Honest Signals Of Quality Research Articles

Skewed performance distributions as evidence of motor constraint in sports and animal displays.

Animal displays (i.e. movement-based signals) often involve extreme behaviours that seem to push signallers to the limits of their abilities. If motor constraints limit display performance, signal evolution will be constrained, and displays can function as honest signals of quality. Existing approaches for measuring constraint, however, require multiple kinds of behavioural data. A method that requires only one kind could open up new research directions. We propose a conceptual model of performance under constraint, which predicts that the distribution of constrained performance will skew away from the constraint. We tested this prediction with sports data, because we know a priori that athletic performance is constrained and that athletes attempt to maximize performance. Performance consistently skewed in the predicted direction in a variety of sports. We then used statistical models based on the skew normal distribution to estimate the constraints on athletes and displaying animals while controlling for potential confounds and clustered data. We concluded that motor constraints tend to generate skewed behaviour and that skew normal models are useful tools to estimate constraints from a single axis of behavioural data. This study expands the toolkit for identifying, characterizing, and comparing performance constraints for applications in animal behaviour, physiology and sports.

An Early Cretaceous enantiornithine bird with a pintail

Enantiornithes are the most successful group of Mesozoic birds, arguably representing the first global avian radiation,1-4 and commonly resolved as the sister to the Ornithuromorpha, the clade within which all living birds are nested.1,3 The wealth of fossils makes it feasible to comparatively test evolutionary hypotheses about the pattern and mode of eco-morphological diversity of these sister clades that co-existed for approximately 65 Ma. Here, we report a new Early Cretaceous enantiornithine, Yuanchuavis kompsosoura gen. et. sp. nov., with a rectricial fan combined with an elongate central pair of fully pennaceous rachis-dominated plumes, constituting a new tail plumage previously unknown among nonavialan dinosaurs and Mesozoic birds but which strongly resembles the pintail in many neornithines. The extravagant but aerodynamically costly long central plumes, as an honest signal of quality, likely evolved in enantiornithines through the handicap process of sexual selection. The contrasting tail morphotypes observed between enantiornithines and early ornithuromorphs reflect the complex interplay between sexual and natural selections and indicate that each lineage experienced unique pressures reflecting ecological differences. As in neornithines, early avialans repeatedly evolved extravagant structures highlighting the importance of sexual selection in shaping the plumage of feathered dinosaurs, even early in their evolutionary history.

Physiological costs and age constraints of a sexual ornament: an experimental study in a wild bird

Abstract Sexual ornaments are often considered honest signals of quality because potential costs or constraints prevent their display by low-quality individuals. Testing for potential physiological costs of ornaments is difficult, as this requires experimentally forcing individuals to produce and display elaborate ornaments. We use this approach to test whether a sexually selected trait is physiologically costly to male superb fairy-wrens (Malurus cyaneus). Male fairy-wrens molt from brown to blue breeding plumage at different times of the year, and females strongly prefer the few males that are blue early, during winter. We used short-acting testosterone implants to stimulate males to produce “early-blue” plumage and assessed costs during and after molt using a panel of physiological indices. Testosterone-implanted, T-males molted in winter and produced blue plumage 6 weeks before control-implanted, C-males. T-males molted while in lower body condition, tended to have lower fat reserves, and were more likely to be parasitized by lice. However, we detected no negative effects on immune function, blood parasites, exposure to stressors, or survival. Juvenile males never naturally display early-blue plumage, but we found no evidence for increased costs paid by juvenile T-males. Instead, juvenile T-males molted later than adult T-males, suggesting that age presents an absolute constraint on ornament exaggeration that cannot be fully overcome by testosterone treatment. Together, these small costs and large, age-related constraints may enforce signal honesty, and explain female preference for early-blue males.

