Many bird species have colourful, intricately patterned plumage. This ornamentation is generally believed to exist to attract partners. In the 1970s, however, scientists proposed an alternative idea, called the ‘status signalling hypothesis’. This suggests that some birds have plumage ornaments that indicate the fighting abilities or dominance status of their bearers, much like the military badges worn by humans. These badges of status might evolve because fights, which commonly determine who gets valuable resources such as food, are a risky business. Individuals would greatly benefit from being able to predict the fighting abilities of any potential competitor and so avoid fights that they will probably lose.

Male house sparrows have a black patch on their throat, known as the bib, that has been considered to be a textbook demonstration of the status signalling hypothesis. However, most of the studies that support this idea studied small numbers of birds and used inconsistent methods. Furthermore, some recent studies have failed to replicate previous findings.

Sánchez-Tójar et al. collected data from several house sparrow populations across the world and systematically scrutinized the published literature to find all of the studies that tested the status signalling hypothesis in house sparrows. This revealed only weak evidence that the bib of male house sparrows signals the fighting abilities of its bearer. Instead, the published literature is a biased subsample; failures to replicate the hypothesis likely remain unpublished.

Currently, failures to replicate previous findings are generally deemed uninteresting, and so are not often published. By demonstrating the need to replicate findings robustly to avoid biasing conclusions, Sánchez-Tójar et al. thus join the call for a change in incentives and scientific culture.

Plumage ornamentation is a striking example of colour and pattern diversity in the animal kingdom and has attracted considerable research (Hill, 2002). Most studies have focused on sexual selection as the key mechanism to explain this diversity in ornamentation (Andersson, 1994; Dale et al., 2015). The status signalling hypothesis explains within-species variation in ornaments by suggesting that these ornaments signal individual dominance status or fighting ability (Rohwer, 1975). Aggressive contests are costly in terms of energy use, and risk of injuries and predation (Jakobsson et al., 1995; Kelly and Godin, 2001; Neat et al., 1998; Prenter et al., 2006; Sneddon et al., 1998). These costs could be reduced if individuals can predict the outcome of such contests beforehand using so-called ‘badges of status’ – that is, two potential competitors could decide whether to avoid or engage in aggressive interactions based on the message provided by their opponent’s signals (Rohwer, 1975).

Patches of ornamentation have been suggested to function as badges of status in a wide range of taxa, including insects (Tibbetts and Dale, 2004), reptiles (Whiting et al., 2003) and birds (Senar, 2006). The status signalling hypothesis was originally proposed to explain variation in the size of mountain sheep horns (Beninde, 1937; Geist, 1966), but the hypothesis has become increasingly important in the study of variability in plumage ornamentation in birds (Rohwer, 1975; Senar, 2006). Among the many bird species studied (Santos et al., 2011), the house sparrow (Passer domesticus) has become the classic textbook example of status signalling (Andersson, 1994; Searcy and Nowicki, 2005; Senar, 2006; Davies et al., 2012). The house sparrow is a sexually dimorphic passerine, in which the main difference between the sexes is a prominent black patch on the male’s throat and chest (hereafter ‘bib’). Many studies have suggested that bib size serves as a badge of status, but most studies are based on limited sample sizes, and have used inconsistent methodologies for measuring bib and dominance status (Nakagawa and Cuthill, 2007; Santos et al., 2011).

Meta-analysis is a powerful tool to quantitatively test the overall (across-study) effect size (i.e. the ‘meta-analytic mean’) for a specific hypothesis. Meta-analyses are therefore able to provide more robust conclusions than single studies and are increasingly used in evolutionary ecology (Gurevitch et al., 2018; Nakagawa and Poulin, 2012a; Nakagawa and Santos, 2012b; Senior et al., 2016). Traditional meta-analyses combine summary data across different studies, where design and methodology are study-specific (e.g. effect sizes among studies are typically adjusted for different fixed effects). These differences among studies are expected to increase heterogeneity, and therefore, the uncertainty of the meta-analytic mean (Mengersen et al., 2013). Meta-analysis of primary or raw data is a specific type of meta-analysis where studies are analysed in a consistent manner (Mengersen et al., 2013). This type of meta-analysis allows methodology to be standardized so that comparable effect sizes can be obtained across studies and is, therefore, considered the gold standard in disciplines such as medicine (Simmonds et al., 2005). Unfortunately, meta-analysis of primary data is still rarely used in evolutionary ecology (but see Barrowman et al., 2003; Richards and Bass, 2005; Krasnov et al., 2009), perhaps due to the difficulty of obtaining the primary data of previously published studies until recently (Culina et al., 2018; Schmid et al., 2003).

