Ecological, morphological and phylogenetic correlates of interspecific variation in plasma carotenoid concentration in birds

Carotenoids are important as pigments for bright coloration of animals, and as physiologically active compounds with a wide array of health-related benefits. However, the causes of variation in carotenoid acquisition and physiology among species are poorly known. We measured the concentration of carotenoids in the blood of 80 wild bird species differing in diet, body size and the extent of carotenoid-based traits. Preliminary analyses showed that diet significantly explains interspecific variability in plasma carotenoids. However, dietary influences were apparently overridden by phylogenetic relationships among species, which explained most (65%) of this variability. This phylogenetic effect could be due partly to its covariation with diet, but may also be caused by interspecific differences in carotenoid absorption from food to the blood stream, mediated, for example by endothelial carriers or gut parasites. Carotenoid concentrations also decreased with body size (which may be explained by the allometric relationship between ingestion rate and body mass), and correlated positively with the extent of carotenoid-dependent coloration of plumage and bare parts. Therefore, the acquisition of carotenoids from the diet and their use for both health and display functions seem to be constrained by ecological and physiological aspects linked to the phylogeny and size of the species.     

Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.)

Many vertebrates use carotenoid-based signals in social or sexual interactions. Honest signalling via carotenoids implies some limitation of carotenoid-based colour expression among phenotypes in the wild, and at least five limiting proximate mechanisms have been hypothesized. Limitation may arise by carotenoid-availability, genetic constraints, body condition, parasites, or detrimental effects of carotenoids. An understanding of the relative importance of the five mechanisms is relevant in the context of natural and sexual selection acting on signal evolution. In an experimental field study with carotenoid supplementation, simultaneous cross-fostering, manipulation of brood size and ectoparasite load, we investigated the relative importance of these mechanisms for the variation in carotenoid-based coloration of nestling great tits (Parus major). Carotenoid-based plumage coloration was significantly related to genetic origin of nestlings, and was enhanced both in carotenoid-supplemented nestlings, and nestlings raised in reduced broods. We found a tendency for ectoparasite-induced limitation of colour expression and no evidence for detrimental effects of carotenoids on growth pattern, mortality and recruitment of nestlings to the local breeding population. Thus, three of the five proposed mechanisms can generate individual variation in the expression of carotenoid-based plumage coloration in the wild and thus could maintain honesty in a trait potentially used for signalling of individual quality.     

Broodmate aggression and life history variation in accipitrid birds of prey

Aggressive sibling competition for parental food resources is relatively infrequent in animals but highly prevalent and extreme among certain bird families, particularly accipitrid raptors (Accipitriformes). Intense broodmate aggression within this group is associated with a suite of traits including a large adult size, small broods, low provisioning rates, and slow development. In this study, we apply phylogenetic comparative analyses to assess the relative importance of several behavioral, morphological, life history, and ecological variables as predictors of the intensity of broodmate aggression in 65 species of accipitrid raptors. We show that intensity of aggression increases in species with lower parental effort (small clutch size and low provisioning rates), while size effects (adult body mass and length of nestling period) are unimportant. Intense aggression is more closely related to a slow life history pace (high adult survival coupled with a restrained parental effort), rather than a by‐product of allometry or food limitation. Consideration of several ecological variables affecting prey abundance and availability reveals that certain lifestyles (e.g., breeding in aseasonal habitats or hunting for more agile prey) may slow a species’ life history pace and favor the evolution of intense broodmate aggression.     

Evolution of tooth crown shape in Mesozoic birds,and its adaptive significance with respect to diet

Both the evolution of tooth morphology and the relationship between dental features and diet in toothed birds have long been studied. Here we quantify variation in tooth crown shape in 28 key Mesozoic bird species, and examine differences in dental morphology among birds belonging to different taxonomic groupings and inferred to have had different diets. Using geometric morphometric methods (GMM) and phylogenetic comparative methods (PCM), we found few clear differences in tooth crown shape between different taxonomic and ecological categories, and our analysis provides little support for many dietary inferences drawn in previous studies. However, the Solnhofen Archaeopteryx, Jeholornis, Protopteryx, Pengornis, Longipteryx, Tianyuornis, Mengciusornis, Ichthyornis and Hesperornis all were found to possess relatively specialized tooth crown shapes, perhaps reflecting specialized diets such as insectivory, granivory, piscivory and consumption of soft-shelled arthropods. Similarity in tooth crown shape across many Mesozoic birds may indicate the lack of dietary specialization, and the association between tooth form and diet may have been weakened in any case by ‘functional replacement’ of the dentition by a horny beak and, in many cases, gastroliths.     