Handicap theory is applied to females but not males in relation to mate choice in the stalk-eyed fly Sphyracephala detrahens

Handicap theory explains that exaggeratedly developed sexual traits become handicaps but serve as honest signals of quality. Because very weak signals are less likely to provide benefits than to simply incur costs, it is interesting to elucidate how sexual traits are generated and developed during evolution. Many stalk-eyed fly species belonging to tribe Diopsini exhibit marked sexual dimorphism in their eye spans, and males with larger eye spans have larger bodies and reproductive capacities, which are more advantageous in terms of contests between males and acceptance for mating by females. In this study, we investigated the role of eye span in a more primitive species, Sphyracephala detrahens, in tribe Sphyracephalini with less pronounced sexual dimorphism. Male-male, female-female, and male–female pairs showed similar contests influenced by eye span, which was correlated with nutrition and reproductive ability in both sexes. During mating, males did not distinguish between sexes and chose individuals with larger eye spans, whereas females did not choose males. However, males with larger eye spans copulated repeatedly. These results indicate that, in this species, eye span with a small sexual difference does not function in sex recognition but affects contest and reproductive outcomes, suggesting the primitive state of sexual dimorphism.

CYP2J19 mediates carotenoid colour introgression across a natural avian hybrid zone.

It has long been of interest to identify the phenotypic traits that mediate reproductive isolation between related species, and more recently, the genes that underpin them. Much work has focused on identifying genes associated with animal colour, with the candidate gene CYP2J19 identified in laboratory studies as the ketolase converting yellow dietary carotenoids to red ketocarotenoids in birds with red pigments. However, evidence that CYP2J19 explains variation between red and yellow feather coloration in wild populations of birds is lacking. Hybrid zones provide the opportunity to identify genes associated with specific traits. Here we investigate genomic regions associated with colour in red-fronted and yellow-fronted tinkerbirds across a hybrid zone in southern Africa. We sampled 85 individuals, measuring spectral reflectance of forecrown feathers and scoring colours from photographs, while testing for carotenoid presence with Raman spectroscopy. We performed a genome-wide association study to identify associations with carotenoid-based coloration, using double-digest RAD sequencing aligned to a short-read whole genome of a Pogoniulus tinkerbird. Admixture mapping using 104,933 single nucleotide polymorphisms (SNPs) identified a region of chromosome 8 that includes CYP2J19 as the only locus with more than two SNPs significantly associated with both crown hue and crown score, while Raman spectra provided evidence of ketocarotenoids in red feathers. Asymmetric backcrossing in the hybrid zone suggests that yellow-fronted females mate more often with red-fronted males than vice versa. Female red-fronted tinkerbirds mating assortatively with red-crowned males is consistent with the hypothesis that converted carotenoids are an honest signal of quality.

Testosterone regulates CYP2J19-linked carotenoid signal expression in male red-backed fairywrens (Malurus melanocephalus).

Carotenoid pigments produce most red, orange and yellow colours in vertebrates. This coloration can serve as an honest signal of quality that mediates social and mating interactions, but our understanding of the underlying mechanisms that control carotenoid signal production, including how different physiological pathways interact to shape and maintain these signals, remains incomplete. We investigated the role of testosterone in mediating gene expression associated with a red plumage sexual signal in red-backed fairywrens (Malurus melanocephalus). In this species, males within a single population can flexibly produce either red/black nuptial plumage or female-like brown plumage. Combining correlational analyses with a field-based testosterone implant experiment and quantitative polymerase chain reaction, we show that testosterone mediates expression of carotenoid-based plumage in part by regulating expression of CYP2J19, a ketolase gene associated with ketocarotenoid metabolism and pigmentation in birds. This is, to our knowledge, the first time that hormonal regulation of a specific genetic locus has been linked to carotenoid production in a natural context, revealing how endocrine mechanisms produce sexual signals that shape reproductive success.

Does white tail patch size indicate quality in male Cerulean Warblers (Setophaga cerulea)?

ABSTRACT Within species of birds, variation in plumage may allow potential mates or competitive rivals to quickly assess the quality of an individual. Little is known about the role of white tail feather patches (“tail white”) in male Cerulean Warblers (Setophaga cerulea) and whether variation in patch size could serve as a signal. We hypothesized that the size of tail white patches in males acts as an honest signal of quality, with larger white patches indicating high quality males. We measured and compared the area of tail white to four estimates of quality (age, structural size, body mass, and blood parasite load) in 71 male Cerulean Warblers at the Queen’s University Biological Station in eastern Ontario. We found that males 2 years old or older had significantly larger tail white patches than 1 year old males, and that structurally larger males (estimated by wing length) had significantly larger tail white patches than smaller males. Our best-performing statistical model suggested that heavier indivi...

