Evolutionary predictors of the specific colors of birds.

Animal coloration is one of the most conspicuous aspects of human-perceived organismal diversity, yet also one of the least understood. In particular, explaining why species have specific colors (e.g., blue vs. red) has proven elusive. Here, we quantify for nearly all bird species, the proportion of the body covered by each of 12 human-visible color categories, and test whether existing theory can predict the direction of color evolution. The most common colors are black, white, gray and brown, while the rarest are green, blue, purple, and red. Males have more blue, purple, red, or black, whereas females have more yellow, brown, or gray. Sexual dichromatism is partly due to sexual selection favoring ornamental colors in males but not in females. However, sexual selection also correlated positively with brown in both sexes. Strong social selection favors red and black, colors used in agonistic signaling, with the strongest effects in females. Reduced predation risk selects against cryptic colors (e.g., brown) and favors specific ornamental colors (e.g., black). Nocturnality is mainly associated with brown. The effects of habitat use support the sensory drive theory for camouflage and signaling. Darker colors are more common in species living in wet and cold climates, matching ecogeographical rules. Our study unambiguously supports existing theories of color evolution across an entire class of vertebrates, but much variation remains unexplained.

When does early-life telomere length predict survival? A case study and meta-analysis.

Suboptimal conditions during development can shorten telomeres, the protective DNA caps on the end of chromosomes. Shorter early-life telomere length (TL) can indicate reduced somatic maintenance, leading to lower survival and shorter lifespan. However, despite some clear evidence, not all studies show a relationship between early-life TL and survival or lifespan, which may be due to differences in biology or study design (e.g., survival period measured). In superb fairy-wrens (Malurus cyaneus), we assessed whether early-life TL predicts mortality across different life-history stages (fledgling, juvenile, adult). However, in contrast to a similar study on a congener, early-life TL did not predict mortality across any life stage in this species. We then performed a meta-analysis including 32 effect sizes from 23 studies (15 birds and three mammals) to quantify the effect of early-life TL on mortality whilst taking into consideration potential sources of biological and methodological variation. Overall, the effect of early-life TL on mortality was significant, corresponding to a 15% reduction in mortality risk with each standard deviation increase in TL. However, the effect became weaker when correcting for publication bias. Contrary to our predictions, there was no evidence that effects of early-life TL on mortality varied with species lifespan or the period over which survival was measured. However, negative effects of early-life TL on mortality risk were pervasive throughout life. These results imply that effects of early-life TL on mortality are more likely to be context-dependent than age-dependent, although substantial power and publication bias issues highlight the need for more research.

The evolution of carotenoid-based plumage colours in passerine birds.

Many birds use carotenoids to colour their plumage yellow to red. Because birds cannot synthesise carotenoids, they need to obtain these pigments from food, although some species metabolise dietary carotenoids (which are often yellow) into derived carotenoids (often red). Here, we study the occurrence of yellow and red carotenoid-based plumage colours in the passerines, the largest bird radiation and quantify the effects of potential ecological and life-history drivers on their evolution. We scored the presence/absence of yellow and red carotenoid-based plumage in nearly 6,000 species and use Bayesian phylogenetic mixed models to assess the effects of carotenoid-availability in diet, primary productivity, body size, habitat and sexual selection. We also test the widespread assumption that red carotenoid-based colours are more likely to be the result of metabolization. Finally, we analyse the pattern of evolutionary transitions between yellow and red carotenoid-based plumage colours to determine whether, as predicted, the evolution of yellow carotenoid-based colours precedes red. We show that, as expected, both colours are more likely to evolve in smaller species and in species with carotenoid-rich diets. Yellow carotenoid-based plumage colours, but not red, are more prevalent in species that inhabit environments with higher primary productivity and closed vegetation. In general, females were more likely to have yellow and males more likely to have red carotenoid-based plumage colours, closely matching the effects of sexual selection. Our analyses also confirm that red carotenoid-based colours are more likely to be metabolised than yellow carotenoid-based colours. Evolutionary gains and losses of yellow and red carotenoid-based plumage colours indicate that red colours evolved more readily in species that already deposited yellow carotenoids, while the reverse was rarely the case. Our study provides evidence for a general, directional evolutionary trend from yellow to red carotenoid-based colours, which are more likely to be the result of metabolization. This may render them potentially better indicators of quality, and thus favoured by sexual selection.

