Pathways to elaboration of sexual dimorphism in bird plumage patterns

Patterns, such as bars and spots, are common in birds. Some patterns can function in camouflage and/or communication and can benefit both males and females, paving the way for elaboration in sexual dimorphism. Historically, sexual dichromatism was predominantly considered to be a consequence of mating systems. However, the distribution of traits between the sexes is not always indicative of function; genetic correlation may cause traits to evolve in both sexes and traits may serve a social function in males and/or females. In addition, sexual dichromatism in bird plumage patterns can be composed of multiple types of patterns within and/or between the sexes. Therefore, there can be more than one type of dimorphism and some are more elaborate than others. Under classical models of genetic correlation, patterns evolve in both sexes followed by a loss of patterning in one sex. Elaborate types of sexual dimorphism in plumage patterns may be due to selection acting on existing patterns and are perhaps derived. Waterfowl (Anseriformes) and gamebirds (Galliformes) arguably have the most striking plumage patterns. Using 288 species from these orders I reconstructed the evolutionary history of plumage pattern dimorphism. There was little support for genetic correlation but elaborate types of dimorphism are probably derived. Backward and forward evolutionary transitions between different types of dimorphism can occur by loss or elaboration. These results demonstrate that plumage patterns are evolutionary labile and current forms may represent shifting adaptations to a changing environment. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 262–273.     

Insight into glycan diversity and evolutionary lineage based on comparative Avio-N-glycomics and sialic acid analysis of 88 egg whites of Galloanserae

A large set of glycome information was obtained from egg white proteins of 88 samples from Galloanserae (63 Anseriformes and 25 Galliformes). The data were obtained on whole N-glycan structures and types of sialic acids of these egg whites by glycoblotting-based high-throughput and quantitative glycomics. The results revealed clear trends and complexity patterns as well as diversity among taxonomic groups. It is well-known that chicken, a representative domesticated poultry involved in Galliformes, can become an influenza host. However, our data demonstrate that duck, wild goose, and swan of Anseriformes are representative migratory birds that are known as natural hosts of the influenza virus. Hierarchical clustering analysis of the expression pattern of N-glycome (total of 61 N-glycan peaks) revealed that the members of Galloanserae can be classified into two major groups and five submajor clusters (clusters 1-5) on the basis of simple m/z values obtained by MALDI-TOF MS. It is clear that expression patterns of N-glycomes in the five clusters are influenced significantly by the features such as the body size of the birds, rather than by the difference of the family. On the other hand, quantitative analysis showed that the total amounts of sialic acids in egg whites of Galliformes were distinctly larger than those of Anseriformes. However, it was also revealed in Anseriformes that Neu5Gc and KDN, in addition to common Neu5Ac, were expressed significantly in both N- and O-glycans of glycoproteins and glycosphingolipids, suggesting the influence of their lifestyles and diet. This is the first report that KDN exists in egg white. These results and the environmental factors are discussed preliminarily with respect to their evolutionary lineage.     

Using deep neural networks to model similarity between visual patterns: Application to fish sexual signals

The evolution of visual patterns is a frontier in the theory of sexual selection as we seek to understand the function of complex visual patterning in courtship. Recently, the sensory drive and sensory bias models of sexual selection have been applied to higher-level visual processing. One prediction of this application is that animals' sexual signals will mimic the visual statistics of their habitats. An enduring difficulty of testing predictions of visual pattern evolution is in developing quantitative methods for comparing patterns. Advances in artificial neural networks address this challenge by allowing for the direct comparison of images using both simple and complex features. Here, we use VGG19, an industry‑leading image classification network to test predictions of sensory drive, by comparing visual patterns in darter fish (Etheostoma spp.) to images of their habitats. We find that images of female darters are significantly more similar to images of their habitat than are images of males, supporting a role of camouflage in female patterning. We do not find direct evidence for sensory drive shaping the design of male patterns; however, this work demonstrates the utility of network methods for pattern analysis and suggests future directions for visual pattern research.     