An important feature of any meta-analysis is to identify the existence of bias in the literature (Nakagawa and Santos, 2012b; Jennions et al., 2013). For example, publication bias occurs whenever particular effect sizes (e.g. larger ones) are more likely found in the literature than others (e.g. smaller ones). This tends to be the case when statistical significance and/or direction of effect sizes determines whether results were submitted or accepted for publication (Jennions et al., 2013). Thus, publication bias can strongly affect the estimation of the meta-analytic mean, and distort the interpretation of the hypothesis (Rothstein et al., 2005). Several methods have been developed to identify this and other biases (Nakagawa and Santos, 2012b; Jennions et al., 2013); however, such methods are imperfect and dependent on the number of effect sizes available, and therefore should be considered as types of sensitivity analysis (Nakagawa et al., 2017; Nakagawa and Santos, 2012b).

Here, we meta-analytically assessed the textbook example of the status signalling hypothesis in the house sparrow. Specifically, we combined summary and primary data from published and unpublished studies to test the prediction that dominance rank is positively associated with bib size across studies. We found that the meta-analytic mean was small, uncertain and overlapped zero. Hence, our results challenge the status signalling function of the male house sparrow’s bib. Also, we identified several biases in the published literature. Finally, we discuss potential biological explanations for our results, and provide advice for future studies testing the status signalling hypothesis.

Overall, we obtained the primary data for seven of 13 (54%) published studies, and we provided data for six additional unpublished studies (Table 1—Appendix 1).

Meta-analytic mean

Our meta-analyses revealed a small overall effect size with large 95% credible intervals that overlapped zero (Table 2; Figure 1). Additionally, the overall heterogeneity (I²_overall) was moderate (53%; Table 2). Thus, our results suggested that generally, bib size is at best a weak and unreliable signal of dominance status in male house sparrows.

Figure 1

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Table 2

Meta-analysis	K	Meta-analytic mean [95% CrI]	I2population ID [95% CrI] (%)	I2study ID [95% CrI] (%)	I2overall [95% CrI] (%)	Egger’s regression [95% CrI]
meta 1	85	0.23 [−0.01,0.45]	16 [0,48]	21 [0,51]	53 [33,73]	−0.13 [−0.59,0.27]
meta 2	87	0.20 [−0.01,0.40]	15 [0,46]	20 [0,49]	53 [34,74]	−0.12 [−0.55,0.28]

1. k = number of estimates; CrI = credible intervals; I² = heterogeneity.

Detection of publication bias

There was no clear asymmetry in the funnel plots (Figure 2). Also, Egger’s regression tests did not show evidence of funnel plot asymmetry in any of the meta-analyses (Table 2). However, published effect sizes were larger than unpublished ones, and the latter were not different from zero (Table 4; Figure 3). Additionally, we found that the overall effect size decreased over time and approached zero (Table 4; Figure 4).

Figure 2

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Figure 3

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Figure 4

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Table 4

Meta-regression	Estimates	Mean [95% CrI]
time-lag bias	intercept	0.26 [0.03,0.57]
(k = 53)	year of publication	−0.21 [-0.41,–0.01]
	R2marginal=	29 [0,66]
published vs.	intercept	−0.09 [-0.37,0.18]
unpublished (k = 85)	publisheda	0.50 [0.19,0.81]
	R2marginal=	38 [0,68]

1. k = number of estimates; CrI = credible intervals; R²_marginal = percentage of variance explained by the moderators; ^a relative to unpublished. Year of publication was z-transformed.

The male house sparrow’s bib is not the strong across-study predictor of dominance status once believed. In contrast to the medium-to-large effect found in the previous meta-analysis (Nakagawa et al., 2007), our updated meta-analytic mean was small, uncertain and overlapped zero. Thus, the male house sparrow’s bib should not be unambiguously considered or called a badge of status. Furthermore, we found evidence for the existence of bias in the published literature that further undermines the validity of the available support for the status signalling hypothesis. First, the meta-analytic mean of unpublished studies was essentially zero, compared to the medium effect size detected in published studies. Second, we found that the effect size estimated in published studies has been decreasing over time, and recently published effects were on average no longer distinguishable from zero. Our findings call for reconsidering this textbook example in evolutionary and behavioural ecology, and should stimulate renewed attention to hypotheses explaining within-species variation in ornamentation.