Ornaments are equally informative in male and female birds.

Female ornaments are often reduced, male-like traits. Although these were long perceived as non-functional, it is now broadly accepted that female ornaments can be adaptive. However, it is unclear whether this is as common in females as it is in males, and whether ornaments fulfil similar signalling roles. Here, we apply a bivariate meta-analysis to a large dataset of ornaments in mutually ornamented birds. As expected, female ornament expression tends to be reduced compared to males. However, ornaments are equally strongly associated with indicators of condition and aspects of reproductive success in both sexes, regardless of the degree of sexual dimorphism. Thus, we show here in a paired comparison within-and-across species, that ornaments in birds provide similar information in both sexes: more ornamented individuals are in better condition and achieve higher reproductive success. Although limited by their correlational nature, these outcomes imply that female ornaments could widely function in a similar manner as male ornaments.

Hot and dry conditions predict shorter nestling telomeres in an endangered songbird: Implications for population persistence.

Climate warming is increasingly exposing wildlife to sublethal high temperatures, which may lead to chronic impacts and reduced fitness. Telomere length (TL) may link heat exposure to fitness, particularly at early-life stages, because developing organisms are especially vulnerable to adverse conditions, adversity can shorten telomeres, and TL predicts fitness. Here, we quantify how climatic and environmental conditions during early life are associated with TL in nestlings of wild purple-crowned fairy-wrens (Malurus coronatus), endangered songbirds of the monsoonal tropics. We found that higher average maximum air temperature (range 31 to 45 °C) during the nestling period was associated with shorter early-life TL. This effect was mitigated by water availability (i.e., during the wet season, with rainfall), but independent of other pertinent environmental conditions, implicating a direct effect of heat exposure. Models incorporating existing information that shorter early-life TL predicts shorter lifespan and reduced fitness showed that shorter TL under projected warming scenarios could lead to population decline across plausible future water availability scenarios. However, if TL is assumed to be an adaptive trait, population viability could be maintained through evolution. These results are concerning because the capacity to change breeding phenology to coincide with increased water availability appears limited, and the evolutionary potential of TL is unknown. Thus, sublethal climate warming effects early in life may have repercussions beyond individual fitness, extending to population persistence. Incorporating the delayed reproductive costs associated with sublethal heat exposure early in life is necessary for understanding future population dynamics with climate change.

Cooperative breeding and the emergence of multilevel societies in birds.

Multilevel societies (MLSs), where social levels are hierarchically nested within each other, are considered one of the most complex forms of animal societies. Although thought to mainly occurs in mammals, it is suggested that MLSs could be under-detected in birds. Here, we propose that the emergence of MLSs could be common in cooperatively breeding birds, as both systems are favoured by similar ecological and social drivers. We first investigate this proposition by systematically comparing evidence for multilevel social structure in cooperative and non-cooperative birds in Australia and New Zealand, a global hotspot for cooperative breeding. We then analyse non-breeding social networks of cooperatively breeding superb fairy-wrens (Malurus cyaneus) to reveal their structured multilevel society, with three hierarchical social levels that are stable across years. Our results confirm recent predictions that MLSs are likely to be widespread in birds and suggest that these societies could be particularly common in cooperatively breeding birds.

Migratory birds are lighter coloured.

Migratory birds undertake long and challenging journeys that have selected for a suite of adaptations from sensory mechanisms that facilitate orientation to extreme feats of endurance that push physiological limits. Recent work on two distantly related species revealed that migrating individuals increase their flight altitude dramatically during the day compared to at night1,2. These studies suggested that the phenomenon is driven by thermoregulation: the ascent to cooler heights during the day may offset heat generated by absorption of solar radiation. If thermoregulation is an important selective force on migratory species, migrants should have evolved lighter, more reflective plumage to avoid overheating. Here we show, across the entire avian radiation, that migratory species are indeed lighter coloured.

Lens and cornea limit UV vision of birds - a phylogenetic perspective.