Testing the shared-pathway hypothesis in the carotenoid-based coloration of red crossbills

The mechanisms involved in the production of red carotenoid-based ornaments of vertebrates are still poorly understood. These colorations often depend on enzymatic transformations (ketolation) of dietary yellow carotenoids, which could occur in the inner mitochondrial membrane (IMM). Thus, carotenoid ketolation and cell respiration could share biochemical pathways, favoring the evolution of ketocarotenoid-based ornaments as reliable indices of individual quality under sexual selection. Captive male red crossbills (Loxia curvirostra Linnaeus) were exposed to redox-active compounds designed to penetrate and act in the IMM: an ubiquinone (mitoQ) or a superoxide dismutase mimetic (mitoTEMPO). MitoQ can act as an antioxidant but also distort the IMM structure, increasing mitochondrial free radical production. MitoQ decreased yellow carotenoids and tocopherol levels in blood, perhaps by being consumed as antioxidants. Contrarily, mitoTEMPO-treated birds rose circulating levels of the second most abundant ketocarotenoid in crossbills (i.e., canthaxanthin). It also increased feather total red ketocarotenoid concentration and redness, but only among those birds exhibiting a redder plumage at the start of the study, that is, supposedly high-quality individuals. The fact that mitoTEMPO effects depended on original plumage color suggests that the red-ketocarotenoid-based ornaments indicate individual quality as mitochondrial function efficiency. The findings would thus support the shared pathway hypothesis.     

Male colour variation in a eurytopic African cichlid: the role of diet and hypoxia

Species that cross strong environmental gradients are expected to face divergent selective pressures that can act on sexually‐selected traits. In the present study, we examine the role of hypoxia and carotenoid availability in driving divergence in two sexually‐selected traits, male colour and reproductive behaviour, in the African cichlid Pseudocrenilabrus multicolor victoriae. Low‐dissolved oxygen (DO) (hypoxic) environments are expected to be energetically challenging; given that male nuptial colour expression and courtship displays can be costly, we expected fish in low‐DO versus high‐DO environments to differ in these traits. First, a field survey was used to describe natural variation in male nuptial colour patterns and diet across habitats divergent in DO. Next, using wild‐caught fish from a low‐DO and high‐DO habitat, we tested for differences in reproductive behaviour. Finally, a laboratory rearing experiment was used to quantify the interaction of DO and diet (low‐ versus high‐carotenoid availability) on the expression of male colour during development. In energetically challenging low‐DO environments, fish were more red and, in high‐DO environments, fish were typically brighter and more yellow. The frequency of reproductive displays in fish of low‐DO origin was 75% lower, although this had no consequence for brooding frequency (i.e. both populations produced the same number of broods on average). Our laboratory rearing study showed carotenoid availability to be important in colour production with no direct influence of DO on colour. Additionally, weak patterns of diet variation across wild populations suggest that other factors in combination with diet are contributing to colour divergence.     

Environmentally induced changes in carotenoid-based coloration of female lizards: a comment on Vercken et al

Colouration may either reflect a discrete polymorphism potentially related to life-history strategies, a continuous signal related to individual quality or a combination of both. Recently, Vercken et al. [J. Evol. Biol. (2007) 221] proposed three discrete ventral colour morphs in female common lizards, Lacerta vivipara, and suggested that they reflect alternative reproductive strategies. Here, we provide a quantitative assessment of the phenotypic distribution and determinants of the proposed colour polymorphism. Based on reflectance spectra, we found no evidence for three distinct visual colour classes, but observed continuous variation in colour from pale yellow to orange. Based on a 2-year experiment, we also provide evidence for reversible colour plasticity in response to a manipulation of the adult population sex ratio; yet, a significant portion of the colour variation was invariant throughout an adult female's life. Our results are thus in agreement with continuous colour variation in adults determined by environmental factors and potentially also by genetic factors.     

Interspecific abundance–occupancy relationships of British mammals and birds: is it possible to explain the residual variation?

