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. 2021 Sep 8;17(9):20210283. doi: 10.1098/rsbl.2021.0283

Colourful traits in female birds relate to individual condition, reproductive performance and male-mate preferences: a meta-analytic approach

América Hernández 1,2,✉, Margarita Martínez-Gómez 3,4, René Beamonte-Barrientos 4, Bibiana Montoya 4,✉
PMCID: PMC8424322  PMID: 34493064

Abstract

Colourful traits in females are suggested to have evolved and be maintained by sexual selection. Although several studies have evaluated this idea, support is still equivocal. Evidence has been compiled in reviews, and a handful of quantitative syntheses has explored cumulative support for the link between condition and specific colour traits in males and females. However, understanding the potential function of females' colourful traits in sexual communication has not been the primary focus of any of those previous studies. Here, using a meta-analytic approach, we find that evidence from empirical studies in birds supports the idea that colourful female ornaments are positively associated with residual mass and immune response, clutch size and male-mate preferences. Hence, colourful traits in female birds likely evolved and are maintained by sexual selection as condition-dependent signals.

Keywords: female ornaments, sexual selection, melanins, carotenoids, structural coloration, male-mate choice

1. Introduction

Although females of many species exhibit conspicuous traits, research on the evolution of extravagant characters through sexual selection has mainly focused on male ornaments [1]. Hypotheses explaining the occurrence of female ornamentation propose that female ornaments evolved because they share genetic architecture with male ornaments, confer privileges during the competition for ecological resources or are advantageous during sexual selection [2–5]. Comparative studies indicate that selective pressures favoured the evolution of female ornamentation, but whether those pressures arise mainly from natural selection, female–female competition or male-mate preferences is unclear [1,6,7]. There is growing evidence that male-mate choice has played a role in the evolution of female ornamental traits [5,8–12], but the overall strength of that evidence has seldom been systematically evaluated.

There are several (non-exclusive) scenarios where sexual selection is expected to favour the evolution of female ornaments, for instance, when the variation in females’ reproductive value is large and is related to their ornamentation; when there are more females available than males can mate with and/or mating with one female reduces the opportunity to mate with another; and under reversed sex roles [11–15]. Female ornamentation is also expected in the context of mutual mate choice, where acquiring information from ornaments about the potential direct or indirect benefits of mating with a particular partner may be beneficial to both sexes, such as in species with biparental care and serial monogamy [16–18]. However, male-mate choice has been shown to occur even in polygynous species, as evidenced by differential sperm transfer depending on a female's attractiveness [19–21].

Birds exhibit striking colours, and the role of male coloration as a condition-dependent signal has been extensively studied in this taxon [22–24]. However, females have undergone evolutionary change more frequently than males, and changes have often been towards more ornamented traits in females, suggesting that selection may have acted on male and female ornaments independently [25]. Hence, birds may be a good model for studying the evolution of female ornamentation. Coloured avian traits are mainly produced by carotenoids, melanin and tissue structures [23,26]. These three types of coloration depend on different underlying mechanisms and therefore may communicate different information [25]. Carotenoid coloration depends on individuals' capacity to acquire, metabolize and store carotenoids from their diet [27] and have been positively linked to immune competence and oxidative balance ([28–39], but see [40]). Melanin-based colours are ubiquitous in birds; they rely on a synthesis pathway that releases cytotoxic compounds and requires metal cofactors that are functionally linked to other physiological functions [23]. Frequently, melanins have been associated with social status, but what type of condition-dependent information melanin-based colours may provide is less clear [41,42]. Finally, colours that result from the interaction between light and the arrangement of the nanostructure (i.e. array of melanosomes and keratin matrix) and microstructure of tissues (i.e. array of barbs or barbules) have received comparatively less attention in this context [43–46] but a recent meta-analysis found them to be correlated to residual body mass and immune function [47]. Whether these different colour displays are condition-dependent sexually selected signals used by males to evaluate females in a way that is analogous to female-mate choice is still under debate [18,48–52].

Here, using a meta-analytic approach, we evaluate the available evidence from published studies assessing the idea that conspicuously coloured traits, in female birds, have evolved through sexual selection as condition-dependent signals. We expect female colour traits to be positively associated with the female condition, reproductive performance and male-mate preferences.

2. Methods

A systematic search of the literature was performed using the PRISMA method (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) [53]. We looked for literature using the Google Scholar and Web of Science search engines, using the keywords: ‘female bird ornament’, ‘female bird ornamentation’, ‘female bird traits’, ‘female bird quality’, ‘female bird condition’, ‘female bird attractiveness', ‘female bird colour’, ‘female bird color’, ‘female bird coloration’, ‘male bird choice’ and ‘male bird preference’. References within papers were also checked. The last search was conducted on 15 October 2020.