Most vertebrates have UV-sensitive vision, but the UV sensitivity of their eyes is limited by the transmittance of the ocular media, and the specific contribution of the different media (cornea, lens) has remained unclear. Here, we describe the transmittance of all ocular media (OMT), as well as that of lenses and corneas of birds. For 66 species belonging to 18 orders, the wavelength at which 50% of light is transmitted through the ocular media to the retina (λT0.5) ranges from 310 to 398 nm. Low λT0.5 corresponds to more UV light transmitted. Corneal λT0.5 varies only between 300 and 345 nm, whereas lens λT0.5 values are more variable (between 315 and 400 nm) and tend to be the limiting factor, determining OMT in the majority of species. OMT λT0.5 is positively correlated with eye size, but λT0.5 of corneas and lenses are not correlated with their thickness when controlled for phylogeny. Corneal and lens transmittances do not differ between birds with UV- and violet-sensitive SWS1 opsin when controlling for eye size and phylogeny. Phylogenetic relatedness is a strong predictor of OMT, and ancestral state reconstructions suggest that from ancestral intermediate OMT, highly UV-transparent ocular media (low λT0.5) evolved at least five times in our sample of birds. Some birds have evolved in the opposite direction towards a more UV-opaque lens, possibly owing to pigmentation, likely to mitigate UV damage or reduce chromatic aberration.

Variability, heritability and condition-dependence of the multidimensional male colour phenotype in a passerine bird.

Elaborate ornamental traits are commonly assumed to be honest signals of individual quality, owing to the presumed costs involved in their production and/or maintenance. Such traits are often highly variable, possibly because of condition-dependence and/or high underlying genetic variation, and it has been suggested that their expression should be more sensitive to condition and/or more heritable than non-ornamental traits. Many bird species display colourful plumage with multiple distinct patches of different developmental origins, forming complex colour phenotypes. Despite this complexity, colourful ornaments are often studied in isolation, without comparison to suitable non-ornamental controls. Based on plumage reflectance data collected over 8 years, we assessed the signalling potential of the multidimensional male colour phenotype in a tropical bird: the purple-crowned fairy-wren Malurus coronatus. Specifically, we tested the predictions that the expression of putative ornamental colours (purple and black - the breeding colours - and blue) is (1) more variable, (2) more heritable and (3) more condition-dependent compared to year-round non-ornamental colours (buff-white and brown). Our results show that ornamental colours exhibit greater levels of variability, and some chromatic components of purple and blue colouration appear slightly heritable (h² = 0.19-0.30). However, contrary to predictions of heightened condition-dependence in ornaments, only brightness of the buff-white and brown colouration increased with male body condition, although brightness of the purple colouration was related to male age as expected. Despite partial support for predictions, the lack of consistent patterns illustrates the complexity of visual signals and highlights the need to study colour phenotypes in their entirety.

Is color data from citizen science photographs reliable for biodiversity research?

Color research continuously demands better methods and larger sample sizes. Citizen science (CS) projects are producing an ever-growing geo- and time-referenced set of photographs of organisms. These datasets have the potential to make a huge contribution to color research, but the reliability of these data need to be tested before widespread implementation.We compared the difference between color extracted from CS photographs with that of color extracted from controlled lighting conditions (i.e., the current gold standard in spectrometry) for both birds and plants. First, we tested the ability of CS photographs to quantify interspecific variability by assessing > 9,000 CS photographs of 537 Australian bird species with controlled museum spectrometry data. Second, we tested the ability of CS photographs to quantify intraspecific variability by measuring petal color data for two plant species using seven methods/sources with varying levels of control.For interspecific questions, we found that by averaging out variability through a large sample size, CS photographs capture a large proportion of across species variation in plumage color within the visual part of the spectrum (R2  = 0.68-0.71 for RGB space and 0.72-0.77 for CIE-LAB space). Between 12 and 14 photographs per species are necessary to achieve this averaging effect for interspecific studies. Unsurprisingly, the CS photographs taken with commercial cameras failed to capture information in the UV part of the spectrum. For intraspecific questions, decreasing levels of control increase the color variation but averaging larger sample sizes can partially mitigate this, aside from particular issues related to saturation and irregularities in light capture.CS photographs offer a very large sample size across space and time which offers statistical power for many color research questions. This study shows that CS photographs contain data that lines up closely with controlled measurements within the visual spectrum if the sample size is large enough, highlighting the potential of CS photographs for both interspecific and intraspecific ecological or biological questions. With regard to analyzing color in CS photographs, we suggest, as a starting point, to measure multiple random points within the ROI of each photograph for both patterned and unpatterned patches and approach the recommended sample size of 12-14 photographs per species for interspecific studies. Overall, this study provides groundwork in analyzing the reliability of a novel method, which can propel the field of studying color forward.

