Revisiting the Baltimore-Bullock's Oriole hybrid zone reveals changing plumage colour in Bullock's Orioles.

Hybrid zones are dynamic areas where populations of two or more interbreeding species may change through an influx of novel genetic material resulting from hybridization or selection on standing genetic variation. Documenting changes in populations through time, however, is challenging because repeated samples are often missing or because long-term storage can affect trait morphologies, especially colour traits that may fade through time. We document a change in carotenoid-based orange breast feathers of Bullock's Orioles (Icterus bullockii) from the Great Plains hybrid zone, USA. Contemporary Bullock's Orioles are more orange than historic individuals from the same location sampled approximately 60 years ago. Spectrophotometry revealed that contemporary Bullock's Orioles resemble orange colour profiles of Baltimore Orioles (I. galbula), the species with which they hybridize. Fading or changes in diet hypotheses do not appear to explain the shift in colour we report for Bullock's Orioles. We propose that these changes in colour are facilitated through introgression with Baltimore Orioles, and favoured by females that choose brighter, more orange males. Our study highlights the long memory of natural history collections and how they offer new insights to the dynamic roll of hybrid zones in trait evolution between interacting species.

Sociality and migration predict hybridization across birds.

Hybridization represents a natural experiment that can provide insight into processes of speciation and diversification. Though considerable research has focused on hybrid zone dynamics, macroevolutionary investigations of the factors that influence hybridization are few. Here, we compile a database of avian hybrids and perform comparative analyses to determine whether several social and life-history variables influence broad patterns of hybridization. We perform three main analyses: phylogenetic logistic regression to examine variables that are associated with the presence of hybridization, phylogenetic Poisson regression of only those species exhibiting hybridization to determine which variables are associated with the extent of hybridization, and a phylogenetic logistic regression on a subset of data to assess potential pseudoreplication. After testing several social and life-history variables, we found that social bond duration is associated with the presence and extent of hybridization. Specifically, lengthy social bonds are negatively associated with the presence and extent of hybridization. In addition to social bond length, migration is positively linked with a greater likelihood of hybridization. The broad-scale correlations between species-specific traits and hybridization across diverse avian lineages suggest commonalities in the fine-scale processes involved in mating with heterospecifics, which in turn has implications for how we think about, study and understand hybridization processes and their influence on evolutionary trajectories.

Comparative bioacoustics: a roadmap for quantifying and comparing animal sounds across diverse taxa.

Animals produce a wide array of sounds with highly variable acoustic structures. It is possible to understand the causes and consequences of this variation across taxa with phylogenetic comparative analyses. Acoustic and evolutionary analyses are rapidly increasing in sophistication such that choosing appropriate acoustic and evolutionary approaches is increasingly difficult. However, the correct choice of analysis can have profound effects on output and evolutionary inferences. Here, we identify and address some of the challenges for this growing field by providing a roadmap for quantifying and comparing sound in a phylogenetic context for researchers with a broad range of scientific backgrounds. Sound, as a continuous, multidimensional trait can be particularly challenging to measure because it can be hard to identify variables that can be compared across taxa and it is also no small feat to process and analyse the resulting high-dimensional acoustic data using approaches that are appropriate for subsequent evolutionary analysis. Additionally, terminological inconsistencies and the role of learning in the development of acoustic traits need to be considered. Phylogenetic comparative analyses also have their own sets of caveats to consider. We provide a set of recommendations for delimiting acoustic signals into discrete, comparable acoustic units. We also present a three-stage workflow for extracting relevant acoustic data, including options for multivariate analyses and dimensionality reduction that is compatible with phylogenetic comparative analysis. We then summarize available phylogenetic comparative approaches and how they have been used in comparative bioacoustics, and address the limitations of comparative analyses with behavioural data. Lastly, we recommend how to apply these methods to acoustic data across a range of study systems. In this way, we provide an integrated framework to aid in quantitative analysis of cross-taxa variation in animal sounds for comparative phylogenetic analysis. In addition, we advocate the standardization of acoustic terminology across disciplines and taxa, adoption of automated methods for acoustic feature extraction, and establishment of strong data archival practices for acoustic recordings and data analyses. Combining such practices with our proposed workflow will greatly advance the reproducibility, biological interpretation, and longevity of comparative bioacoustic studies.

Ecological and geographical overlap drive plumage evolution and mimicry in woodpeckers.