Why the leopard got its spots: relating pattern development to ecology in felids

A complete explanation of the diversity of animal colour patterns requires an understanding of both the developmental mechanisms generating them and their adaptive value. However, only two previous studies, which involved computer-generated evolving prey, have attempted to make this link. This study examines variation in the camouflage patterns displayed on the flanks of many felids. After controlling for the effects of shared ancestry using a fully resolved molecular phylogeny, this study shows how phenotypes from plausible felid coat pattern generation mechanisms relate to ecology. We found that likelihood of patterning and pattern attributes, such as complexity and irregularity, were related to felids' habitats, arboreality and nocturnality. Our analysis also indicates that disruptive selection is a likely explanation for the prevalence of melanistic forms in Felidae. Furthermore, we show that there is little phylogenetic signal in the visual appearance of felid patterning, indicating that camouflage adapts to ecology over relatively short time scales. Our method could be applied to any taxon with colour patterns that can reasonably be matched to reaction-diffusion and similar models, where the kinetics of the reaction between two or more initially randomly dispersed morphogens determines the outcome of pattern development.     

A phylogenetic supertree of the fowls (Galloanserae, Aves)

The fowls (Anseriformes and Galliformes) comprise one of the major lineages of birds and occupy almost all biogeographical regions of the world. The group contains the most economically important of all bird species, each with a long history of domestication, and is an ideal model for studying ecological and evolutionary patterns. Yet, despite the relatively large amount of systematic attention fowls have attracted because of their socio‐economic and biological importance, the species‐level relationships within this clade remain controversial. Here we used the supertree method matrix representation with parsimony to generate a robust estimate of species‐level relationships of fowls. The supertree represents one of the most comprehensive estimates for the group to date, including 376 species (83.2% of all species; all 162 Anseriformes and 214 Galliformes) and all but one genera. The supertree was well‐resolved (81.1%) and supported the monophyly of both Anseriformes and Galliformes. The supertree supported the partitioning of Anseriformes into the three traditional families Anhimidae, Anseranatidae, and Anatidae, although it provided relatively poor resolution within Anatidae. For Galliformes, the majority‐rule supertree was largely consistent with the hypothesis of sequential sister‐group relationships between Megapodiidae, Cracidae, and the remaining Galliformes. However, our species‐level supertree indicated that more than 30% of the polytypic genera examined were not monophyletic, suggesting that results from genus‐level comparative studies using the average of the constituent species’ traits should be interpreted with caution until analogous species‐level comparative studies are available. Poorly resolved areas of the supertree reflect gaps or outstanding conflict within the existing phylogenetic database, highlighting areas in need of more study in addition to those species not present on the tree at all due to insufficient information. Even so, our supertree will provide a valuable foundation for understanding the diverse biology of fowls in a robust phylogenetic framework.     

The evolution of patterning during movement in a large-scale citizen science game

The motion dazzle hypothesis posits that high contrast geometric patterns can cause difficulties in tracking a moving target and has been argued to explain the patterning of animals such as zebras. Research to date has only tested a small number of patterns, offering equivocal support for the hypothesis. Here, we take a genetic programming approach to allow patterns to evolve based on their fitness (time taken to capture) and thus find the optimal strategy for providing protection when moving. Our ‘Dazzle Bug’ citizen science game tested over 1.5 million targets in a touch screen game at a popular visitor attraction. Surprisingly, we found that targets lost pattern elements during evolution and became closely background matching. Modelling results suggested that targets with lower motion energy were harder to catch. Our results indicate that low contrast, featureless targets offer the greatest protection against capture when in motion, challenging the motion dazzle hypothesis.     

