Evolution of Plumage Patterns in a Pattern Morphospace: A Phylogenetic Analysis of Melanerpine Woodpeckers.

AbstractPlumage patterns of melanerpine (Melanerpes-Sphyrapicus) woodpeckers are strikingly diverse. Understanding the evolution and function of this diversity is challenging because of the difficulty of quantifying plumage patterns. We use a three-dimensional space to characterize the evolution of melanerpine achromatic plumage patterns. The axes of the space are three pattern features (spatial frequency, orientation, and contrast) quantified using two-dimensional fast Fourier transformation of museum specimen images. Mapping plumage in pattern space reveals differences in how species and subclades occupy the space. To quantify these differences, we derive two new measures of pattern: pattern diversity (diversity across plumage patches within a species) and pattern uniqueness (divergence of patterns from those of other species). We estimate that the melanerpine ancestor had mottled plumage and find that pattern traits across patches and subclades evolve at different rates. We also find that smaller species are more likely to display horizontal face patterning. We promote pattern spaces as powerful tools for investigating animal pattern evolution.

A hypothesis for robust polarization vision: an example from the Australian imperial blue butterfly, Jalmenus evagoras.

The Australian lycaenid butterfly Jalmenus evagoras has iridescent wings that are sexually dimorphic, spectrally and in their degree of polarization, suggesting that these properties are likely to be important in mate recognition. We first describe the results of a field experiment showing that free-flying individuals of J. evagoras discriminate between visual stimuli that vary in polarization content in blue wavelengths but not in others. We then present detailed reflectance spectrophotometry measurements of the polarization content of male and female wings, showing that female wings exhibit blue-shifted reflectance, with a lower degree of polarization relative to male wings. Finally, we describe a novel method for measuring alignment of ommatidial arrays: by measuring variation of depolarized eyeshine intensity from patches of ommatidia as a function of eye rotation, we show that (a) individual rhabdoms contain mutually perpendicular microvilli; (b) many rhabdoms in the array have their microvilli misaligned with respect to neighboring rhabdoms by as much as 45 deg; and (c) the misaligned ommatidia are useful for robust polarization detection. By mapping the distribution of the ommatidial misalignments in eye patches of J. evagoras, we show that males and females exhibit differences in the extent to which ommatidia are aligned. Both the number of misaligned ommatidia suitable for robust polarization detection and the number of aligned ommatidia suitable for edge detection vary with respect to both sex and eye patch elevation. Thus, J. evagoras exhibits finely tuned ommatidial arrays suitable for perception of polarized signals, likely to match sex-specific life history differences in the utility of polarized signals.

Wild hummingbirds discriminate nonspectral colors.

Many animals have the potential to discriminate nonspectral colors. For humans, purple is the clearest example of a nonspectral color. It is perceived when two color cone types in the retina (blue and red) with nonadjacent spectral sensitivity curves are predominantly stimulated. Purple is considered nonspectral because no monochromatic light (such as from a rainbow) can evoke this simultaneous stimulation. Except in primates and bees, few behavioral experiments have directly examined nonspectral color discrimination, and little is known about nonspectral color perception in animals with more than three types of color photoreceptors. Birds have four color cone types (compared to three in humans) and might perceive additional nonspectral colors such as UV+red and UV+green. Can birds discriminate nonspectral colors, and are these colors behaviorally and ecologically relevant? Here, using comprehensive behavioral experiments, we show that wild hummingbirds can discriminate a variety of nonspectral colors. We also show that hummingbirds, relative to humans, likely perceive a greater proportion of natural colors as nonspectral. Our analysis of plumage and plant spectra reveals many colors that would be perceived as nonspectral by birds but not by humans: Birds' extra cone type allows them not just to see UV light but also to discriminate additional nonspectral colors. Our results support the idea that birds can distinguish colors throughout tetrachromatic color space and indicate that nonspectral color perception is vital for signaling and foraging. Since tetrachromacy appears to have evolved early in vertebrates, this capacity for rich nonspectral color perception is likely widespread.

Egg patterns as identity signals in colonial seabirds: a comparison of four alcid species.

