wing length (Dunn et al., 2001). Our results further suggest that tive correlation between cooperative breeding and size dimorphism
predominant female care leads to male-biased wing length dimor- described in Afrotropical birds (Du Plessis et al., 1995; Rubenstein &
phism, while predominant male care leads to female-biased wing Lovette, 2009) may not generalize across species but vary both de-
length dimorphism (Figure 2c,e, Tables S18, S19, S22, S23). Parental pending on the male and female sex-roles and on the sex of the help-
role asymmetry can lead to higher size dimorphism either through ers. While this is beyond the scope of our study, the link between
freeing the non-caring sex from the constraints imposed by parental cooperation and sexual dimorphism deserves further investigation.
care or by segregating the ecological niches of the caring and non- In migratory birds, early arrival at the breeding grounds can con-
caring sex. For example, a higher contribution to offspring provi- fer a competitive advantage to the sex with the higher variance in re-
sioning can select for efficient hunting and lower flight costs which, productive success. Natural selection should favour larger size in the
particularly in predators, leads to smaller size in the provisioning sex early arriving sex because early migration is associated with harsher
(Mueller, 1989; Sonerud et al., 2014). Offspring diet can potentially environmental conditions, in which body size can confer a survival
mediate such an effect, particularly when it deviates from the typical advantage. It has therefore been proposed that migration should fa-
adult diet. Parental role asymmetry and prey size can for instance vour the evolution of size dimorphism (Weatherhead & Clark, 1994).
explain female-biased wing length dimorphism in raptors (Sonerud At least in some species, wing length dimorphism is positively as-
et al., 2014), and we expect that this mechanism could also extend to sociated with the difference in arrival dates of males and females
other groups. In species where the non-incubating parent provisions (Kissner et al., 2003, but see Rubolini et al., 2004). However, a com-
the incubating parent, the same adaptations required for offspring parative analysis investigating the link between migratory behaviour
provisioning could also arise in the non-incubating sex. and sexual size dimorphism (scored as present or absent) found no
Several studies have investigated the link between size dimor- evidence for an association with either dimorphism in wing length or
phism and cooperative behaviour, that is, species in which more in body mass (Dunn et al., 2001). In contrast to the initial predictions,
than two individuals provide parental care at a single nest or brood we found that both wing length and body mass dimorphism decline
(Arnold & Owens, 1999; Hatchwell & Komdeur, 2000). Although co- with migration distance, indicating that adaptations to long-distance
operative behaviour takes different forms across species, it is gener- migration may prevail over those related to early arrival at the breed-
ally accepted that cooperation evolves in life-history and ecological ing grounds. The discrepancy with the results of Dunn et al. (2001)
contexts that lead to high competition for breeding opportunities could reflect the differences in the method of scoring migratory
(Hatchwell & Komdeur, 2000). In non-cooperative species, females behaviour.
are often the limited resource for which males compete (Bateman's The relationship between sexual size dimorphism and body size
principle), and thus experience lower competition for mates, lower is described by Rensch's rule, whereby ‘in larger species, the rela-
skew in reproductive success and lower intensity in sexual selective sexual difference in size is generally more significant than in
tion (Hauber & Lacey, 2005). In cooperatively breeding species with small species of the same kin group’ (Rensch, 1950). Fairbairn (1997)
non-reproducing ‘helpers’, a proportion of individuals of one or both proposed that larger sizes facilitate the evolution of sexual size
sexes temporarily forgo reproduction, which increases the skew in dimorphism, by increasing the probability of sexual selection act-
reproduction success in the sex of the helpers. Because this effect ing on body size rather than on other traits. As originally recog-
is stronger in females compared to males (Hauber & Lacey, 2005), nized by Rensch, the rule does not apply to all lineages (Webb &
cooperatively breeding species with conventional sex roles should Freckleton, 2007). However, many avian groups exhibit allometries
experience lower sex bias in sexual selection and therefore display in body mass, wing length, tarsus length, bill length and tail length
lower sexual dimorphism (Rubenstein & Lovette, 2009). This hypoth- consistent with the rule (Dale et al., 2007; Székely et al., 2007; Webb
esis has been supported by an early study on South African birds (217 & Freckleton, 2007). In agreement with these results, we found
species) which showed that obligate cooperative breeding species that both dimorphism in wing length (Figure 3) and in body mass
(25 species) are more monomorphic (size and plumage dimorphism (Figure S2) increase with body size (wing length and body mass,
|
VALCU et al. 775
respectively). The effect was stronger for body mass dimorphism, in species nesting at shrub level (not in those nesting on the ground
which can explain why previous studies found evidence for the for- or at tree level), which are at greatest risk of nest predation (Dunn
mer association, but not for the latter (Dunn et al., 2001). et al., 2015). With our dataset, we found no evidence that sex-biased