Organismal appearances are shaped by selection from both biotic and abiotic drivers. For example, Gloger's rule describes the pervasive pattern that more pigmented populations are found in more humid areas. However, species may also converge on nearly identical colours and patterns in sympatry, often to avoid predation by mimicking noxious species. Here we leverage a massive global citizen-science database to determine how biotic and abiotic factors act in concert to shape plumage in the world's 230 species of woodpeckers. We find that habitat and climate profoundly influence woodpecker plumage, and we recover support for the generality of Gloger's rule. However, many species exhibit remarkable convergence explained neither by these factors nor by shared ancestry. Instead, this convergence is associated with geographic overlap between species, suggesting occasional strong selection for interspecific mimicry.

Evolution of correlated complexity in the radically different courtship signals of birds-of-paradise.

Ornaments used in courtship often vary wildly among species, reflecting the evolutionary interplay between mate preference functions and the constraints imposed by natural selection. Consequently, understanding the evolutionary dynamics responsible for ornament diversification has been a longstanding challenge in evolutionary biology. However, comparing radically different ornaments across species, as well as different classes of ornaments within species, is a profound challenge to understanding diversification of sexual signals. Using novel methods and a unique natural history dataset, we explore evolutionary patterns of ornament evolution in a group-the birds-of-paradise-exhibiting dramatic phenotypic diversification widely assumed to be driven by sexual selection. Rather than the tradeoff between ornament types originally envisioned by Darwin and Wallace, we found positive correlations among cross-modal (visual/acoustic) signals indicating functional integration of ornamental traits into a composite unit-the "courtship phenotype." Furthermore, given the broad theoretical and empirical support for the idea that systemic robustness-functional overlap and interdependency-promotes evolutionary innovation, we posit that birds-of-paradise have radiated extensively through ornamental phenotype space as a consequence of the robustness in the courtship phenotype that we document at a phylogenetic scale. We suggest that the degree of robustness in courtship phenotypes among taxa can provide new insights into the relative influence of sexual and natural selection on phenotypic radiations.

Visual Detection and Avoidance of Pathogenic Bacteria by Aphids.

Aphids are diverse sap-sucking insects [1] that can be serious agricultural pests and vectors of plant disease [2]. Some species, including pea aphids (Acyrthosiphon pisum), are susceptible to infection by epiphytic bacteria that are commonly found on plant surfaces [3-5]. Pea aphids appear unable to recover from these infections, possibly because pea aphids are missing apparent orthologs of some immune response genes [6], and these aphids exhibit relatively low immune responses after pathogen exposure [7]. We therefore tested the ability of pea aphids to use avoidance as a non-immunological defense against Pseudomonas syringae, a widespread plant epiphyte and aphid pathogen [8, 9]. Pea aphids avoided highly virulent strains of P. syringae, but not all strains, and avoidance led to a significant reduction in infection among aphids. We found that aphids can use visual cues to detect the ultraviolet (UV)-based fluorescence of the bacterial siderophore pyoverdine [10] produced by virulent strains. Avoided epiphytic bacteria caused light leaving the surface of leaves to be richer in wavelengths that were tightly linked to both aphid visual sensitivities and the fluorescent emission spectra of pyoverdine, suggesting that pyoverdine fluorescence mediates avoidance and may be a visual cue used by aphids to detect epiphytic pathogens. Although pyoverdine production in Pseudomonas species may be a broadly reliable indicator of bacterial virulence within the phyllosphere, it was not directly responsible for virulence to aphids. Aphids may be under selection to avoid fluorescence on leaves, a phenomenon with potential use for the control of agricultural pest insects.

Behavioral Evolution: Can You Dig It?

Behaviors are among the most complex phenotypes, making the genetic dissection of behavioral differences extremely challenging. A careful dissection of ontogenetic differences in burrowing behavior between mouse species highlights the importance of integrative approaches to the study of behavioral evolution.

Social costs enforce honesty of a dynamic signal of motivation.

Understanding the processes that promote signal reliability may provide important insights into the evolution of diverse signalling strategies among species. The signals that animals use to communicate must comprise mechanisms that prohibit or punish dishonesty, and social costs of dishonesty have been demonstrated for several fixed morphological signals (e.g. colour badges of birds and wasps). The costs maintaining the honesty of dynamic signals, which are more flexible and potentially cheatable, are unknown. Using an experimental manipulation of the dynamic visual signals used by male veiled chameleons (Chamaeleo calyptratus) during aggressive interactions, we tested the idea that the honesty of rapid colour change signals is maintained by social costs. Our results reveal that social costs are an important mechanism maintaining the honesty of these dynamic colour signals-'dishonest' chameleons whose experimentally manipulated coloration was incongruent with their contest behaviour received more physical aggression than 'honest' individuals. This is the first demonstration, to the best our knowledge, that the honesty of a dynamic signal of motivation-physiological colour change-can be maintained by the social costliness of dishonesty. Behavioural responses of signal receivers, irrespective of any specific detection mechanisms, therefore prevent chameleon cheaters from prospering.