The ability to recognize mates, kin, offspring and neighbors by their individually distinctive traits-individual recognition (IR)-is widespread in animals. Much work has investigated IR from the perspective of the recognizer, but less is known about the extent to which signals have evolved to facilitate IR. To explore this, one approach is to compare putative identity signals among species that differ in life history and extent of IR. In Common Murres (Uria aalge), a colonially breeding seabird, the eggs of individual females are remarkably variable in terms of color and pattern (maculation). Common Murres also appear to recognize their own eggs, leading to the hypothesis that variable egg phenotypes evolved to promote recognizability. However, we lack a quantitative assessment of the egg pattern information in Common Murres and their close relatives. Here, we analyzed images of eggs laid by four alcid species: Common Murres, Thick-billed Murres (Uria lomvia), Razorbills (Alca torda) and Dovekies (Alle alle). We extracted pattern measures believed to be relevant to bird vision and calculated Beecher's information statistic (Hs ), which allowed us to compare the amount of identity information contained in each species' egg patterns. Murres, which nest in dense colonies and can recognize their own eggs, have egg patterns with a relatively large amount of identity information compared to Razorbills and Dovekies. Egg recognition has not been demonstrated in Razorbills and Dovekies, whose colonies are less dense. Our results are consistent with the hypothesis that complex patterns of Murre eggs may have evolved to increase individual recognizability.

Avian Coloration Genetics: Recent Advances and Emerging Questions.

The colorful phenotypes of birds have long provided rich source material for evolutionary biologists. Avian plumage, beaks, skin, and eggs-which exhibit a stunning range of cryptic and conspicuous forms-inspired early work on adaptive coloration. More recently, avian color has fueled discoveries on the physiological, developmental, and-increasingly-genetic mechanisms responsible for phenotypic variation. The relative ease with which avian color traits can be quantified has made birds an attractive system for uncovering links between phenotype and genotype. Accordingly, the field of avian coloration genetics is burgeoning. In this review, we highlight recent advances and emerging questions associated with the genetic underpinnings of bird color. We start by describing breakthroughs related to 2 pigment classes: carotenoids that produce red, yellow, and orange in most birds and psittacofulvins that produce similar colors in parrots. We then discuss structural colors, which are produced by the interaction of light with nanoscale materials and greatly extend the plumage palette. Structural color genetics remain understudied-but this paradigm is changing. We next explore how colors that arise from interactions among pigmentary and structural mechanisms may be controlled by genes that are co-expressed or co-regulated. We also identify opportunities to investigate genes mediating within-feather micropatterning and the coloration of bare parts and eggs. We conclude by spotlighting 2 research areas-mechanistic links between color vision and color production, and speciation-that have been invigorated by genetic insights, a trend likely to continue as new genomic approaches are applied to non-model species.

Animal Coloration Patterns: Linking Spatial Vision to Quantitative Analysis.

Animal coloration patterns, from zebra stripes to bird egg speckles, are remarkably varied. With research on the perception, function, and evolution of animal patterns growing rapidly, we require a convenient framework for quantifying their diversity, particularly in the contexts of camouflage, mimicry, mate choice, and individual recognition. Ideally, patterns should be defined by their locations in a low-dimensional pattern space that represents their appearance to their natural receivers, much as color is represented by color spaces. This synthesis explores the extent to which animal patterns, like colors, can be described by a few perceptual dimensions in a pattern space. We begin by reviewing biological spatial vision, focusing on early stages during which neurons act as spatial filters or detect simple features such as edges. We show how two methods from computational vision-spatial filtering and feature detection-offer qualitatively distinct measures of animal coloration patterns. Spatial filters provide a measure of the image statistics, captured by the spatial frequency power spectrum. Image statistics give a robust but incomplete representation of the appearance of patterns, whereas feature detectors are essential for sensing and recognizing physical objects, such as distinctive markings and animal bodies. Finally, we discuss how pattern space analyses can lead to new insights into signal design and macroevolution of animal phenotypes. Overall, pattern spaces open up new possibilities for exploring how receiver vision may shape the evolution of animal pattern signals.