Aim The majority of studies concerning positive interspecific abundance–occupancy relationships have used broad‐scale and microcosm data to test the occurrence and correlates of the relationship to determine which of the proposed mechanisms give rise to it. It has been argued recently that studying the residual variation about abundance–occupancy relationships is a more logical analysis and may yield faster progress in identifying the relative roles of the mechanisms. However, to date this approach has been largely unsuccessful. Here we test if fundamental species traits such as the status (native and introduced), habitat and trophic group of mammal and bird species may explain any of the residual variation about their respective abundance–occupancy relationships. Location The study used British mammal and bird species. Methods We tested if species traits explained any of the variation about abundance–occupancy relationships using linear regression techniques both treating species as independent data points for analysis and controlling for phylogenetic association. Results None of the species traits could explain any residual variation about the positive interspecific abundance–occupancy relationships of British mammals and birds. This applied both when treating species as independent data points and after controlling for phylogenetic association. Conclusions Given the lack of explanatory power of the species traits here and in other studies using this approach it seems that the variation about positive interspecific abundance–occupancy relationships is not explicable in a simple fashion. Predicting the likely influence of traits that are independent of phylogeny is also problematic. Therefore, the general utility of this approach and its future role in understanding the mechanisms causing positive interspecific abundance–occupancy relationships is doubtful.     

Interspecific variation in dietary carotenoid assimilation in birds: links to phylogeny and color ornamentation

Many birds use carotenoid pigments to acquire rich red, orange, and yellow coloration in feathers and bare parts that is used as a signal of mate quality. Because carotenoids are derived from foods, much attention has been paid to the role of diet in generating color variation both within and among avian species. Less consideration has been given to physiological underpinnings of color variability, especially among species. Here, I surveyed published literature (e.g. captive feeding studies) on carotenoid assimilation in six bird species and completed additional controlled carotenoid-supplementation experiments in two others to consider the ability of different taxa to extract carotenoids from the diet in relation to phylogeny and coloration. I found that, for a given level of carotenoids in the diet, passerine birds (zebra finch, Taeniopygia guttata; house finch, Carpodacus mexicanus; American goldfinch, Carduelis tristis; society finch, Lonchura domestica) exhibit higher levels of carotenoids in circulation than non-passerines like gamebirds (domestic chicken, Gallus domesticus; red junglefowl, Gallus gallus; Japanese quail, Coturnix coturnix; red-legged partridge, Alectoris rufa). This difference in carotenoid accumulation is likely due to interspecific variation in micelle, chylomicron, or lipoprotein concentrations or affinities for xanthophyll carotenoids. Passerine birds more commonly develop carotenoid-based colors than do birds from ancient avian lineages such as Galliformes, and the physiological differences I uncover may explain why songbirds especially capitalize on carotenoid pigments for color production. Ultimately, because we can deconstruct color traits into component biochemical, physical, and physiological parts, avian color signals may serve as a valuable model for illuminating the proximate mechanisms behind interspecific variation in signal use in animals.     

Interspecies variation in yolk selenium concentrations among eggs of free-living birds: The effect of phylogeny

Birds deposit the trace element selenium (Se) into their eggs because an adequate supply of this micronutrient is essential for embryonic development. Although there is considerable interest in egg Se with regard to topics as diverse as poultry nutrition and environmental pollution, data on the natural levels of Se in eggs of free-living avian species are currently very limited. To address this lack of information, we measured the yolk Se concentrations in eggs of 14 avian species collected in the wild. The concentrations (ng/g wet yolk) varied from 394 to 2238, with a mean value of 1040. Values (means+/-SD) for eggs from the UK, Canada and New Zealand were, respectively, 522+/-192 (3 species), 1194+/-584 (8 species) and 1147+/-200 (3 species). However, analysis by appropriate statistical models indicates that the effect of phylogenetic relatedness among these species is so significant that it removes any effect of geographical location. In particular, species belonging to the order Passeriformes displayed significantly higher yolk Se levels than Non-Passeriforme species. In marked contrast to the free-living species, our previously published data indicate that the Se concentration in egg yolk of the domestic chicken is only about 100 ng/g wet yolk when the birds are maintained on a basal commercial diet without supplementary Se. The results reveal an extensive interspecies variation in yolk Se (across a 6-fold range) for eggs collected from the wild. Nevertheless, the Se concentrations in the yolks of all the free-living species were far higher (4-21-fold) than that achieved in the yolk of the domestic chicken consuming a standard basal diet.     