Evolutionary innovation and diversification of carotenoid-based pigmentation in finches.

The ornaments used by animals to mediate social interactions are diverse, and by reconstructing their evolutionary pathways we can gain new insights into the mechanisms underlying ornamental innovation and variability. Here, we examine variation in plumage carotenoids among the true finches (Aves: Fringillidae) using biochemical and comparative phylogenetic analyses to reconstruct the evolutionary history of carotenoid states and evaluate competing models of carotenoid evolution. Our comparative analyses reveal that the most likely ancestor of finches used dietary carotenoids as yellow plumage colorants, and that the ability to metabolically modify dietary carotenoids into more complex pigments arose secondarily once finches began to use modified carotenoids to create red plumage. Following the evolutionary "innovation" that enabled modified red carotenoid pigments to be deposited as plumage colorants, many finch species subsequently modified carotenoid biochemical pathways to create yellow plumage. However, no reversions to dietary carotenoids were observed. The finding that ornaments and their underlying mechanisms may be operating under different selection regimes-where ornamental trait colors undergo frequent reversions (e.g., between red and yellow plumage) while carotenoid metabolization mechanisms are more conserved-supports a growing empirical framework suggesting different evolutionary patterns for ornaments and the mechanistic innovations that facilitate their diversification.

Body mass and immune function, but not bill coloration, predict dominance in female mallards.

Competition over indivisible resources is common and often costly. Therefore, selection should favor strategies, including efficient communication, that minimize unnecessary costs associated with such competition. For example, signaling enables competitors to avoid engaging in costly asymmetrical contests. Recently, bill coloration has been identified as an information-rich signal used by some birds to mediate aggressive interactions and we evaluated this possibility in female mallards Anas platyrhynchos. Specifically, we conducted two rounds of competitive interactions among groups of unfamiliar adult female ducks. By recording all aggressive behaviors exhibited by each individual, as well as the identity of attack recipients, we were able to assign dominance scores and evaluate links between numerous physiological, morphological, and experimental variables that we predicted would influence contest outcome and dominance. Contrary to our predictions, dominance was not linked to any aspect of bill coloration, access to dietary carotenoids during development, two of three measures of immune function, or ovarian follicle maturation. Instead, heavier birds were more dominant, as were those with reduced immune system responses to an experimentally administered external immunostimulant, phytohemagglutinin. These results suggest that visual signals are less useful during the establishment of dominance hierarchies within multi-individual scramble competitions, and that immune function is correlated with contest strategies in competitions for access to limited resources.

Biochemical regulation of pigment motility in vertebrate chromatophores: a review of physiological color change mechanisms.

The fundamental unit of rapid, physiological color change in vertebrates is the dermal chromatophore unit. This unit, comprised of cellular associations between different chromatophore types, is relatively conserved across the fish, amphibian, and reptilian species capable of physiological color change and numerous attempts have been made to understand the nature of the four major chromatophore types (melanophores, erythrophores, xanthophores, and iridophores) and their biochemical regulation. In this review, we attempt to describe the current state of knowledge regarding what classifies a pigment cell as a dynamic chromatophore, the unique characteristics of each chromatophore type, and how different hormones, neurotransmitters, or other signals direct pigment reorganization in a variety of vertebrate taxa.

Interactions between Biliverdin, Oxidative Damage, and Spleen Morphology after Simulated Aggressive Encounters in Veiled Chameleons.

Stressors frequently increase oxidative damage--unless organisms simultaneously mount effective antioxidant responses. One putative mitigative mechanism is the use of biliverdin, an antioxidant produced in the spleen during erythrocyte degradation. We hypothesized that both wild and captive-bred male veiled chameleons (Chamaeleo calyptratus), which are highly aggressive to conspecifics, would respond to agonistic displays with increased levels of oxidative damage, but that increased levels of biliverdin would limit this increase. We found that even just visual exposure to a potential combatant resulted in decreased body mass during the subsequent 48-hour period, but that hematocrit, biliverdin concentration in the bile, relative spleen size, and oxidative damage in plasma, liver, and spleen were unaffected. Contrary to our predictions, we found that individuals with smaller spleens exhibited greater decreases in hematocrit and higher bile biliverdin concentrations, suggesting a revision to the idea of spleen-dependent erythrocyte processing. Interestingly, individuals with larger spleens had reduced oxidative damage in both the liver and spleen, demonstrating the spleen's importance in modulating oxidative damage. We also uncovered differences in spleen size and oxidative damage between wild and captive-bred chameleons, highlighting environmentally dependent differences in oxidative physiology. Lastly, we found no relationship between oxidative damage and biliverdin concentration, calling into question biliverdin's antioxidant role in this species.