Behaviorally Induced Camouflage: A New Mechanism of Avian Egg Protection.

When animals potentially occupy diverse microhabitats, how can camouflage be achieved? Here we combine descriptive and experimental methods to uncover a novel form of phenotypic plasticity in the camouflage of bird eggs that may be present in other avian taxa. Soil from the bare substrate adheres to the blue-footed booby's (Sula nebouxii's) pale eggs, which parents manipulate both under and on top of their webs. Analysis of digital images confirmed that dirtiness increases progressively during the first 16 days of the incubation period, making eggs more similar to the nest substrate. Observations of 3,668 single-egg clutches showed that the probability of egg loss declines progressively over the same time frame and then remains low for the rest of the 41-day incubation period. An experiment showed that when chicken eggs are soiled and exposed in artificial booby nests, they are less likely to be taken by Heermann's gulls (Larus heermanni) than clean eggs.

How colorful are fruits? Limited color diversity in fleshy fruits on local and global scales.

The colors of fleshy fruits are considered to be a signal to seed-dispersing animals, but their diversity remains poorly understood. Using an avian color space to derive a sensory morphospace for fruit color, we tested four hypotheses of fruit color diversity: fruit colors occupy a limited area of the color space; they are less diverse than flower colors; fruit colors within localities are similar to each other; and fruit color diversity reflects phylogeny. The global fruit color diversity of 948 primarily bird-dispersed plant species and the color diversity of localities were compared with null models of random, unconstrained evolution of fruit color. Fruit color diversity was further compared with the diversity of 1300 flower colors. Tests of phylogenetic effects on fruit color were used to assess the degree of correspondence with phylogeny. Global and local fruit color diversity was limited compared with null models and fruits have achieved only half the color diversity of flowers. Interestingly, we found little indication of phylogenetic conservatism. Constraints resulting from the chemical properties of pigments probably limit global fruit and flower color diversity. Different types of selection on fruits and flowers may further explain the smaller color diversity of fruits.

Evolution of nest architecture in tyrant flycatchers and allies.

Innovations in nest design are thought to be one potential factor in the evolutionary success of passerine birds (order: Passeriformes), which colonized new ecological niches as they diversified in the Oligocene and Miocene. In particular, tyrant flycatchers and their allies (parvorder: Tyrannida) are an extremely diverse group of New World suboscine passerines occupying a wide range of habitats and exhibiting substantial extant variation in nest design. To explore the evolution of nest architecture in this clade, we first described nest traits across the Tyrannida phylogeny and estimated ancestral nest conditions. We then quantified macroevolutionary transition rates between nest types, examined a potential coevolutionary relationship between nest type and habitat, and used phylogenetic mixed models to determine possible ecological and environmental correlates of nest design. The Tyrannida ancestor probably built a cup nest in a closed habitat, and dome nests independently evolved at least 15 times within this group. Both cup- and dome-nesting species diversified into semi-open and open habitats, and we did not detect a coevolutionary relationship between nest type and habitat. Furthermore, nest type was not significantly correlated with several key ecological, life-history and environmental traits, suggesting that broad variation in Tyrannida nest architecture may not easily be explained by a single factor. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

The evolutionary ecology of nests: a cross-taxon approach.

Nests, including the enormous structures housing colonies of eusocial insects and the elaborately built nests of some fishes, have long fascinated scientists, yet our understanding of the evolutionary ecology of nests has lagged behind our understanding of subsequent reproductive stages. There has, however, been a burgeoning amount of interest in nests over the past decade, and this special issue on 'The evolutionary ecology of nests: a cross-taxon approach' outlines our understanding of the form and function of nests in diverse animal lineages. Papers in 'The function of nests: mechanisms and adaptive benefits' theme examine the various functions of nests, while papers in 'The evolution of nest characteristics' theme examine the evolution of nesting behaviours. Meanwhile, papers in the 'Large communal nests in harsh environments' theme examine how the enormous structures constructed by eusocial insects and social birds enable them to inhabit harsh arid environments, whereas papers in the 'Nests in the Anthropocene' theme examine how adaptive shifts in nest architecture allow animals to adapt to breed in the age of accelerating global human impacts. Finally, the synthesis outlines how the mixture of ideas and approaches from researchers studying different taxa will advance our understanding of this exciting field of research. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Repeatable randomness, invariant properties, and the design of biological signatures of identity.