Deep phylogeny,net primary productivity,and global body size gradient in birds

Body size is evolutionarily constrained, but the influence of phylogenetic relationships on global body size (i.e. body mass) gradients is unexplored. We quantify and map the family‐level phylogenetic and non‐phylogenetic structure of the global gradient of birds, evaluating the extent to which it is influenced by phylogenetic inertia in contrast to heat conservation, resource availability, starvation resistance, niche conservatism, or interspecific competition. Phylogenetic eigenvector regression (PVR) partitioned the global bird body size gradient into phylogenetically autocorrelated (PA) and phylogenetically independent (PI) components. Simple, piecewise, and partial regressions were used to investigate associations between the PA and PI components of body size and environmental correlates, and to quantify independent and overlapping contributions of environment, phylogenetic autocorrelation, and species richness to the body size gradient. Two‐thirds of the geographic variation in bird body size can be explained by phylogenetic relationships at the family level. The global variation in body size, independent of phylogenetic relationships, is most strongly associated with net primary productivity, which is consistent with ‘starvation resistance’. However, the New and Old worlds have very different patterns. We found no independent association of species richness with body size. Despite major unresolved regional differences, deep phylogenetic relationships, heat conservation, and starvation resistance probably operate in concert in shaping the global bird body size gradient in different parts of the world. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Effects of predation,parasites, and phylogeny on the evolution of bright coloration in north american male passerines

Summary Numerous mechanisms have been proposed to account for the evolution of cryptic and bright coloration in passerine birds. The Hamilton-Zuk revealing handicap model holds that cyclic interactions between hosts and parasites maintain additive genetic variance in secondary sexual traits and adaptive mate choice of resistant genotypes ensues (Hamilton and Zuk, 1982). Here I report no support for this model using various within-taxa techniques to test the functional relationship between the prevalence of hematozoan parasites and male brightness in many species of North American passerines. I establish that phylogeny and predation risk are most strongly associated with variation in male coloration. Ground-nesting passerines are considerably more cryptic than off-ground nesters, and there is evidence that ground-nesting passerines are under greater predation risk. Predation risk may limit the role of sexual selection in the development of bright coloration.     

Ancient origins and multiple appearances of carotenoid-pigmented feathers in birds

The broad palette of feather colours displayed by birds serves diverse biological functions, including communication and camouflage. Fossil feathers provide evidence that some avian colours, like black and brown melanins, have existed for at least 160 million years (Myr), but no traces of bright carotenoid pigments in ancient feathers have been reported. Insight into the evolutionary history of plumage carotenoids may instead be gained from living species. We visually surveyed modern birds for carotenoid-consistent plumage colours (present in 2956 of 9993 species). We then used high-performance liquid chromatography and Raman spectroscopy to chemically assess the family-level distribution of plumage carotenoids, confirming their presence in 95 of 236 extant bird families (only 36 family-level occurrences had been confirmed previously). Using our data for all modern birds, we modelled the evolutionary history of carotenoid-consistent plumage colours on recent supertrees. Results support multiple independent origins of carotenoid plumage pigmentation in 13 orders, including six orders without previous reports of plumage carotenoids. Based on time calibrations from the supertree, the number of avian families displaying plumage carotenoids increased throughout the Cenozoic, and most plumage carotenoid originations occurred after the Miocene Epoch (23 Myr). The earliest origination of plumage carotenoids was reconstructed within Passeriformes, during the Palaeocene Epoch (66–56 Myr), and not at the base of crown-lineage birds.     

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

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.     

Social costs and development of nuptial coloration in male Psammodromus algirus lizards: an experiment

In the lizard Psammodromus algirus, larger and older males show orangenuptial coloration on most of the head and are dominant oversmaller and younger, albeit sexually mature, males which donot show such extensive nuptial coloration. This raises thequestion of why young, small males delay the development ofnuptial coloration until a later breeding season. We tested thehypothesis of social costs by manipulating the color of thehead of small males. The results of agonistic interactions suggestedthat small males may pay a cost in terms of being punished bylarge males. Small males with heads painted orange were stillrecognized as small by other small males, suggesting that theywould not gain in social status relative to normal, dull, small males.We also manipulated the coloration of large males. Small malesshowed a similar response toward all large males, independentof coloration. This suggests that in short-distance communication,males used other cues, such as body size and behavior, whenjudging fighting ability. In staged experiments without malecompetition, female acceptance of matings was influenced bymale body size but not by coloration because large males weremore successful in obtaining matings than were small males,and within each age/size category there was no difference inmating success between experimental and control males.