The effect of carotenoid supplementation on immune system development in juvenile male veiled chameleons (Chamaeleo calyptratus).

INTRODUCTION: Nutrient availability, assimilation, and allocation can have important and lasting effects on the immune system development of growing animals. Though carotenoid pigments have immunostimulatory properties in many animals, relatively little is known regarding how they influence the immune system during development. Moreover, studies linking carotenoids to health at any life stage have largely been restricted to birds and mammals. We investigated the effects of carotenoid supplementation on multiple aspects of immunity in juvenile veiled chameleons (Chamaeleo calyptratus). We supplemented half of the chameleons with lutein (a xanthophyll carotenoid) for 14 weeks during development and serially measured multiple aspects of immune function, including: agglutination and lysis performance of plasma, wound healing, and plasma nitric oxide concentrations before and after wounding. RESULTS: Though lutein supplementation effectively elevated circulating carotenoid concentrations throughout the developmental period, we found no evidence that carotenoid repletion enhanced immune function at any point. However, agglutination and lysis scores increased, while baseline nitric oxide levels decreased, as chameleons aged. CONCLUSIONS: Taken together, our results indicate that body mass and age, but not carotenoid access, may play an important role in immune performance of growing chameleons. Hence, studying well-understood physiological processes in novel taxa can provide new perspectives on alternative physiological processes and nutrient function.

Chameleons communicate with complex colour changes during contests: different body regions convey different information.

Many animals display static coloration (e.g. of feathers or fur) that can serve as a reliable sexual or social signal, but the communication function of rapidly changing colours (as in chameleons and cephalopods) is poorly understood. We used recently developed photographic and mathematical modelling tools to examine how rapid colour changes of veiled chameleons Chamaeleo calyptratus predict aggressive behaviour during male-male competitions. Males that achieved brighter stripe coloration were more likely to approach their opponent, and those that attained brighter head coloration were more likely to win fights; speed of head colour change was also an important predictor of contest outcome. This correlative study represents the first quantification of rapid colour change using organism-specific visual models and provides evidence that the rate of colour change, in addition to maximum display coloration, can be an important component of communication. Interestingly, the body and head locations of the relevant colour signals map onto the behavioural displays given during specific contest stages, with lateral displays from a distance followed by directed, head-on approaches prior to combat, suggesting that different colour change signals may evolve to communicate different information (motivation and fighting ability, respectively).

Invasive ants alter foraging and parental behaviors of a native bird.

Introduced species can exert outsized impacts on native biota through both direct (predation) and indirect (competition) effects. Ants frequently become established in new areas after being transported by humans across traditional biological or geographical barriers, and a prime example of such establishment is the red imported fire ant (Solenopsis invicta). Introduced to North America in the 1930's, red imported fire ants are now firmly established throughout the southeastern United States. Although these invasive predators can dramatically impact native arthropods, their effect on vertebrates through resource competition is essentially unknown. Using a paired experimental design, we compared patterns of foraging and rates of provisioning for breeding eastern bluebirds (Sialia sialis) in unmanipulated (control) territories to those in adjacent (treated) territories where fire ants were experimentally reduced. Bluebirds inhabiting treated territories foraged nearer their nests and provisioned offspring more frequently than bluebirds inhabiting control territories with unmanipulated fire ant levels. Additionally, nestlings from treated territories were in better condition than those from control territories, though these differences were largely confined to early development. The elimination of significant differences in body condition towards the end of the nestling period suggests that bluebird parents in control territories were able to make up the food deficit caused by fire ants, potentially by working harder to adequately provision their offspring. The relationship between fire ant abundance and bluebird behavior hints at the complexity of ecological communities and suggests negative effects of invasive species are not limited to taxa with which they have direct contact.

Invasive fire ants reduce reproductive success and alter the reproductive strategies of a native vertebrate insectivore.