What makes a perfect signature? Optimal signatures should be consistent within individuals and distinctive between individuals. In defense against avian brood parasitism, some host species have evolved "signatures" of identity on their eggs, comprising interindividual variation in color and pattern. Tawny-flanked prinia (Prinia subflava) egg signatures facilitate recognition and rejection of parasitic cuckoo finch (Anomalospiza imberbis) eggs. Here, we show that consistency and distinctiveness of patterns are negatively correlated in prinia eggs, perhaps because non-random, repeatable pattern generation mechanisms increase consistency but limit distinctiveness. We hypothesize that pattern properties which are repeatable within individuals but random between individuals ("invariant properties") allow hosts to circumvent this trade-off. To find invariant properties, we develop a method to quantify entire egg phenotypes from images taken from different perspectives. We find that marking scale (a fine-grained measure of size), but not marking orientation or position, is an invariant property in prinias. Hosts should therefore use differences in marking scale in egg recognition, but instead field experiments show that these differences do not predict rejection of conspecific eggs by prinias. Overall, we show that invariant properties allow consistency and distinctiveness to coexist, yet receiver behavior is not optimally tuned to make use of this information.

Bird eggs.

I once spent a summer studying gulls on Appledore Island in the Gulf of Maine, off the east coast of the United States. The rocky island is a breeding colony for herring gulls (Larus argentatus) and great black-backed gulls (Larus marinus), so I had a front-row seat to the dramas that unfolded as birds paired up, laid and incubated eggs, and raised chicks. I saw chicks hatch from large speckled eggs (Figure 1A), a Herculean feat that took over an hour. Eggs and chicks are extremely vulnerable, and many gull offspring do not survive. Now, when a gull soars past - or pilfers my sandwich at the beach - I appreciate the hurdles it overcame just to reach adulthood.

Evolution of brilliant iridescent feather nanostructures.

The brilliant iridescent plumage of birds creates some of the most stunning color displays known in the natural world. Iridescent plumage colors are produced by nanostructures in feathers and have evolved in diverse birds. The building blocks of these structures-melanosomes (melanin-filled organelles)-come in a variety of forms, yet how these different forms contribute to color production across birds remains unclear. Here, we leverage evolutionary analyses, optical simulations, and reflectance spectrophotometry to uncover general principles that govern the production of brilliant iridescence. We find that a key feature that unites all melanosome forms in brilliant iridescent structures is thin melanin layers. Birds have achieved this in multiple ways: by decreasing the size of the melanosome directly, by hollowing out the interior, or by flattening the melanosome into a platelet. The evolution of thin melanin layers unlocks color-producing possibilities, more than doubling the range of colors that can be produced with a thick melanin layer and simultaneously increasing brightness. We discuss the implications of these findings for the evolution of iridescent structures in birds and propose two evolutionary paths to brilliant iridescence.

How Signaling Geometry Shapes the Efficacy and Evolution of Animal Communication Systems.

Animal communication is inherently spatial. Both signal transmission and signal reception have spatial biases-involving direction, distance, and position-that interact to determine signaling efficacy. Signals, be they visual, acoustic, or chemical, are often highly directional. Likewise, receivers may only be able to detect signals if they arrive from certain directions. Alignment between these directional biases is therefore critical for effective communication, with even slight misalignments disrupting perception of signaled information. In addition, signals often degrade as they travel from signaler to receiver, and environmental conditions that impact transmission can vary over even small spatiotemporal scales. Thus, how animals position themselves during communication is likely to be under strong selection. Despite this, our knowledge regarding the spatial arrangements of signalers and receivers during communication remains surprisingly coarse for most systems. We know even less about how signaler and receiver behaviors contribute to effective signaling alignment over time, or how signals themselves may have evolved to influence and/or respond to these aspects of animal communication. Here, we first describe why researchers should adopt a more explicitly geometric view of animal signaling, including issues of location, direction, and distance. We then describe how environmental and social influences introduce further complexities to the geometry of signaling. We discuss how multimodality offers new challenges and opportunities for signalers and receivers. We conclude with recommendations and future directions made visible by attention to the geometry of signaling.