Why climate change should generally lead to lighter coloured animals.

How species will adapt to future climate change is a key question in modern biology. One way to predict such adaptation is to draw from our knowledge of current spatial patterns of phenotypic variation. These are often summarised by different ecogeographical rules that describe how environmental gradients predict geographic variation in form and function. A recent review in Current Biology [1] synthesises how ecogeographical rules can lead to predictions about future responses to climate change in terms of appendage size, physiology, life-history traits, distribution and colour. Based on Gloger's rule, which predicts darker coloured animals in warm and wet environments, Tian and Benton [1] suggest that animals will become darker with global warming. Although the authors mention that uncertainties in the way this ecogeographical rule is interpreted make predictions difficult [1], here we argue that the opposite scenario is more likely - that selection will favour animals with lighter colours.

Partial or complete? The evolution of post-juvenile moult strategies in passerine birds.

Moulting strategies in birds have evolved to avoid overlap with, or prepare for, other demanding parts of the annual cycle, such as reproduction or migration. When moulting for the first time after leaving the nest, young birds replace their typically poor-quality plumage during the post-juvenile moult. The extent of this moult varies between species from partial to complete. Earlier studies, restricted to Western Palearctic birds, suggest that in most species a complete post-juvenile moult may not be possible simply because young birds are constrained by not having the same access to resources as adults, unless environmental conditions are favourable. These studies also show that complete post-juvenile moult is more common in species with poor-quality nest-grown plumage. We expanded the spatial and taxonomic scope of previous studies to 1,315 species of passerines from across the world and considered both the role of constraints, plumage quality and other selective pressures favouring a complete post-juvenile moult. Thus, we test whether complete moult is more prevalent in species where nest-grown feathers are presumably of poor quality (shorter nestling period), that live in environments that foster quick plumage degradation (open habitats, high insolation and humidity), and where males are under strong sexual selection. Our data reveal that 24% of species carry out a complete post-juvenile moult, and that this trait has a strong phylogenetic signal. Complete moult is more common in species that inhabit warmer regions and open habitats, show no delayed plumage maturation and have higher levels of sexual dichromatism (indicative of strong sexual selection). Neither the presumed quality of the nest-grown plumage nor living in regions with high insolation correlates with complete moult. In conclusion, the evolution of complete post-juvenile moult not only depends on whether birds can perform a complete moult (i.e. suitable environmental conditions) but also on the strength of selection associated with the need of a complete moult. In particular, the necessity to keep the plumage in good condition in challenging environments and the benefits associated with producing adult-like plumage colours to attract mates or deter rivals seem to play an important role.

Body size and climate as predictors of plumage colouration and sexual dichromatism in parrots.

Psittaciformes (parrots, cockatoos and lorikeets) comprise one of the most colourful clades of birds. Their unique pigments and safe cavity nesting habits are two potential explanations for their colourful character. However, plumage colour varies substantially between parrot species and sometimes also between males and females of the same species. Here, we use comparative analyses to evaluate what factors correlate with colour elaboration, colour diversity and sexual dichromatism. Specifically, we test the association between different aspects of parrot colouration and (a) the intensity of sexual selection and social interactions, (b) variation along the slow-fast life-history continuum and (c) climatic variation. We show that larger species and species that live in warm environments display more elaborated colours, yet smaller species have higher levels of sexual dichromatism. Larger parrots tend to have darker and more blue and red colours. Parrots that live in wetter environments are darker and redder, whereas species inhabiting warm regions have more blue plumage colours. In general, each of the variables we considered explain small to moderate amounts of variation in parrot colouration (up to 15%). Our data suggest that sexual selection may be acting more strongly on males in small, short-lived parrots leading to sexual dichromatism. More elaborate colouration in both males and females of the larger, long-lived species with slow tropical life histories suggests that mutual mate choice, social selection and reduced selection for crypsis may be important in these species, as has been shown for passerines.

Evolutionary drivers of seasonal plumage colours: colour change by moult correlates with sexual selection, predation risk and seasonality across passerines.