Corticosterone regulates multiple colour traits in Lacerta [Zootoca] vivipara males

Ornamental colours usually evolve as honest signals of quality, which is supported by the fact that they frequently depend on individual condition. It has generally been suggested that some, but not all types of ornamental colours are condition dependent, indicating that different evolutionary mechanisms underlie the evolution of multiple types of ornamental colours even when these are exhibited by the same species. Stress hormones, which negatively affect condition, have been shown to affect colour traits based on different pigments and structures, suggesting that they mediate condition dependence of multiple ornament types both among and within individuals. However, studies investigating effects of stress hormones on different ornament types within individuals are lacking, and thus, evidence for this hypothesis is scant. Here, we investigated whether corticosterone mediates condition dependence of multiple ornaments by manipulating corticosterone levels and body condition (via food availability) using a two-factorial design and by assessing their effect on multiple colour traits in male common lizards. Corticosterone negatively affected ventral melanin- and carotenoid-based coloration, whereas food availability did not affect coloration, despite its significant effect on body condition. The corticosterone effect on melanin- and carotenoid-based coloration demonstrates the condition dependence of both ornaments. Moreover, corticosterone affected ventral coloration and had no effect on the nonsexually selected dorsal coloration, showing specific effects of corticosterone on ornamental ventral colours. This suggests that corticosterone simultaneously mediates condition dependence of multiple colour traits and that it therefore accounts for covariation among them, which may influence their evolution via correlational selection.

Ultraviolet crown coloration in female blue tits predicts reproductive success and baseline corticosterone

A growing number of studies provide evidence that female plumage coloration is indicative of individual quality and can influence male mate choice. In blue tits (Cyanistes caeruleus), both sexes exhibit bright ultraviolet (UV)-reflectant crown feathers, which have previously been shown to be attractive to the opposite sex. In males, there is evidence that UV reflectance of the crown feathers is an honest signal of quality in this species, but it is unclear whether this is the case for females. To address this, the UV signal (an index of relative UV reflectance specific to the visual sensitivities of the blue tit) of mothers was measured during brood rearing for 3 years (2008–2010) and related to indices of reproductive success, that is, lay date, clutch size, and number of chicks fledged and maternal state, that is, body condition and baseline corticosterone (CORT). Maternal UV signal was unrelated to clutch size but was positively correlated with number of chicks fledged in 3 years. Maternal UV signal was also negatively correlated with lay date, but this was not consistent across years. In addition, maternal UV signal was negatively correlated with baseline CORT in all years but was not predictive of body condition. Taken together, these results provide evidence that female plumage coloration is indicative of female quality and may serve as a signal for mate choice. Further, it provides novel evidence that maternal baseline CORT is associated with UV plumage signal in free-living birds and may be an important mechanistic link between an individual’s ornamentation, state, and reproductive performance.

The interplay between gonadal steroids and immune defence in affecting a carotenoid-dependent trait

The hypothesis that sexual ornaments are honest signals of quality because their expression is dependent on hormones with immune-depressive effects has received ambiguous support. The hypothesis might be correct for those signals that are carotenoid-dependent because the required carotenoid deposition in the signal, stimulated by testosterone, might lower the carotenoid-dependent immune defence of the organism. Two pathways underlying this androgen-dependent honest signaling have been suggested. Firstly, androgens that are needed for ornament expression may suppress immune defence, a cost that only high-quality animals can afford. Alternatively, immune activation may downregulate the production of androgens in low-quality individuals. Which of these alternatives is correct, and to what extent these effects are mediated by the different metabolites of androgens, remain open questions. To provide answers to these questions, we manipulated the levels of testosterone (T), 5α-dihydrotestosterone (DHT), and 17-β-estradiol (E2) in diamond doves Geopelia cuneata, a species in which both sexes exhibit a carotenoid-dependent, androgen-regulated red–orange periorbital ring of bare skin. On the first day of the experiment (day 0), we inserted steroid-releasing implants into groups of birds and on day 14, we subjected half of the birds to an immunological challenge by immunizing them with sheep red blood cells (SRBC). In females, but not in males, androgen but not estradiol treatments reduced antibody production to SRBC. In addition, the immunological challenge reduced redness and size of the trait as well as androgens levels in both sexes and in all treatments. This indicates that an immunological challenge can lower circulating T at the cost of the trait expression. These findings are in accordance with both pathways postulated in the immunocompetence-handicap hypothesis, but do not entirely support the idea that the immunosuppressive effect of androgens yields honest signaling since both T and DHT were not immunosuppressive in males, for which sexual signaling is supposed to be especially important.