The status signalling hypothesis (Rohwer, 1975) has been extensively tested to try and explain within-species trait variation (e.g. reptiles: Whiting et al., 2003; insects: Tibbetts and Dale, 2004; humans: Dixson and Vasey, 2012), particularly plumage variation (Santos et al., 2011). Soon after the first empirical tests on birds, the black bib of male house sparrows became a textbook example of the status signalling hypothesis (Andersson, 1994; Searcy and Nowicki, 2005; Senar, 2006; Davies et al., 2012), an idea that was later confirmed meta-analytically (Nakagawa et al., 2007). However, Nakagawa et al., 2007 meta-analytic mean was over-estimated because only nine low-powered studies were available (more in Button et al., 2013). Here, we updated that meta-analysis with newly published and unpublished data. Our results showed that the overall effect size is much smaller and much more uncertain than previously thought. The status signalling hypothesis is thus no longer a compelling explanation for the evolution of bib size across populations of house sparrows.

Similar contradicting conclusions have been reported for other model species. An exhaustive review and meta-analysis on plumage coloration of blue tits (Cyanistes caeruleus) revealed that, after dozens of publications studying the function of plumage ornamentation in this species, the only robust conclusion is that females’ plumage differs from that of males (Parker, 2013). Another example is the long-believed effect of leg bands of particular colours on the perceived attractiveness of male zebra finches (Taeniopygia guttata), which has been also experimentally and meta-analytically refuted (Seguin and Forstmeier, 2012; Wang et al., 2018). Finally, the existence of a badge of status in a non-bird model species, the paper wasp (Polistes dominulus; Tibbetts and Dale, 2004) has also been challenged multiple times (e.g. Cervo et al., 2008; Green and Field, 2011; Green et al., 2013), generating doubts about its generality. Our findings corroborate studies showing that abundant replication is needed before any strong or general conclusion can be drawn (Aarts et al., 2015), and highlight the existence of important impediments (e.g. publication bias) to scientific progress in evolutionary ecology (Forstmeier et al., 2017; Fraser et al., 2018).

Indeed, our results showed that the published literature on status signalling in house sparrows is likely a biased subsample. The main evidence for this is that the mean effect size of unpublished studies was essentially zero and clearly different from the mean effect size based on published studies, which was of medium size. Furthermore, this moderator (i.e. unpublished vs. published) explained a large percentage of the model’s variance. In some of our own unpublished datasets, the relationship between dominance rank and bib size was never formally tested (D.F. Westneat and V. Bókony, personal communication, February, 2018), that is, our unpublished datasets are not all examples of the ‘file drawer problem’ (sensu Rosenthal, 1979). Egger’s regression tests failed to detect any funnel plot asymmetry, even in the meta-analyses based on published effect sizes only (Appendix 2—table 1). However, because unpublished data indeed existed (i.e. those obtained for this study), the detection failure was likely the consequence of the limited number of effect sizes available (i.e. low power) and the moderate level of heterogeneity found in this study (Moreno et al., 2009; Sterne and Egger, 2005).

An additional type of publication bias is time-lag bias, where early studies report larger effect sizes than later studies (Trikalinos and Ioannidis, 2005). We detected evidence for such bias because the correlation between dominance rank and bib size in published studies has decreased over time and approached zero. Year of publication explained a large percentage of the model's variance, and accounting for year of publication resulted in a strong reduction of the mean effect size across published studies (Table 4 vs. Appendix 2—table 1). Time-lag bias has been detected in other ecological studies (Poulin, 2000); Jennions and Moller, 2002b), including a meta-analysis on status signalling across bird species (Santos et al., 2011). In the latter study, a positive overall (across-species) effect size persisted regardless of the time-lag bias, and no strong evidence for other types of biases was found (Santos et al., 2011). However, Santos et al., 2011 did not attempt to analyse unpublished data, so additional evidence is needed to determine the effect that unpublished data may have on the overall validity of the status signalling hypothesis across bird species. If effect sizes based on unpublished data for other species were of similar magnitude to those obtained for house sparrows, the validity of the status signalling hypothesis across species would need reconsideration. The existence of publication bias in ecology has long been recognized (Cassey et al., 2004; Jennions and Moller, 2002b; Palmer, 2000). Publication bias leads to false conclusions if not accounted for (Rothstein et al., 2005), and is, thus, a serious impediment to scientific progress.