Pattern mimicry of host eggs by the common cuckoo, as seen through a bird's eye.

Cuckoo-host interactions provide classical examples of coevolution. Cuckoos place hosts under selection to detect and reject foreign eggs, while host defences result in the evolution of host-egg mimicry in cuckoos. Despite a long history of research, egg pattern mimicry has never been objectively quantified, and so its coevolution with host defences has not been properly assessed. Here, we use digital image analysis and modelling of avian vision to quantify the level of pattern mimicry in eight host species of the common cuckoo Cuculus canorus and their respective cuckoo host-races. We measure a range of pattern attributes, including marking size, diversity in size, contrast, coverage and dispersion. This new technique reveals hitherto unnoticed sophistication in egg pattern mimicry. We show that various features of host egg pattern are mimicked by the eggs of their respective cuckoo host-races, and that cuckoos have evolved better pattern mimicry for host species that exhibit stronger egg rejection. Pattern differs relatively more between eggs of different host species than between their respective cuckoo host-races. We suggest that cuckoos may have more 'average' markings in order to be able to use subsidiary hosts. Our study sheds new light on cuckoo-host coevolution and illustrates a new technique for quantifying animal markings with respect to the relevant animal visual system.

Multimodal mimicry of hosts in a radiation of parasitic finches.

Brood parasites use the parental care of others to raise their young and sometimes employ mimicry to dupe their hosts. The brood-parasitic finches of the genus Vidua are a textbook example of the role of imprinting in sympatric speciation. Sympatric speciation is thought to occur in Vidua because their mating traits and host preferences are strongly influenced by their early host environment. However, this alone may not be sufficient to isolate parasite lineages, and divergent ecological adaptations may also be required to prevent hybridization collapsing incipient species. Using pattern recognition software and classification models, we provide quantitative evidence that Vidua exhibit specialist mimicry of their grassfinch hosts, matching the patterns, colors and sounds of their respective host's nestlings. We also provide qualitative evidence of mimicry in postural components of Vidua begging. Quantitative comparisons reveal small discrepancies between parasite and host phenotypes, with parasites sometimes exaggerating their host's traits. Our results support the hypothesis that behavioral imprinting on hosts has not only enabled the origin of new Vidua species, but also set the stage for the evolution of host-specific, ecological adaptations.

Higher-level pattern features provide additional information to birds when recognizing and rejecting parasitic eggs.

Despite a recent explosion of research on pattern recognition, in both neuroscience and computer vision, we lack a basic understanding of how most animals perceive and respond to patterns in the wild. Avian brood parasites and their hosts provide an ideal study system for investigating the mechanisms of pattern recognition. The cuckoo finch, Anomalospiza imberbis, and its host the tawny-flanked prinia, Prinia subflava, lay highly polymorphic eggs with a great deal of variation in colour and patterning, with the cuckoo finch capable of close egg mimicry. Behavioural experiments in Zambia have previously shown that prinias use colour and multiple 'low-level' (occurring in early stages of visual processing) pattern attributes, derived from spatial frequency analysis, when rejecting foreign eggs. Here, we explore the extent to which host birds might also use 'higher-level' pattern attributes, derived from a feature detection algorithm, to make rejection decisions. Using a SIFT-based pattern recognition algorithm, NaturePatternMatch, we show that hosts are more likely to reject a foreign egg if its higher-level pattern features-which capture information about the shape and orientation of markings-differ from those of the host eggs. A revised statistical model explains about 37% variance in egg rejection behaviour, and differences in colour, low-level and higher-level pattern features all predict rejection, accounting for 42, 44 and 14% of the explained variance, respectively. Thus, higher-level pattern features provide a small but measurable improvement to the original model and may be especially useful when colour and low-level pattern features provide hosts with little information. Understanding the relative importance of low- and higher-level pattern features is a valuable goal for future work on animal coloration, especially in the contexts of mimicry, camouflage and individual recognition. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

I see your false colours: how artificial stimuli appear to different animal viewers.