Acoustic, visual, and chemical signaling during courtship in an African cichlid fish.

The ability to attract and assess the quality of potential mates is critical for reproductive success, but few studies examine coincident multimodal sensory cues used for reproductive signaling within a single species. Here we examined acoustic, visual, and chemical signaling used by male African cichlid fish (Astatotilapia burtoni) during reproduction. Dominant males produced pulsed sounds in tight association with visual courtship displays where their bodies quivered vigorously in close proximity to a female. Sound production always occurred with visual courtship displays, but not all body quivers were associated with sound, which supports the hypothesis of intentional acoustic communication. Peak frequency of courtship sounds decreased with increasing male body size, possibly providing females with an honest signal of quality. Male chemical signaling, visualized as urine pulses, was higher in the presence of gravid compared to non‐gravid females, but did not occur during any specific acoustic or visual courtship displays. These data suggest that dominant males use acoustic, visual, and olfactory channels at different times during courtship possibly to convey distinct types of information such as social/dominance status, motivation to spawn, and fitness.

Queen pheromones

Group-living species produce signals that alter the behavior and even the physiology of their social partners. Social insects possess especially sophisticated chemical communication systems that govern every aspect of colony life, including the defining feature of eusociality: reproductive division of labor. Current evidence hints at the central importance of queen pheromones, but progress has been hindered by the fact that such pheromones have only been isolated in honeybees. In a pair of papers on the ant Lasius niger, we identified and investigated a queen pheromone regulating worker sterility. The cuticular hydrocarbon 3-methylhentriacontane (3-MeC31) is correlated with queen maturity and fecundity, and workers are also more likely to execute surplus queens that have low amounts of this chemical. Experiments with synthetic 3-MeC31 found that it inhibits ovarian development in queenless workers and lowers worker aggression towards objects coated with it. Production of 3-MeC31 by queens was depressed by an experimental immune challenge, and the same chemical was abundant on queen-laid eggs, suggesting that the workers’ responses to the queen are conditional on her health and fecundity. Together with other studies, these results indicate that queen pheromones are honest signals of quality that simultaneously regulate multiple social behaviors.

A cost of reproduction in male Atlantic cod (Gadus morhua)

In many species, females are thought to base their choice of mate on quality, which males signal through displays and body ornamentation. One important question is whether these signals represent an honest reflection of quality so that they carry an intrinsic cost to the male. A considerable body of evidence has revealed complex mating behaviours in gadoid fish, such as Atlantic cod ( Gadus morhua L., 1758), for which male reproductive success may be related to some form of female choice. However, if present, the cost of male signalling is not clear. To test the hypothesis that male behavioural displays are energetically costly, we quantified the number of displays initiated by males during spawning, and their corresponding mass loss, in two separate experiments. The number of displays was positively associated with mass loss in both experiments, suggesting that reproductive displays are costly to males; they also may be regarded as an honest signal of quality upon which females could base their choice of mate. To our knowledge, this is the first study to demonstrate a cost of male reproductive behaviour in a broadcast-spawning fish.

Quality prevails over identity in the sexually selected vocalisations of an ageing mammal.

BackgroundMale sexually selected vocalisations generally contain both individuality and quality cues that are crucial in intra- as well as inter-sexual communication. As individuality is a fixed feature whereas male phenotypic quality changes with age, individuality and quality cues may be subjected to different selection pressures over time. Individuality (for example, morphology of the vocal apparatus) and quality (for example, body size and dominance status) can both affect the vocal production mechanism, inducing the same components of vocalisations to convey both kinds of information. In this case, do quality-related changes to the acoustic structure of calls induce a modification of vocal cues to identity from year to year? We investigated this question in fallow deer (Dama dama), in which some acoustic parameters of vocalisations (groans) code for both individuality and quality.ResultsWe carried out a longitudinal analysis of groan individuality, examining the effects of age and dominance rank on the acoustic structure of groans of the same males recorded during consecutive years. We found both age- and rank-related changes to groans; the minimum values of the highest formant frequencies and the fundamental frequency increased with the age of males and they decreased when males became more dominant. Both age- and rank-related acoustic parameters contributed to individuality. Male quality changed with age, inducing a change in quality-related parameters and thus, a modification of vocal cues to male individuality between years.ConclusionsThe encoding of individuality and quality information in the same components of vocalisations induces a tradeoff between these two kinds of signals over time. Fallow deer vocalisations are honest signals of quality that are not fixed over time but are modified dynamically according to male quality. As they are more reliable cues to quality than to individuality, they may not be used by conspecifics to recognize a given male from one year to another, but potentially used by both sexes to assess male quality during each breeding season.