In addition to estimating the overall effect size for a hypothesis, meta-analyses are also used to assess heterogeneity among estimates (Higgins and Thompson, 2002; Higgins et al., 2003). Understanding the sources of heterogeneity is an important step towards the correct interpretation of a meta-analytic mean, and can be done using meta-regressions (Nakagawa and Santos, 2012b). Here, we found that the percentage of variance that was not attributable to sampling error (i.e. heterogeneity) was moderate. This value is below the average calculated across ecological and evolutionary meta-analyses (Senior et al., 2016), and indicates that we accounted for large differences among estimates. Our meta-regressions based on biological moderators explained 20–23% of the variance (Table 3). However, none of the biological moderators that we tested strongly influenced the overall effect size, possibly because of limited sample sizes.

The badge of status idea is more complex than typically portrayed (reviewed by Diep and Westneat, 2013). Badges of status are expected to be particularly important in large and unstable groups of individuals where individual recognition would otherwise be difficult (Rohwer, 1975). While the evolution of badges of status in New and Old World sparrows has been related to sociality (i.e. flocking) during the non-breeding season (Tibbetts and Safran, 2009), additional factors need to be involved if the signal is to function in reducing aggression but retaining honesty (Diep and Westneat, 2013). Our results, however, did not show any evidence for a season-dependent effect as the moderator ‘season’ (breeding vs. non-breeding) was not a strong predictor in our models. Badges of status are expected to function both within and between sexes (Rohwer, 1975; Senar, 2006). Indeed, we found little evidence that the status signalling function of bib size differed between male-only and mixed-sex flocks. Interestingly, when competing for resources, possessing a badge of status would be beneficial for both males and females. However, male but not female house sparrows have a bib. This sexual dimorphism suggests that the bib’s function is likely more important when competing for resources other than essential, a priori non-sex-specific resources such as food, water, sand baths and roosting sites. Møller, 1988 and Pape Moller, 1989 reported that female house sparrows preferentially choose males with large bibs (but see Kimball, 1996), and bib size has been positively correlated with sexual behaviour (Veiga, 1996; Møller, 1990), which suggests that the bib may play a role in mate choice. Furthermore, the original status signalling hypothesis posits that the main benefit of using badges of status would be to avoid fights, which should be particularly important when interacting with unfamiliar individuals (Rohwer, 1975; Senar, 2006). Although we did not have data to test whether unfamiliarity among contestants is an important pre-requisite for the status signalling hypothesis, we found no change in mean effect size when only obviously aggressive interactions were studied. In practice, testing whether the bib is important in mediating aggression among unfamiliar individuals is difficult because the certainty of the estimates of individual dominance increases over time as more contests are recorded, but so does familiarity among contestants.

There are some additional explanations for the small and uncertain effect detected by our meta-analyses. First, different populations might be under different selective pressures regarding status signalling. Indeed, the population-specific heterogeneity (I²_{population ID}) estimated in our meta-analyses was 15–16%, suggesting that population-dependent effects might exist. Second, although none of the moderators had a strong influence on the overall effect size, the study-specific heterogeneity estimated in our meta-analyses (I²_{study ID} = 20–21%) suggests that the uncertainty observed could still be explained by the status signal being context-dependent. However, context-dependence is often invoked post hoc to explain variation among studies, but strong evidence for it is lacking in most cases. Last, most studies testing the status signalling hypothesis in house sparrows are observational (Table 1), and the only two experimental studies conducted so far were inconclusive (Diep, 2012; Gonzalez et al., 2002). Thus, it cannot be ruled out that the weak correlation observed between dominance status and bib size is driven by a third, unknown variable. In this respect, it has been proposed that the association between melanin-based coloration (such as the bib; e.g. Galván et al., 2015; Galván and Alonso-Alvarez, 2017) and aggression is due to pleiotropic effects of the genes involved in regulating the synthesis of melanin (reviewed by Ducrest et al., 2008). Furthermore, bib size has been shown to correlate with testosterone, a hormone often involved in aggressive behaviour (Gonzalez et al., 2001) but this relationship has not been consistently observed (Laucht et al., 2010). Future studies should shift the focus towards understanding the function of bib size in wild populations and increase considerably the number of birds studied per group. The latter is essential because the statistical power of published tests of the status signalling hypothesis in house sparrows is alarmingly low (power = 8.5% for r = 0.20, Appendix 3) and lower than the average in behavioural ecology (Jennions, 2003).