BACKGROUND: Introduced organisms can alter ecosystems by disrupting natural ecological relationships. For example, red imported fire ants (Solenopsis invicta) have disrupted native arthropod communities throughout much of their introduced range. By competing for many of the same food resources as insectivorous vertebrates, fire ants also have the potential to disrupt vertebrate communities. METHODOLOGY/PRINCIPAL FINDINGS: To explore the effects of fire ants on a native insectivorous vertebrate, we compared the reproductive success and strategies of eastern bluebirds (Sialia sialis) inhabiting territories with different abundances of fire ants. We also created experimental dyads of adjacent territories comprised of one territory with artificially reduced fire ant abundance (treated) and one territory that was unmanipulated (control). We found that more bluebird young fledged from treated territories than from adjacent control territories. Fire ant abundance also explained significant variation in two measures of reproductive success across the study population: number of fledglings and hatching success of second clutches. Furthermore, the likelihood of bluebird parents re-nesting in the same territory was negatively influenced by the abundance of foraging fire ants, and parents nesting in territories with experimentally reduced abundances of fire ants produced male-biased broods relative to pairs in adjacent control territories. CONCLUSIONS/SIGNIFICANCE: Introduced fire ants altered both the reproductive success (number of fledglings, hatching success) and strategies (decision to renest, offspring sex-ratio) of eastern bluebirds. These results illustrate the negative effects that invasive species can have on native biota, including species from taxonomically distant groups.

Host reproductive phenology drives seasonal patterns of host use in mosquitoes.

Seasonal shifts in host use by mosquitoes from birds to mammals drive the timing and intensity of annual epidemics of mosquito-borne viruses, such as West Nile virus, in North America. The biological mechanism underlying these shifts has been a matter of debate, with hypotheses falling into two camps: (1) the shift is driven by changes in host abundance, or (2) the shift is driven by seasonal changes in the foraging behavior of mosquitoes. Here we explored the idea that seasonal changes in host use by mosquitoes are driven by temporal patterns of host reproduction. We investigated the relationship between seasonal patterns of host use by mosquitoes and host reproductive phenology by examining a seven-year dataset of blood meal identifications from a site in Tuskegee National Forest, Alabama USA and data on reproduction from the most commonly utilized endothermic (white-tailed deer, great blue heron, yellow-crowned night heron) and ectothermic (frogs) hosts. Our analysis revealed that feeding on each host peaked during periods of reproductive activity. Specifically, mosquitoes utilized herons in the spring and early summer, during periods of peak nest occupancy, whereas deer were fed upon most during the late summer and fall, the period corresponding to the peak in births for deer. For frogs, however, feeding on early- and late-season breeders paralleled peaks in male vocalization. We demonstrate for the first time that seasonal patterns of host use by mosquitoes track the reproductive phenology of the hosts. Peaks in relative mosquito feeding on each host during reproductive phases are likely the result of increased tolerance and decreased vigilance to attacking mosquitoes by nestlings and brooding adults (avian hosts), quiescent young (avian and mammalian hosts), and mate-seeking males (frogs).

Vector-host interactions in avian nests: do mosquitoes prefer nestlings over adults?

The hypothesis that nestlings are a significant driver of arbovirus transmission and amplification is based upon findings that suggest nestlings are highly susceptible to being fed upon by vector mosquitoes and to viral infection and replication. Several previous studies have suggested that nestlings are preferentially fed upon relative to adults in the nest, and other studies have reported a preference for adults over nestlings. We directly tested the feeding preference of nestling and adult birds in a natural setting, introducing mosquitoes into nesting boxes containing eastern bluebirds (Sialia sialis), collecting blood-fed mosquitoes, and matching the source of mosquito blood meals to individual birds using microsatellite markers. Neither nestlings nor adults were fed upon to an extent significantly greater than would be predicted based upon their relative abundance in the nests, although feeding upon mothers decreased as the age of the nestlings increased.

Sex-biased parental investment is correlated with mate ornamentation in eastern bluebirds.

Males typically have greater variance in reproductive success than females, so mothers should benefit by producing sons under favorable conditions. Being paired with a better-than-average mate is one such favorable circumstance. High-quality fathers can improve conditions for their offspring by providing good genes, good resources, or both, so females paired to such males should invest preferentially in sons. Ornamentation has been linked to male quality in many birds and, in support of differential allocation theory, females of several avian species invest more in entire broods when paired to attractive mates. Additionally, the females of some bird species apparently manipulate the primary sex-ratio of their broods in relation to the attractiveness of their mates. However, empirical support for a link between mate ornamentation and preferential feeding of sons (another form of biased investment) is lacking. We tested for correlations between sex-biased parental investment and mate plumage colour in the eastern bluebird (Sialia sialis), a species in which juveniles have sexually dichromatic UV-blue plumage. We found that the proportion of maternal feeding attempts to fledgling sons (versus fledgling daughters) was positively correlated with structurally coloured plumage ornamentation of fathers. Additionally, paternal feeding attempts to sons were correlated with plumage ornamentation of mothers and increased in fathers exhibiting breast plumage characteristics typical of older males. These results provide further support for the idea that parental strategies are influenced by mate attractiveness and provide the first evidence that mate ornamentation can influence parental behavior even after offspring have left the nest.