We excluded studies that were missing data on statistical values, did not provide independent estimates for each sex or did not specify the type of coloration analysed. We detected 83 studies in our search, 59 of which satisfied the inclusion criteria (electronic supplementary material, figure S1, [54]). Of the 47 total species (eight species were used in more than one study), 42 had a socially monogamous mating system, four were facultatively polygamous and one was polygamous. Carotenoid-dependent ornaments were present in 23 species, melanin-based in 18 and structural colorations in 11 (electronic supplementary material, table S1). In the studies included in the meta-analyses, coloration was originally estimated using the number and/or size of coloured structures/patches, spectrophotometry, digital image analysis (RGB or LBA) and visual rank scales (colour charts and visual rank score).

Using independent meta-analyses, we evaluated the evidence of an association of colourful female ornaments with the condition, reproductive performance and male preferences (see below). Studies assessing more than one of these associations were included in each meta-analysis that applied. Effect sizes for quality and reproductive success were analysed as Pearson's correlation coefficients (r). When this coefficient was not directly available from papers (i.e. different statistics were reported, such as F, t and χ2), reported values were transformed to correlation coefficients following Rosenberg's formulae [55]. Pearson's coefficients were subsequently transformed to Fisher's z-values (Zr) for statistical analyses ([56], see equations in the electronic supplementary material). All effect sizes were weighted using the inverse of the sampling variance [57,58]. Effect sizes for male preferences were reported as Hedges' g, calculated from Pearson's coefficients (reported statistics were transformed when necessary, see above) [56], and weighted using the g’ variance ([56], see equations in the electronic supplementary material).

Three moderators were considered in the model evaluating the association between female colour and condition: condition proxy (residual body mass, immune response—humoral or cellular—and parasite load), ornament type (feathers or integuments) and coloration type (carotenoid-dependent, melanin-based or structural). In the model evaluating the association between female colour and reproductive performance, we used the same ornament type and coloration type moderator variables but replaced the condition proxy with a reproductive performance proxy (laying date, clutch size or fledging success). When the clutch size and fledging success were assessed in the same study, only fledging success was considered. In the analyses exploring the relationship between female colour and male mating preferences, only four effect sizes were available for melanin-based and structural colours (one and three, respectively), so we fit this model including effect sizes only from studies evaluating carotenoid-dependent coloration (n = 11). The ornament type (feathers or integuments) was included as a moderator.

In the case that two or more effect sizes were available from a single paper testing the same hypothesis and using the same ornament type and coloration (e.g. two carotenoid-dependent feather patches), those effect sizes were averaged to avoid overrepresentation. In studies that contained multiple effect sizes from different ornament or coloration types (e.g. one carotenoid-dependent feather patch and one melanin-based integument patch), we included each of the effect sizes separately and study identity as a random factor. We used Cochran's Q as a measure of effect size heterogeneity and the QE-test and QM-test to estimate whether moderators were associated with estimates of effect size. Publication bias was illustrated using funnel plots [59] and assessed by the trim and fill method [60,61]. All analyses were conducted using the R package metafor and the function rma.mv [62] in R v. 4.0.2 software [63].

Ornaments exhibited by different species may share evolutionary history, generating phylogenetic non-independence. To account for this, a phylogeny for each analysis was obtained using a maximum clade credibility consensus tree and a sample of 100 phylogenies downloaded from BirdTree (www.birdtree.org) [64] based on the Ericson et al. [65] backbone. The influence of phylogenetic signal was assessed using two independent approaches (electronic supplementary material, table S2). First, we determined the phylogenetic signal in model residuals as Pagel's λ [66] and Blomberg's Kappa (K) [67] using the phylosig function from the phytools package [68]. Second, we used phylogenetic generalized least-squares models to estimate Pagel's λ through maximum likelihood, by fitting the model as effect sizes approximately 1, using the R package caper [69]. Results obtained suggest that closely related species show similar relationships between female coloration and reproductive performance (electronic supplementary material, table S2) Here, we present the results of the analyses including phylogeny, following Nakagawa & Santos [70].

3. Results

Thirty-five studies (46 effect sizes) analysed supported a positive association between female colour and condition (Zr = 0.16 ± 0.03, p < 0.0001; figure 1). Females' colourful characters were positively associated with residual mass (Zr = 0.16 ± 0.04, p < 0.0001) and immune response (Zr = 0.31 ± 0.10, p = 0.002) but not parasite load (table 1a). Structural, carotenoid-dependent and (marginally) melanin-based coloration of plumage as well as integuments were related to the female condition (table 1a). Publication bias was found, suggesting eight missing studies supporting the null hypothesis (electronic supplementary material, figure S2). However, when the effect size considering missing studies was calculated equivalent results were obtained (Zr = 0.13 ± 0.03, p = 0.0003). Finally, QE was significant, which suggests that there is still variance that is unaccounted for by the model (table 1a).