Our analyses have several potential limitations. First, although the number of studies included in this meta-analysis is more than double that of the previous meta-analysis (Nakagawa et al., 2007), it is still limited. Also, it is likely (see above) that additional unpublished data are stored in ‘file drawers’ (sensu Rosenthal, 1979). Second, most tests included in this study were still low-powered in terms of group size (median = 6 individuals/estimate, range = 4–41), and the sample size is inflated because some of the published studies pooled individuals from different groups (Figure 4). Third, although our results showed little evidence of an effect of sampling effort on the overall effect size, the quality of the data on dominance and bib size may still be a potential factor explaining differences among studies. Fourth, experiments will normally yield larger effect sizes than observational studies because effects of confounding factors can be reduced (Palmer, 2000). Nonetheless, our systematic review only identified two studies where the status signalling hypothesis was tested experimentally in house sparrows (Gonzalez et al., 2002; Diep, 2012), preventing us from estimating the meta-analytic mean for experimental studies. Note, however, that the results of those experiments were inconclusive, and potentially affected by regression to the mean (Forstmeier et al., 2017).

In conclusion, our results challenge an established textbook example of the status signalling hypothesis, which aims to explain within-species variation in ornament size. In house sparrows, we find no evidence that bib size consistently acts as a badge of status across studies and populations, and thus, bib size can no longer be considered a textbook example of the status signalling hypothesis. Furthermore, our analyses highlight the existence of publication biases in the literature, further undermining the validity of past conclusions. Bias against the publication of small (‘non-significant’) effects hinders scientific progress. We thus join the call for a change in incentives and scientific culture in ecology and evolution (Forstmeier et al., 2017; Ihle et al., 2017; Nakagawa and Parker, 2015; Parker et al., 2016).

All data generated or analysed during this study are openly available at the Open Science Framework. We direct the reader to this project in the main text and the reference list. Link: https://osf.io/cwkxb/ DOI: 10.17605/OSF.IO/CWKXB

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Author details

1. Alfredo Sánchez-Tójar

   1. Evolutionary Biology Group, Max Planck Institute for Ornithology, Seewiesen, Germany
   2. Department of Life Sciences, Imperial College London, Ascot, United Kingdom

   Present address

   Department of Evolutionary Biology, Bielefeld University, Bielefeld, Germany

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   alfredo.tojar@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2886-0649

2. Shinichi Nakagawa

   School of Biological, Earth and Environmental Sciences, University of New South Wales, Sidney, Australia

   Contribution

   Conceptualization, Software, Supervision, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7765-5182

3. Moisès Sánchez-Fortún

   1. Evolutionary Biology Group, Max Planck Institute for Ornithology, Seewiesen, Germany
   2. Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom

   Present address

   Department de Biologia Evolutiva, Ecologia i Ciències Ambientals, University of Barcelona, Barcelona, Spain

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

4. Dominic A Martin

   Department of Life Sciences, Imperial College London, Ascot, United Kingdom

   Present address

   Biodiversity, Macroecology and Biogeography, University of Goettingen, Goettingen, Germany

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7197-2278

5. Sukanya Ramani

   1. Evolutionary Biology Group, Max Planck Institute for Ornithology, Seewiesen, Germany
   2. Department of Animal Behaviour, Bielefeld University, Bielefeld, Germany

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

6. Antje Girndt

   1. Evolutionary Biology Group, Max Planck Institute for Ornithology, Seewiesen, Germany
   2. Department of Life Sciences, Imperial College London, Ascot, United Kingdom

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9558-1201

7. Veronika Bókony

   Lendület Evolutionary Ecology Research Group, Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, Hungary

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2136-5346

8. Bart Kempenaers

   Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Seewiesen, Germany

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7505-5458

9. András Liker

   MTA-PE Evolutionary Ecology Research Group, University of Pannonia, Veszprém, Hungary

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

10. David F Westneat

    Department of Biology, University of Kentucky, Lexington, United States

    Contribution

    Investigation, Writing—review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0001-5163-8096

11. Terry Burke

    Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom

    Contribution

    Conceptualization, Supervision, Funding acquisition, Writing—review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-3848-1244

12. Julia Schroeder

    1. Evolutionary Biology Group, Max Planck Institute for Ornithology, Seewiesen, Germany
    2. Department of Life Sciences, Imperial College London, Ascot, United Kingdom

    Contribution

    Conceptualization, Supervision, Funding acquisition, Writing—review and editing

    Competing interests

    No competing interests declared

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