The carotenoid-continuum: carotenoid-based plumage ranges from conspicuous to cryptic and back again

BackgroundCarotenoids are frequently used by birds to colour their plumage with green, yellow, orange or red hues, and carotenoid-based colours are considered honest signals of quality, although they may have other functions, such as crypsis. It is usually assumed that red through yellow colours have a signalling function while green is cryptic. Here we challenge this notion using the yellow and green colouration of blue tits (Cyanistes caeruleus), great tits (Parus major) and greenfinches (Carduelis chloris) as a model.ResultsThe relationship between colouration (chroma, computed using visual sensitivities of conspecifics) and detectability (contrast against natural backgrounds as perceived by conspecifics and avian predators) followed a similar curvilinear pattern for yellow and green plumage with minimum detectability at intermediate levels of carotenoid deposition. Thus, for yellow and green plumage, colours at or close to the point of minimum detectability may aid in crypsis. This may be the case for blue and great tit green and yellow plumage, and greenfinch green plumage, all of which had comparably low levels of detectability, while greenfinch yellow plumage was more chromatic and detectable. As yellow and green blue tit colouration are strongly affected by carotenoid availability during moult, variation in pigment availability between habitats may affect the degree of background-matching or the costliness of producing cryptic plumage.ConclusionsIncreasing carotenoid-deposition in the integument does not always lead to more conspicuous colours. In some cases, such as in blue or great tits, carotenoid deposition may be selected through enhanced background-matching, which in turn suggests that producing cryptic plumage may entail costs. We stress however, that our data do not rule out a signalling function of carotenoid-based plumage in tits. Rather, it shows that alternative functions are plausible and that assuming a signalling function based solely on the deposition of carotenoids in the integument may not be warranted.

UV plumage color is an honest signal of quality in male budgerigars

AbstractElaborate and colorful feathers are important traits in female mate choice in birds. Plumage coloration can result from pigments deposited in feathers such as carotenoids and melanins, or can be caused by nano‐scale reflective tissues (structurally based coloration), usually producing ultraviolet (UV) coloration. Structural colorations remain the least studied of the three most important feather colorations. Previous studies have found a female preference for UV color in the budgerigar, Melopsittacus undulatus, but it is not clear what information this ornament conveys, nor what is the possible cost associated with its production. We investigated possible correlations between immune response and plumage color of wild‐type (green) male budgerigars. In particular we measured the wing web swelling resulting from injection of phytohaemagglutinin (PHA). We did not detect any correlation between the sedimentation rate and morphological and color variables. We found that UV chroma is the best predictor for the cutaneous immune activity. Indeed, male budgerigars with high UV reflectance in the breast feathers showed stronger immune responses. These results are consistent with the idea that UV colors are special signals conveying information about a bird's condition.

Age‐related differences in plumage characteristics of male tree swallows Tachycineta bicolor: hue and brightness signal different aspects of individual quality

Age‐related differences in plumage characteristics of birds can be the result of differential survival of more ornamented individuals, within‐individual changes in plumage attributes with age, or a combination of both. In this study, we investigated age‐class related differences in plumage attributes of male tree swallows Tachycineta bicolor by performing both cross‐sectional and longitudinal analyses. Male tree swallows in their first breeding season do not display delayed plumage maturation, and possess, like experienced breeders, metallic green to metallic blue iridescent plumage on their dorsal surface. Our results showed that, at the population level, older males were brighter and reflected light maximally at shorter wavelengths (i.e. were more blue). Differences in plumage brightness were most likely caused by changes within individuals as males increased in brightness between the first time they were captured and the subsequent year. Differences in hue, however, were not due to within‐individual changes, but rather appear to be the result of greener individuals having lower survival and/or nest site fidelity. Indeed, relatively dull, greener birds had a lower probability of being recaptured the subsequent year. In contrast, we found that if birds captured in their first year as breeding adults were relatively bright, hue was not related to the probability of recapture. These results suggest that plumage attributes in male tree swallows have the potential of being honest signals of quality. Furthermore, plumage brightness and plumage hue might signal different aspects of male quality in this species.

Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged partridge (Alectoris rufa)

Carotenoid pigments cannot be synthesized by vertebrates but must be ingested through the diet. As they seem to be a limited resource, carotenoid-based ornaments are particularly interesting as possible honest signals of individual quality, in particular of foraging efficiency and nutritional status. Some studies have demonstrated the condition dependence of carotenoid-based plumage in birds. However, many other carotenoid-pigmented bare parts (i.e. skin, caruncles, bills, cere, and tarsi) are present in birds but, in comparison with plumage, little is known about these traits as indicators of individual quality. Here, we show that the eye ring pigmentation and bill redness of the red-legged partridge (Alectoris rufa) are positively associated to body condition and recent changes in body mass. Also, we found a negative relationship between these two traits and heterophil-to-lymphocyte ratio, an indicator of physiological stress (the relationship with bill redness being significant only for males). In an experiment, we found that after a period of reduction in food intake (with the consequent loss of body mass), food-restricted birds showed lower eye ring pigmentation than ad-libitum-fed birds. Therefore, different ornaments seem to reflect changes in body condition but at different speeds or intensities (eye ring, a fleshy ornament, appears to respond more rapidly to changes in the nutritional status than a keratinized structure as the bill). These results indicate that carotenoid-based ornaments are condition-dependent traits in the red-legged partridge, being therefore susceptible to be employed as honest signals of quality in sexual selection.

Plumage characteristics, reproductive investment and assortative mating in tree swallows Tachycineta bicolor

Elaborate ornamental plumage has been associated with various measures of individual quality in many species of birds. Male plumage characteristics, which have been relatively well studied, have been shown to reflect past reproductive investment, as well as the potential for reproductive investment in the current breeding attempt. In contrast, the signalling functions of female traits remain largely unexplored. In this study, we investigated the relationship between plumage attributes of breeding adult tree swallows and past reproductive investment, current reproductive investment and social mate pairing strategy. Both males and older females possess metallic green to metallic blue iridescent plumage on their dorsal surface, making this a suitable species for this type of investigation. We did not find any effects of past reproductive investment and success on the plumage attributes of returning breeders. In contrast, female plumage hue covaried with fledging success, and female plumage brightness was positively associated with mean clutch egg mass. In addition, we found that social pairs mated assortatively with respect to plumage brightness. We argue that since plumage characteristics vary with age in both male and female tree swallows, plumage attributes in this species are indicative of breeding experience and may be honest signals of quality. Positive assortative pairing could be the result of mutual mate choice or intra-sexual competition for nest sites by both males and females.

Dawn song of the eastern kingbird: an honest signal of male quality?

To be used as honest signals of quality, phenotypic traits must vary markedly within populations and show repeatable differences between individuals. Eastern kingbirds, Tyrannus tyrannus, sing a distinctive dawn song in the predawn darkness, and one hypothesis for its function is that it serves as an honest signal of male quality that females use during choice of within-pair or extrapair mates. Over a 2-year period, we quantified dawn songs of males to measure between- and within-season repeatability of the timing (start and end time) and length of song bouts, and song rate. We also measured morphological characters to measure repeatability and describe individual differences in body size and plumage quality. All song traits varied considerably among males, start time and song rates were repeatable between years, and all song rates were repeatable within both years. All morphological characters were significantly repeatable between years. Moreover, early singing males were larger and had relatively long flight feathers, and males that sang at high rates had relatively long flight feathers. Early singing males were also paired to the earliest breeding females, and in one year, male song rate was positively correlated with their social mate's clutch size. Relatively long flight feathers in other species are typical of older males and individuals of higher body condition, suggesting that, despite being suboscine passerines with relatively simple and innate songs, eastern kingbirds use song performance as an honest signal of male quality that females may use during mate choice.