investment in incubation or offspring provisioning led to the evolu-
tion of plumage colour dimorphism, after controlling for potentially
4.4 | Other evolutionary drivers of sexual confounding variables and phylogeny (all species: Table S1; species
dimorphism in plumage colouration with predominant male care: Tables S20, S24; species with predom-
inant female care: Tables S21, S25). However, the distribution of the
Sexual dimorphism in plumage colouration has been linked to vari- raw data (Figure 2d,f) suggests that the lack of statistical support
ous reproductive and life-
history traits (Dale et al., 2015; Dunn may be due to the limited sample size.
et al., 2001, 2015). However, EPP was not considered in any of these Migration could lead to plumage colour dimorphism if intense co-
studies. After controlling for EPP, we found little support for a link louration in the sex with higher competition for mates would be linked
between plumage colour dimorphism and other traits. to a higher likelihood of obtaining a mate faster and hence to earlier
Previous studies have reported a positive association between breeding, which might be particularly relevant in migratory species
dimorphism in plumage colouration and social polygyny (Dale with short breeding seasons (Fitzpatrick, 1994; Hamilton, 1961).
et al., 2015; Dunn et al., 2001, 2015; Irwin, 1994). We found no Alternatively, higher plumage colour dimorphism could evolve in mi-
statistical support for an association between plumage colour di- gratory species if reduced female colouration lowers predation risk
morphism and either polygamy in general (Table S1), or the degree during migration, or if the intensity of selection for social signalling is
of polygyny (Table S16) or polyandry (Table S17), even though the lower among females at high latitudes (Friedman et al., 2009; Simpson
direction of the effects was consistent with earlier results. The et al., 2015). Although a link between migration and plumage coloura-
differences in results could derive from the method of scoring the tion has been clearly established (Dale et al., 2015; Delhey et al., 2021;
mating system (see also the discussion above regarding coopera- Dunn et al., 2015), the evidence supporting a link with plumage colour
tive breeding) or from the sample of species included in the analy- dimorphism is limited to specific avian groups (Friedman et al., 2009;
sis. We note, however, that other studies which, like ours, included Simpson et al., 2015). In studies with broader phylogenetic cover-
the frequency of EPP as a predictor in multivariate analyses, also age, this association was either inferred solely from single predictor
found no support for an association between plumage dimor- models (Dale et al., 2015) or was not supported statistically (Dunn
phism and the mating system (Møller & Birkhead, 1994; Owens & et al., 2001, 2015). While we did not investigate the effect of migra-
Hartley, 1998). tory behaviour on male and female plumage colouration, our results
Cooperative breeding is predicted to increase plumage coloura- concur with the latter studies in finding no association between mi-
tion in females and thus decrease plumage dimorphism, at least gration and plumage colour dimorphism.
in species with male-biased dimorphism (Hauber & Lacey, 2005; Recent studies have revealed that in some avian groups there is a
Rubenstein & Lovette, 2009). A study on almost 2500 passerine negative association between plumage colour dimorphism and body
species has confirmed both the effect on female plumage coloura- size. Both in passerines (Dale et al., 2015) and in parrots (Carballo
tion and that on plumage dimorphism (Dale et al., 2015). However, et al., 2020), larger species are less dichromatic than smaller species,
the opposite effect was reported by Dunn et al. (2015), who scored despite having more elaborate colours. Our results suggest that this
cooperative behaviour as a distinct mating system in 977 species effect may not occur in other groups. Similar to other studies with
covering 79% of avian orders and found that dimorphism in plum- broader phylogenetic coverage (Dunn et al., 2001, 2015; Owens &
age brightness and hue are higher in cooperatively breeding species. Hartley, 1998), we found no association between plumage colour di-
Dunn et al. (2015) considered this effect to be a consequence of the morphism and body size (Figures 3, S2b).
higher EPP rates in these species. We found no evidence that coop-
erative behaviour is associated with plumage dimorphism (Figure 3)
but cannot exclude that a broader coverage of species could reveal 4.5 | Limitations of the study
such an effect.
Plumage colour dimorphism could also evolve as a consequence The primary limitation of this study is the availability and qual-
of parental role asymmetry, for example when selection has fa- ity of published data. Firstly, the dataset includes only 401 species
voured a more cryptic plumage in the caring sex. Several studies for which the frequency of EPP has been measured in wild popula-
supported this prediction showing that female-only care was asso- tions. Because EPP can only be defined in species that form social
ciated with stronger plumage colour dimorphism (Dale et al., 2015; bonds, our dataset necessarily excludes lekking species and species
Dunn et al., 2001, 2015; Owens & Hartley, 1998). However, so far with a promiscuous mating system. These species typically experi-
the evidence is not conclusive, because this association was either ence intense sexual selection and display strong sexual dimorphism.
found in single-predictor models (Dale et al., 2015) and could not be Secondly, although dimorphism in both size and plumage colouration