Some birds undergo seasonal colour change by moulting twice each year, typically alternating between a cryptic, non-breeding plumage and a conspicuous, breeding plumage ('seasonal plumage colours'). We test for potential drivers of the evolution of seasonal plumage colours in all passerines (N = 5901 species, c. 60% of all birds). Seasonal plumage colours are uncommon, having appeared on multiple occasions but more frequently lost during evolution. The trait is more common in small, ground-foraging species with polygynous mating systems, no paternal care and strong sexual dichromatism, suggesting it evolved under strong sexual selection and high predation risk. Seasonal plumage colours are also more common in species predicted to have seasonal breeding schedules, such as migratory birds and those living in seasonal climates. We propose that seasonal plumage colours have evolved to resolve a trade-off between the effects of natural and sexual selection on colouration, especially in seasonal environments.

Immunosenescence in wild animals: meta-analysis and outlook.

Immunosenescence, the decline in immune defense with age, is an important mortality source in elderly humans but little is known of immunosenescence in wild animals. We systematically reviewed and meta-analysed evidence for age-related changes in immunity in captive and free-living populations of wild species (321 effect sizes in 62 studies across 44 species of mammals, birds and reptiles). As in humans, senescence was more evident in adaptive (acquired) than innate immune functions. Declines were evident for cell function (antibody response), the relative abundance of naïve immune cells and an in vivo measure of overall immune responsiveness (local response to phytohaemagglutinin injection). Inflammatory markers increased with age, similar to chronic inflammation associated with human immunosenescence. Comparisons across taxa and captive vs free-living animals were difficult due to lack of overlap in parameters and species measured. Most studies are cross-sectional, which yields biased estimates of age-effects when immune function co-varies with survival. We therefore suggest longitudinal sampling approaches, and highlight techniques from human cohort studies that can be incorporated into ecological research. We also identify avenues to address predictions from evolutionary theory and the contribution of immunosenescence to age-related increases in disease susceptibility and mortality.

A review of Gloger's rule, an ecogeographical rule of colour: definitions, interpretations and evidence.

Gloger's rule is an ecogeographical rule that links animal colouration with climatic variation. This rule is named after C.W.L. Gloger who was one of the first to summarise the associations between climatic variation and animal colouration, noting in particular that birds and mammals seemed more pigmented in tropical regions. The term 'Gloger's rule' was coined by B. Rensch in 1929 and included different patterns of variation from those described by Gloger. Rensch defined the rule in two ways: a simple version stating that endothermic animals are predicted to be darker in warmer and humid areas due to the increased deposition of melanin pigments; and a complex version that includes the differential effects of humidity and temperature on both main types of melanin pigments - eu- and phaeo-melanin. The blackish eu-melanins are predicted to increase with humidity, and decrease only at extreme low temperatures, while the brown-yellowish phaeomelanins prevail in dry and warm regions and decrease rapidly with lower temperatures. A survey of the literature indicates that there is considerable variation/confusion in the way Gloger's rule is understood (based on 271 studies that define the rule). Whereas the complex version is hardly mentioned, only a quarter of the definitions are consistent with the simple version of Gloger's rule (darker where warm and wet), and most definitions mention only the effects of humidity (darker where wet). A smaller subset of studies define the rule based on other correlated climatic and environmental variables such as vegetation, latitude, altitude, solar radiation, etc., and a few even contradict the original definition (darker where cold). Based on the literature survey, I synthesised the qualitative (N = 124 studies) and quantitative (meta-analytically, N = 38 studies, 241 effects) evidence testing the simple version of Gloger's rule (I found no tests of the complex version). Both lines of evidence supported the predicted effects of humidity (and closely linked variables) on colour variation, but not the effects of temperature. Moreover, humidity effects are not restricted to birds and mammals, as the data indicate that these effects also apply to insects. This suggests that the simple version of Gloger's rule as originally defined may not be valid, and possibly that the rule should be re-formulated in terms of humidity effects only. I suggest, however, that more data are needed before such a reformulation, due to potential publication biases. In conclusion, I recommend that authors cite Rensch when referring to Gloger's rule and that they make clear which version they are referring to. Future research should concentrate on rigorously testing the validity and generality of both versions of Gloger's rule and establishing the mechanism(s) responsible for the patterns it describes. Since humidity seems to be the core climatic variable behind Gloger's rule, I suggest that the two most plausible mechanisms are camouflage and protection against parasites/pathogens, the latter possibly through pleiotropic effects on the immune system. Understanding the processes that lead to climatic effects on animal colouration may provide insights into past and future patterns of adaptation to climatic change.