Cuttlefish camouflage: context-dependent body pattern use during motion

It is virtually impossible to camouflage a moving target against a non-uniform background, but strategies have been proposed to reduce detection and targeting of movement. Best known is the idea that high contrast markings produce ‘motion dazzle’, which impairs judgement of speed and trajectory. The ability of the cuttlefish Sepia officinalis to change its visual appearance allows us to compare the animal''s choice of patterns during movement to the predictions of models of motion camouflage. We compare cuttlefish body patterns used during movement with those expressed when static on two background types; one of which promotes low-contrast mottle patterns and the other promotes high-contrast disruptive patterns. We find that the body pattern used during motion is context-specific and that high-contrast body pattern components are significantly reduced during movement. Thus, in our experimental conditions, cuttlefish do not use high contrast motion dazzle. It may be that, in addition to being inherently conspicuous during movement, moving high-contrast patterns will attract attention because moving particles in coastal waters tend to be of small size and of low relative contrast.     

Ecological,behavioral, and phylogenetic influences on the evolution of dorsal color pattern in geckos*

The dorsal surfaces of many taxonomic groups often feature repetitive pattern elements consisting of stripes, spots, or bands. Here, we investigate how distinct categories of camouflage pattern work by relating them to ecological and behavioral traits in 439 species of gecko. We use phylogenetic comparative methods to test outstanding hypotheses based on camouflage theory and research in other taxa. We found that bands are associated with nocturnal activity, suggesting bands provide effective camouflage for motionless geckos resting in refugia during the day. A predicted association between stripes and diurnal activity was not supported, suggesting that stripes do not work via dazzle camouflage mechanisms in geckos. This, along with a lack of support for our prediction that plain patterning should be associated with open habitats, suggests that similar camouflage patterns do not work in consistent ways across taxa. We also found that plain and striped lineages frequently switched between using open or closed habitats, whereas spotted lineages rarely transitioned. This suggests that pattern categories differ in how specialized or generalized their camouflage is. This result has ramifications for theory on how camouflage compromises to background heterogeneity and how camouflage pattern might influence evolutionary trajectories.     

The dual function of barred plumage in birds: camouflage and communication

A commonly held principle in visual ecology is that communication compromises camouflage: while visual signals are often conspicuous, camouflage provides concealment. However, some traits may have evolved for communication and camouflage simultaneously, thereby overcoming this functional compromise. Visual patterns generally provide camouflage, but it was suggested that a particular type of visual pattern – avian barred plumage – could also be a signal of individual quality. Here, we test if the evolution of sexual dimorphism in barred plumage, as well as differences between juvenile and adult plumage, indicate camouflage and/or signalling functions across the class Aves. We found a higher frequency of female- rather than male-biased sexual dimorphism in barred plumage, indicating that camouflage is its most common function. But we also found that, compared to other pigmentation patterns, barred plumage is more frequently biased towards males and its expression more frequently restricted to adulthood, suggesting that barred plumage often evolves or is maintained as a sexual communication signal. This illustrates how visual traits can accommodate the apparently incompatible functions of camouflage and communication, which has implications for our understanding of avian visual ecology and sexual ornamentation.     

Adaptive body patterning,three‐dimensional skin morphology and camouflage measures of the slender filefish Monacanthus tuckeri on a Caribbean coral reef

The slender filefish is a master of adaptive camouflage and can change its appearance within 1–3 s. Videos and photographs of this animal's cryptic body patterning and behavior were collected in situ under natural light on a Caribbean coral reef. We present an ethogram of body patterning components that includes large‐ and small‐scale spots, stripes and bars that confer a variety of cryptic patterns amidst a range of complex backgrounds. Field images were analyzed to investigate two aspects of camouflage effectiveness: (1) the degree of colour resemblance between animals and their nearby visual stimuli; and (2) the visibility of each fish's actual body outline vs. its illusory outline. Most animals more closely matched the colour of nearby visual stimuli than that of the surrounding background. Three‐dimensional dermal flaps complement the melanophore skin patterns by enhancing the complexity of the fish's physical skin texture to disguise its actual body shape, and the morphology of these structures was studied. The results suggest that the body patterns, skin texture, postures and swimming orientations putatively hinder both the detection and recognition of the fish by potential visual predators. Overall, the rapid speed of change of multiple patterns, colour blending with nearby backgrounds, and the physically complicated edge produced by dermal flaps effectively camouflage this animal among soft corals and macroalgae in the Caribbean Sea.     