The use of artificially coloured stimuli, especially to test hypotheses about sexual selection and anti-predator defence, has been common in behavioural ecology since the pioneering work of Tinbergen. To investigate the effects of colour on animal behaviour, many researchers use paints, markers and dyes to modify existing colours or to add colour to synthetic models. Because colour perception varies widely across species, it is critical to account for the signal receiver's vision when performing colour manipulations. To explore this, we applied 26 typical coloration products to different types of avian feathers. Next, we measured the artificially coloured feathers using two complementary techniques-spectrophotometry and digital ultraviolet--visible photography-and modelled their appearance to mammalian dichromats (ferret, dog), trichromats (honeybee, human) and avian tetrachromats (hummingbird, blue tit). Overall, artificial colours can have dramatic and sometimes unexpected effects on the reflectance properties of feathers, often differing based on feather type. The degree to which an artificial colour differs from the original colour greatly depends on an animal's visual system. 'White' paint to a human is not 'white' to a honeybee or blue tit. Based on our analysis, we offer practical guidelines for reducing the risk of introducing unintended effects when using artificial colours in behavioural experiments.

Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings.

We use a tetrahedral color space to describe and analyze male plumage color variation and evolution in a clade of New World buntings--Cyanocompsa and Passerina (Aves: Cardinalidae). The Goldsmith color space models the relative stimulation of the four retinal cones, using the integrals of the product of plumage reflectance spectra and cone sensitivity functions. A color is represented as a vector defined by the relative stimulation of the four cone types--ultraviolet, blue, green, and red. Color vectors are plotted in a tetrahedral, or quaternary, plot with the achromatic point at the origin and the ultraviolet/violet channel along the Z-axis. Each color vector is specified by the spherical coordinates theta, phi, and r. Hue is given by the angles theta and phi. Chroma is given by the magnitude of r, the distance from the achromatic origin. Color vectors of all distinct patches in a plumage characterize the plumage color phenotype. We describe the variation in color space occupancy of male bunting plumages, using various measures of color contrast, hue contrast and diversity, and chroma. Comparative phylogenetic analyses using linear parsimony (in MacClade) and generalized least squares (GLS) models (in CONTINUOUS) with a molecular phylogeny of the group document that plumage color evolution in the clade has been very dynamic. The single best-fit GLS evolutionary model of plumage color variation over the entire clade is a directional change model with no phylogenetic correlation among species. However, phylogenetic innovations in feather color production mechanisms--derived pheomelanin and carotenoid expression in two lineages--created new opportunities to colonize novel areas of color space and fostered the explosive differentiation in plumage color. Comparison of the tetrahedral color space of Goldsmith with that of Endler and Mielke demonstrates that both provide essentially identical results. Evolution of avian ultraviolet/violet opsin sensitivity in relation to chromatic experience is discussed.

Synchronization of speed, sound and iridescent color in a hummingbird aerial courtship dive.

Many animal signals are complex, often combining multimodal components with dynamic motion. To understand the function and evolution of these displays, it is vital to appreciate their spatiotemporal organization. Male broad-tailed hummingbirds (Selasphorus platycercus) perform dramatic U-shaped courtship dives over females, appearing to combine rapid movement and dive-specific mechanical noises with visual signals from their iridescent gorgets. To understand how motion, sound and color interact in these spectacular displays, we obtained video and audio recordings of dives performed by wild hummingbirds. We then applied a multi-angle imaging technique to estimate how a female would perceive the male's iridescent gorget throughout the dive. We show that the key physical, acoustic and visual aspects of the dive are remarkably synchronized-all occurring within 300 milliseconds. Our results highlight the critical importance of accounting for motion and orientation when investigating animal displays: speed and trajectory affect how multisensory signals are produced and perceived.