confirmed after controlling for phylogenetic relatedness among spe- may vary geographically within the range of a species (Badyaev, 1997;
cies (Dunn et al., 2001; Owens & Hartley, 1998), or it was found only Blondel et al., 2002; Fang et al., 2022), for the majority of species data
|
776 VALCU et al.
are not available at the population level, hence the values used here Our results thus clearly support a role for EPP in the evolution of
are species-level estimates. Thirdly, some potentially relevant predic- both plumage colour and body size dimorphism. Although the actual
tors could not be included in the analyses (e.g. sex-bias in offspring mechanisms responsible for the effect of EPP on sexual dimorphism
defence, sex-bias in the timing of parental care (diurnal/nocturnal), may differ among species (e.g. species with male-vs. female-biased
breeding habitat, nest type and adult and offspring diet) because dimorphism, with different mating systems or with different parental
high-quality data were not available for all species in the dataset. To roles), the proportion of EP broods is the only variable that predicts
gain further insight into the link between EPP and sexual dimorphism, dimorphism in both wing length and colour elaboration. Importantly,
we need data on levels of EPP and on life-history traits from more the size of the EPP effect is comparable to that of social polygamy
species or from more populations per species. and sex-bias in parental care, two other factors linked to the inten-
Another type of limitation comes from the method of scoring sity of sexual selection.
plumage colouration using handbook plates. First, birds can per-
ceive colours that humans cannot (Cuthill, 2006), therefore even AU T H O R C O N T R I B U T I O N S
the most accurate colour plates are only a partial representation Mihai Valcu: Conceptualization (equal); data curation (equal); formal
of the avian plumage colouration. Nevertheless, scores based on analysis (equal); investigation (equal); methodology (equal); writing –
plates are highly correlated with UV–V is measurements of mu- review and editing (equal). Cristina Valcu: Conceptualization (equal);
seum specimens (Dale et al., 2015; Delhey et al., 2019) and hence data curation (equal); formal analysis (equal); investigation (equal);
should lead to reliable estimates of plumage dimorphism. Second, methodology (equal); project administration (equal); visualization
we expect that using colour plates underestimates dichromatism (equal); writing –original draft (equal); writing –review and editing
in species with subtle colour differences because for some species (equal). Bart Kempenaers: Conceptualization (equal); formal analysis
males and females are depicted by a single image. Independent (supporting); funding acquisition (lead); investigation (supporting);
of the method of scoring plumage colour, colour perception often resources (lead); supervision (lead); writing –original draft (support-
depends on the environment (Johnson & Burley, 1998) and is ing); writing –review and editing (supporting).
often perceived differently by conspecifics and predators (Håstad
et al., 2005), aspects which cannot be considered here, but will AC K N OW L E D
G E M E N T S
influence selection on colour. Finally, different types of selection We thank Kaspar Delhey for providing data on the mating system
may act with different intensities on different colours (Badyaev and for helpful comments on the manuscript, and John B. Dunning
& Hill, 2000; Owens & Hartley, 1998) or on colours of different for providing an update of the CRC handbook of avian body mass
body parts. In many species, sexual selection targets specific body data. Additional body size data were kindly provided by Cássia Alves
parts which are presented during courtship display, which may not Lima Rezende, Xinkang Bao, Craig Barnett, Pedro Blendinger, Jim
be appropriately captured on handbook plates or have a limited Briskie, Chang-
Yong Choi, Víctor Cueto, Rosemary Grant, Simon
contribution to total body colouration. The link between EPP and Griffith, Shoji Hamao, Barbara Kus, Jin-Won Lee, Jianqiang Li, Wei
sexual dichromatism of specific body parts deserves further inves- Liang, Javier Lopez de Casenave, Miguel Angelo Marini, Thomas
tigation, as does the link between EPP and dichromatism arising Martin, Yitzchak Ben Mocha, Ângela Ribeiro, María Cecilia Sagario,
from different mechanisms of colour production. Lulu Stader, Diego Sustaita, Masaoki Takagi, Irene van den Heuvel,
Sandra Vehrencamp, Vera Voronova and Miya Warrington. Open
Access funding enabled and organized by Projekt DEAL.
5 | CO N C LU S I O N
C O N FL I C T O F I N T E R E S T S TAT E M E N T
Sexual dimorphism reflects both the species' evolutionary history as The authors have no conflict of interest to declare.
well as adaptations of the sexes to their reproductive and parental
roles. We show that dimorphism in body size and plumage coloura- DATA AVA I L A B I L I T Y S TAT E M E N T
tion are weakly correlated and associated with different reproduc- Computer code and data are available at https://osf.io/vkmxt/.
tive, social and life-history traits, suggesting that different forms of
dimorphism have evolved independently as a consequence of dif- ORCID
ferent selective pressures. Size dimorphism appears to be driven by Mihai Valcu https://orcid.org/0000-0002-6907-7802
multiple factors, probably because body size is adapted to fulfil mul- Bart Kempenaers https://orcid.org/0000-0002-7505-5458
tiple functions. Specifically, dimorphism in wing length is predicted
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Valcu. Extra Pair Paternity and Sexual Dimorphism in Birds