Conspicuous Plumage Does Not Increase Predation Risk: A Continent-Wide Test Using Model Songbirds.

The forces shaping female plumage color have long been debated but remain unresolved. Females may benefit from conspicuous colors but are also expected to suffer costs. Predation is one potential cost, but few studies have explicitly investigated the relationship between predation risk and coloration. The fairy-wrens show pronounced variation in female coloration and reside in a wide variety of habitats across Australasia. Species with more conspicuous females are found in denser habitats, suggesting that conspicuousness in open habitat increases vulnerability to predators. To test this, we measured attack rates on 3-D-printed models mimicking conspicuously colored males and females and dull females in eight different fairy-wren habitats across Australia. Attack rates were higher in open habitats and at higher latitudes. Contrary to our predictions, dull female models were attacked at similar rates to the conspicuous models. Further, the probability of attack in open habitats increased more for both types of female models than for the conspicuous male model. Across models, the degree of contrast (chromatic and achromatic) to environmental backgrounds was unrelated to predation rate. These findings do not support the long-standing hypothesis that conspicuous plumage, in isolation, is costly due to increased attraction of predators. Our results indicate that conspicuousness interacts with other factors in driving the evolution of plumage coloration.

Reconciling ecogeographical rules: rainfall and temperature predict global colour variation in the largest bird radiation.

Ecogeographical rules that associate climate with organismal form and function can reveal patterns of climatic adaptation. Two rules link animal coloration with climate: Gloger's rule (darker coloration where wet and warm), and Bogert's rule (darker coloration where cold). Whereas Gloger's rule was proposed for endotherms, and Bogert's rule for ectotherms, both rules may apply more broadly, despite their seemingly opposing effects. Here, we test this contradiction on a global scale across passerine birds. Consistent with Gloger's rule, birds were darker in wetter areas and, following Bogert's rule, lighter where warm, although birds became lighter again at very low temperatures. Rainfall and temperature had antagonistic or additive effects depending on their pattern of covariation, and this predicted whether birds followed the rules. We integrate both rules into a general framework to explain heterogeneity in climatic effects on coloration, which has implications to understand patterns of diversification, climatic adaptation and climate change impacts.

Avian predation intensity as a driver of clinal variation in colour morph frequency.

Phenotypic variation provides the framework for natural selection to work upon, enabling adaptive evolution. One of the most discernible manifestations of phenotypic variability is colour variation. When this variation is discrete, genetically based colour pattern morphs occur simultaneously within a population. Why and how colour polymorphisms are maintained is an evolutionary puzzle. Several evolutionary drivers have been hypothesized as influencing clinal patterns of morph frequency, with spatial variation in climate and predation being considered especially important. Despite this, no study has examined both of their roles simultaneously. The aims of this study were to: (a) examine the covariation of physiology, environmental variables and colouration at a local scale; and (b) determine if these factors and their interplay explain broad clinal variation in morph frequency. We used the lizard Liopholis whitii as a model system, as this species displays a discrete, heritable polymorphism for colour pattern (plain-backed, patterned morphs) whose morph frequency varies latitudinally. We measured reflectance, field activity temperatures and microhabitat structure to test for differences in crypsis, thermal biology and microhabitat selection of patterned and plain-backed morphs within a single population where colour morphs occur sympatrically. We then used data from the literature to perform a broad-scale analysis to identify whether these factors also explained the latitudinal variation of morph frequency in this species. At the local scale, plain-backed morphs were found to be less cryptic than patterned morphs while no other differences were detected in terms of thermal biology, dorsal reflectance and microhabitat use. At a broader scale, predation was the most influential factor mediating morph frequency across latitudes. However, the observed pattern of morph frequency is opposite to what the modelling results suggest in that the incidence of the least cryptic morph is highest where predation pressure is most severe. Clinal variation in the level of background matching between morphs or the potential reproductive advantage by the plain-backed morph may, instead, be driving the observed morph frequency. Together, these results provide key insights into the evolution of local adaptation as well as the ecological forces involved in driving the dynamics of colour polymorphism.