Figure 1.

Figure 1.

Open in a new tab

Association of colourful female traits with condition (effect sizes ± 95% confidence intervals).

Table 1.

Effect sizes (Zr) of moderator variables for the relationships of colourful female ornaments with condition (a) and reproductive performance (b). Overall effect sizes were obtained in the absence of moderator variables.

Zr s.e. P residual heterogeneity
 moderator heterogeneity
QE P QM P
(a) condition
 overall 0.16 0.03 <0.0001
 proxy 122.23 <0.0001 29.30 <0.0001
 residual mass 0.16 0.04 <0.0001
 immune response 0.31 0.10 0.002
 parasite load 0.09 0.05 0.08
 ornament type 126.60 <0.0001 21.03 <0.0001
 integument 0.18 0.05 0.0008
 plumage 0.15 0.04 <0.0001
 coloration type 124.27 <0.0001 25.05 <0.0001
 carotenoid 0.18 0.05 <0.0001
 melanin 0.10 0.05 0.05
 structural 0.22 0.07 0.002
(b) reproductive performance
 overall 0.15 0.06 0.01
 proxy 135.40 <0.0001 6.41 0.09
 clutch size 0.28 0.14 0.04
 fledging success 0.13 0.07 0.07
 laying date 0.13 0.07 0.07
 ornament type 135.80 <0.0001 5.06 0.08
 integument 0.31 0.14 0.03
 plumage 0.10 0.08 0.23
 coloration type 119.17 <0.0001 10.52 0.01
 carotenoid 0.26 0.08 0.002
 melanin 0.08 0.07 0.26
 structural 0.15 0.08 0.07
Open in a new tab

Twenty-nine studies (42 effect sizes) included in the analysis provided support for a positive association between female colour and reproductive performance (Zr = 0.15 ± 0.06, p = 0.01; figure 2a). Particularly, female colour was positively associated with clutch size (Zr = 0.28 ± 0.14, p = 0.04). Coloration type explained heterogeneity among studies (QM = 10.52, p = 0.01), carotenoid colours were positively linked to reproductive performance (Zr = 0.26 ± 0.08, p = 0.002). Publication bias was found, but the result was qualitatively equivalent even after accounting for the 11 missing studies, following the trim and fill method (Zr = 0.08 ± 0.04, p = 0.056; electronic supplementary material, figure S3). Residual heterogeneity was found (table 1b).

Figure 2.

Figure 2.

Open in a new tab

Association of colourful female traits with reproductive performance (a) and male-mate preference (b) (effect sizes ± 95% confidence intervals).

Eleven experimental studies (11 effect sizes) analysed supported the idea that males prefer females with more colourful carotenoid-dependent traits (g = 0.64 ± 0.11, p < 0.0001; figure 2b). Integument colour (g = 0.60 ± 0.17, p = 0.0004) and plumage colour (g = 0.71 ± 0.21, p = 0.0009) explained the heterogeneity among studies (QM = 17.24, p = 0.0002). Neither unaccounted variance (QE = 16.36, p = 0.06), nor publication bias was identified (electronic supplementary material, figure S4).

4. Discussion

Using a meta-analytic approach, we found support for an association between colourful female traits and individual condition (measured as residual mass and immune response), clutch size and male-mate preferences. Hence, the expression of colourful characters in female birds is likely to be maintained by male preferences due to its probable role as a signal of the female condition and reproductive potential.

The evidence we analysed supported a positive association between colour and condition (figure 1). Thus, our results suggest that, like in males of a great number of species [71], colourful female ornaments are positively associated with residual mass and immune response. A number of empirical studies have suggested these associations might result from more colourful individuals having better foraging abilities or capacity to use micronutrients (carotenoids) ([46,72,73], but see [74]), increased access to nutritional resources through aggressive displays (melanin) ([75], but see [42]), or greater availability of energy storages (structural) ([47], but see [46]). Links between female coloration with residual mass and immune response may have emerged through selective pressures acting on females themselves (as a result of specific selective pressures), males (with correlative consequences on females) or both [76]. Although we cannot directly conclude that female coloration has a signalling role, our results suggest that there is the opportunity for female colour to evolve as a condition-dependent signal, which may be particularly relevant for males when it conveys information on fecundity.