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Received: 19 October 2022 Revised: 1 February 2023 Accepted: 6 February 2023

Extra-pair paternity and sexual dimorphism in birds

Mihai Valcu | Cristina Valcu | Bart Kempenaers

Department of Behavioural Ecology

Mihai Valcu and Cristina Valcu contributed equally to this work.

(Makowski et al., 2019), whereby PD values of 0.5 and 1 correspond

First, we describe how different reproductive, social and life-history

3.1 | Predictors of sexual size dimorphism

The results of the Bayesian phylogenetic models show that sexual

F I G U R E 4 The frequency of extra-

You might also like

Valcu. Extra Pair Paternity and Sexual Dimorphism in Birds

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

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Did you find this document useful?

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Copyright:

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Valcu. Extra Pair Paternity and Sexual Dimorphism in Birds

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Copyright:

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Received: 19 October 2022 Revised: 1 February 2023 Accepted: 6 February 2023

Extra-­pair paternity and sexual dimorphism in birds

Mihai Valcu | Cristina Valcu | Bart Kempenaers

Department of Behavioural Ecology

Mihai Valcu and Cristina Valcu contributed equally to this work.

(Makowski et al., 2019), whereby PD values of 0.5 and 1 correspond

First, we describe how different reproductive, social and life-­history

3.1 | Predictors of sexual size dimorphism

The results of the Bayesian phylogenetic models show that sexual

F I G U R E 4 The frequency of extra-­

You might also like

Extra-pair paternity and sexual dimorphism in birds

First, we describe how different reproductive, social and life-history

F I G U R E 4 The frequency of extra-