Cuttlefish dynamic camouflage: responses to substrate choice and integration of multiple visual cues

Prey camouflage is an evolutionary response to predation pressure. Cephalopods have extensive camouflage capabilities and studying them can offer insight into effective camouflage design. Here, we examine whether cuttlefish, Sepia officinalis, show substrate or camouflage pattern preferences. In the first two experiments, cuttlefish were presented with a choice between different artificial substrates or between different natural substrates. First, the ability of cuttlefish to show substrate preference on artificial and natural substrates was established. Next, cuttlefish were offered substrates known to evoke three main camouflage body pattern types these animals show: Uniform or Mottle (function by background matching); or Disruptive. In a third experiment, cuttlefish were presented with conflicting visual cues on their left and right sides to assess their camouflage response. Given a choice between substrates they might encounter in nature, we found no strong substrate preference except when cuttlefish could bury themselves. Additionally, cuttlefish responded to conflicting visual cues with mixed body patterns in both the substrate preference and split substrate experiments. These results suggest that differences in energy costs for different camouflage body patterns may be minor and that pattern mixing and symmetry may play important roles in camouflage.     

Elements of butterfly wing patterns

The color patterns on the wings of butterflies are unique among animal color patterns in that the elements that make up the overall pattern are individuated. Unlike the spots and stripes of vertebrate color patterns, the elements of butterfly wing patterns have identities that can be traced from species to species, and typically across genera and families. Because of this identity it is possible to recognize homologies among pattern elements and to study their evolution and diversification. Individuated pattern elements evolved from non-individuated precursors by compartmentalization of the wing into areas that became developmentally autonomous with respect to color pattern formation. Developmental compartmentalization led to the evolution of serially repeated elements and the emergence of serial homology. In these compartments, serial homologues were able to acquire site-specific developmental regulation and this, in turn, allowed them to diverge morphologically. Compartmentalization of the wing also reduced the developmental correlation among pattern elements. The release from this developmental constraint, we believe, enabled the great evolutionary radiation of butterfly wing patterns. During pattern evolution, the same set of individual pattern elements is arranged in novel ways to produce species-specific patterns, including such adaptations as mimicry and camouflage.     

Putting the pH into phosphatidic acid signaling

Background

Camouflage patterns that hinder detection and/or recognition by antagonists are widely studied in both human and animal contexts. Patterns of contrasting stripes that purportedly degrade an observer's ability to judge the speed and direction of moving prey ('motion dazzle') are, however, rarely investigated. This is despite motion dazzle having been fundamental to the appearance of warships in both world wars and often postulated as the selective agent leading to repeated patterns on many animals (such as zebra and many fish, snake, and invertebrate species). Such patterns often appear conspicuous, suggesting that protection while moving by motion dazzle might impair camouflage when stationary. However, the relationship between motion dazzle and camouflage is unclear because disruptive camouflage relies on high-contrast markings. In this study, we used a computer game with human subjects detecting and capturing either moving or stationary targets with different patterns, in order to provide the first empirical exploration of the interaction of these two protective coloration mechanisms.

Results

Moving targets with stripes were caught significantly less often and missed more often than targets with camouflage patterns. However, when stationary, targets with camouflage markings were captured less often and caused more false detections than those with striped patterns, which were readily detected.

Conclusions

Our study provides the clearest evidence to date that some patterns inhibit the capture of moving targets, but that camouflage and motion dazzle are not complementary strategies. Therefore, the specific coloration that evolves in animals will depend on how the life history and ontogeny of each species influence the trade-off between the costs and benefits of motion dazzle and camouflage.     