Colourful females had better reproductive performance, measured as clutch size. Interestingly, only carotenoid-dependent colorations and integuments (but not feathers) were associated with clutch size. Hence, carotenoid-dependent colours in integumentary body parts, which can be dynamically updated in response to changes in condition [77], may be signals of direct benefits for males in the form of female fecundity [24]. This result is in line with the fact that colour and condition were positively associated and together suggest that females expressing carotenoid-dependent colourful traits can acquire and allocate resources to both ornamentation and reproduction. Like carotenoid-dependent coloration, clutch size is a phenotypically plastic trait that is sensitive to fluctuations in nutritional resource availability [78]. Thus, both can be linked to environmental sources of variation. However, the fact that carotenoid-dependent colours are repeatable despite being dynamic suggests that genetic variation in, for example, the capacity to acquire, absorb, transport, metabolize and store (micro)nutrients and/or withstand resource fluctuation may also play a role linking this type of colour with reproductive performance and condition [79–82]. Interestingly, a previous review found evidence for a positive association between female colour and reproductive performance in birds, but that result was not replicated in fish and became inconclusive (in birds) when only carotenoid-dependent colours were considered [83]. In addition, that review did not include a quantitative synthesis, so it is unclear whether information on the influence of moderator variables would have affected the interpretation of those results. Contrasting results between fish and birds may be because most of the avian species studied so far exhibit a monogamous mating system. The potential role played by the mating system on these results warrants further examination. Hence, in monogamous birds, male choosiness might be favoured when parental duties are shared by both sexes, reducing opportunities for the male to re-mate [23].

In studies of sexual selection, male-mate choice is still little explored. Accumulated evidence analysed here, mainly from monogamous species, supports the idea that males prefer females that display more colourful carotenoid-dependent traits. The fact that we found carotenoid-dependent colours in females to be related to both condition and reproductive performance suggests that those ornaments may indeed inform about direct benefits for the reproductive partner. However, the association between colourful traits and residual body mass found in females—which may conceivably be directly assessed by the males—highlights the opportunity for further studies to separate the potential confounding effects of these two characteristics on males’ preference. In general, more experimental studies evaluating male preferences for all three main types of female coloration are required to better understand the generality of this result.

This meta-analytic study provides support for the idea that colourful attributes in female birds are linked to condition and reproductive performance and may be maintained by sexual selection through male-mate choice. Accumulated evidence from birds, mainly from species with socially monogamous mating systems and biparental care, suggests that when direct benefits for pairing with a high-quality mate can be accrued, males may choose sexual partners based on information provided by coloured traits.

Acknowledgements

Preliminary analyses were performed during a workshop imparted by R. Saldaña-Vázquez. We thank A. Bentz, D. Becker, A. Gonzalez-Voyer, M. Jennions and D. Jiménez-Ortega for their advice on phylogenetic signal estimation, and M. Méndez-Janovitz, R. Torres, C. Macias Garcia, L. Kyere, A. Ríos-Chelén and three anonymous referees for their comments on previous versions. Dedicated to the memory of our beloved friend René Beamonte-Barrientos.

Contributor Information

América Hernández, Email: ame.bloom@gmail.com.

Bibiana Montoya, Email: bibianac.montoyal@uatx.mx.

Data accessibility

The data are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.bg79cnpb7 [84].

The data are provided in the electronic supplementary material [85].

Authors' contributions

A.H., B.M., R.B.B. and M.M.G. made substantial contributions to conception and design of the study. A.H. and B.M. acquired, analysed and interpreted the data. B.M. and A.H. drafted the manuscript; M.M.G. revised it critically. All coauthors agree to be held accountable for the content therein and approve the final version of the manuscript. R.B.B. died during the development of this research.

Competing interests

We declare we have no competing interests.

Funding

Funding provided by CONACyT (grant no. 10907 - 220418) and PhD fellowship no. 597708 to A.H.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Citations

  1. Hernández A, Beamonte-Barrientos R, Martínez-Gómez M, Montoya B. 2021Colorful traits in female birds relate to individual condition, reproductive performance, and male mate preferences: a meta-analytic approach. Dataset, Dryad, Dataset. ( 10.5061/dryad.bg79cnpb7) [DOI] [PMC free article] [PubMed]
  2. Hernández A, Martínez-Gómez M, Beamonte-Barrientos R, Montoya B. 2021Colourful traits in female birds relate to individual condition, reproductive performance and male-mate preferences: a meta-analytic approach. ( 10.6084/m9.figshare.c.5574178) [DOI] [PMC free article] [PubMed]

Data Availability Statement

The data are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.bg79cnpb7 [84].

The data are provided in the electronic supplementary material [85].

Articles from Biology Letters are provided here courtesy of The Royal Society

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