Size and structure of the bird genome--I. DNA content of 48 species of Neognathae

The nuclear DNA content was evaluated in 48 species of Neognathae birds belonging to 13 orders, namely Anseriformes, Charadriiformes, Columbiformes, Ciconiiformes, Falconiformes, Galliformes, Gruiformes, Passeriformes, Pelicaniformes, Phoenicopteriformes, Piciformes, Psittaciformes and Strigiformes. The DNA content, expressed in pg/nucleus, ranges from 2.81 to 4.97. The genome size variability within and among families is discussed on the basis of the Hinegardner's (1976) model of genome evolution.     

SEXUAL SELECTION AND THE EVOLUTION OF COMPLEX COLOR PATTERNS IN DRAGON LIZARDS

Many species have elaborate and complex coloration and patterning, which often differ between the sexes. Sexual selection may increase the size or intensity of color patches (elaboration) in one sex or drive the evolution of novel signal elements (innovation). The latter potentially increases color pattern complexity. Color pattern complexity may also be influenced by ecological factors related to predation and environment; however, very few studies have investigated the effects of both sexual and natural selection on color pattern complexity across species. We used a phylogenetic comparative approach to examine these effects in 85 species and subspecies of Australian dragon lizards (family Agamidae). We quantified color pattern complexity by adapting the Shannon–Wiener diversity index. There were clear sex differences in color pattern complexity, which were positively correlated with both sexual dichromatism and sexual size dimorphism, consistent with the idea that sexual selection plays a significant role in the evolution of color pattern complexity. By contrast, we found little evidence of a link between environmental factors and color pattern complexity on body regions exposed to predators. Our results suggest that sexual selection rather than natural selection has led to increased color pattern complexity in males.     

Dazzle camouflage affects speed perception

Movement is the enemy of camouflage: most attempts at concealment are disrupted by motion of the target. Faced with this problem, navies in both World Wars in the twentieth century painted their warships with high contrast geometric patterns: so-called "dazzle camouflage". Rather than attempting to hide individual units, it was claimed that this patterning would disrupt the perception of their range, heading, size, shape and speed, and hence reduce losses from, in particular, torpedo attacks by submarines. Similar arguments had been advanced earlier for biological camouflage. Whilst there are good reasons to believe that most of these perceptual distortions may have occurred, there is no evidence for the last claim: changing perceived speed. Here we show that dazzle patterns can distort speed perception, and that this effect is greatest at high speeds. The effect should obtain in predators launching ballistic attacks against rapidly moving prey, or modern, low-tech battlefields where handheld weapons are fired from short ranges against moving vehicles. In the latter case, we demonstrate that in a typical situation involving an RPG7 attack on a Land Rover the reduction in perceived speed is sufficient to make the grenade miss where it was aimed by about a metre, which could be the difference between survival or not for the occupants of the vehicle.     

Control of the Cranio-Cervical System During Feeding in Birds

The avian neck is a complex, kinematically redundant system,which plays a role during inter alia food prehension and manipulation.Kinematical analysis shows that chickens (Gallus domesticus)move their vertebrae according to a geometric principle thatmaximizes angular rotation efficiency. The movement patternshows simultaneous rotations in some joints, while not in theothers. Anseriformes show a pattern of successive, rather thansimultaneous rotations in the rostral part of the neck. A kinematicalmodel indicates that the geometric principle produces an anseriform-likepattern only if a constraint on the movement of the caudal vertebraeis introduced. The strength of this constraint, required fora realistic simulation, is related to the amount of stretchin the long dorsal neck muscles (M. biventer and M. longus collidorsalis), which have a different configuration in Anseriformescompared to the chicken. To investigate whether the differencein movement pattern is a result of differences in anatomy only,or also of differences in neuromotor patterns, the EMG-patternsof the neck muscles of the mallard and chicken during drinkingand pecking were studied. Considerable overlap in the activityof antagonists is found in mallards, but not in chickens. Musclesin the rostral part of the neck are activated successively inmallards, but simultaneously in chickens. We conclude that thedifference in movement patterning between chickens and Anseriformes,results from both a difference in the control system of theneck, and a difference in the anatomy. The anseriform patternis found in water as well as on land, which suggests that neckmovement in both environments is controlled by the same neuromotorpatterns. The modifications in motor control system and anatomyof the Anseriformes may have evolved as an adaptation to aquaticfeeding, since the anseriform pattern is energetically morebeneficial in an aquatic environment than on land.     

Ossification sequence of the avian order anseriformes,with comparison to other precocial birds

Ossification sequences are poorly known for most amniotes, and yet they represent an important source of morphogenetic, phylogenetic, and life history information. Here, the author describes the ossification sequences of three ducks, the Common Eider Somateria mollissima dresseri, the Pekin Duck Anas platyrhynchos, and the Muscovy Duck Cairina moschata. Sequence differences exist both within and among these species, but are generally minor. The Common Eider has the most ossified skeleton prior to hatching, contrary to what is expected in a subarctic migrant species. This may be attributed to a tradeoff between growth rate and locomotory performance. Growth rate is higher in hatchlings with more cartilaginous skeletons, but this may compromise locomotion. No major ossification sequence differences were observed in the craniofacial skeleton when compared with Galliformes, which suggests that the influence of adult morphology on ossification sequence might be relatively minor in many taxa. Galliformes and Anseriformes, while both highly ossified at hatching, differ in the location of their late‐stage ossification centers. In Anseriformes, these are most often located in the appendicular skeleton, whereas in Galliformes they are in the thoracic region and form the ventilatory apparatus. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Evolution of preproinsulin gene in birds

The coding region of the preproinsulin gene has been cloned and partly sequenced in a variety of marine and terrestrial birds (28 species). All genes showed the "ancestral" structure with a large intron-2. The size of intron-2 changed considerably during the evolution of birds (2.4-4.2kb). The hydrophobicity of signal peptides was conserved. Bird C-peptides were predicted to be 28 amino acids long, but circulating C-peptides would be only 26 amino acids long, with Passer as a possible exception. Bird C-peptides were found to lack the sequences identified in mammals as responsible for peptide bioactivity and the structure of the central part. In contrast, predicted insulin sequences were highly conserved. Only two types of analog were identified: the hypoactive form (GluA8), present only in Anseriformes and the hyperactive form (His A8), present in all other species. Based on 3'-nucleotide sequence analysis (extending into intron-2), birds appeared to be monophyletic. Five groups were clearly identified: Paleognathae, Galliformes, Anseriformes, Passeriformes, and Charadriiformes. Paleognathae were suggested as the basal group, supporting the traditional view of avian evolution. Subsequent branching identified a gallo-anserae group and a group containing all other Neognathae. Surprisingly, Columba livia (Columbiforme order) clustered with Galliformes. With represented species, Procellariiformes and possibly Ciconiiformes, and Pelicaniformes were suggested as paraphyletic, in agreement with conclusions from some studies based on mitochondrial DNA sequences.     

Cognition and the evolution of camouflage

Camouflage is one of the most widespread forms of anti-predator defence and prevents prey individuals from being detected or correctly recognized by would-be predators. Over the past decade, there has been a resurgence of interest in both the evolution of prey camouflage patterns, and in understanding animal cognition in a more ecological context. However, these fields rarely collide, and the role of cognition in the evolution of camouflage is poorly understood. Here, we review what we currently know about the role of both predator and prey cognition in the evolution of prey camouflage, outline why cognition may be an important selective pressure driving the evolution of camouflage and consider how studying the cognitive processes of animals may prove to be a useful tool to study the evolution of camouflage, and vice versa. In doing so, we highlight that we still have a lot to learn about the role of cognition in the evolution of camouflage and identify a number of avenues for future research.