Cumulative cultural evolution and mechanisms for cultural selection in wild bird songs.

Cumulative cultural evolution, the accumulation of sequential changes within a single socially learned behaviour that results in improved function, is prominent in humans and has been documented in experimental studies of captive animals and managed wild populations. Here, we provide evidence that cumulative cultural evolution has occurred in the learned songs of Savannah sparrows. In a first step, "click trains" replaced "high note clusters" over a period of three decades. We use mathematical modelling to show that this replacement is consistent with the action of selection, rather than drift or frequency-dependent bias. Generations later, young birds elaborated the "click train" song form by adding more clicks. We show that the new songs with more clicks elicit stronger behavioural responses from both males and females. Therefore, we suggest that a combination of social learning, innovation, and sexual selection favoring a specific discrete trait was followed by directional sexual selection that resulted in naturally occurring cumulative cultural evolution in the songs of this wild animal population.

Natal experience and pre-breeding environmental conditions affect lay date plasticity in Savannah Sparrows.

Phenotypic plasticity allows organisms to adjust the timing of life-history events in response to environmental and demographic conditions. Shifts by individuals in the timing of breeding with respect to variation in age and temperature are well documented in nature, and these changes are known to scale to affect population dynamics. However, relatively little is known about how organisms alter phenology in response to other demographic and environmental factors. We investigated how pre-breeding temperature, breeding population density, age, and rainfall in the first month of life influenced the timing and plasticity of lay date in a population of Savannah Sparrows (Passerculus sandwichensis) monitored over 33 yr (1987-2019). Females that experienced warmer pre-breeding temperatures tended to lay eggs earlier, as did older females, but breeding population density had no effect on lay date. Natal precipitation interacted with age to influence lay date plasticity, with females that experienced high precipitation levels as nestlings advancing lay dates more strongly over the course of their lives. We also found evidence for varied pace of life; females that experienced high natal precipitation had shorter lifespans and reduced fecundity, but more nesting attempts over their lifetimes. Rainfall during the nestling period increased through time, while population density and fecundity declined, suggesting that increased precipitation on the breeding grounds may be detrimental to breeding females and ultimately the viability of the population as a whole. Our results suggest that females adjust their laying date in response to pre-breeding temperature, and as they age, while presenting new evidence that environmental conditions during the natal period can affect phenological plasticity and generate downstream, population-level effects.

Sympatry drives colour and song evolution in wood-warblers (Parulidae).

Closely related species often exhibit similarities in appearance and behaviour, yet when related species exist in sympatry, signals may diverge to enhance species recognition. Prior comparative studies provided mixed support for this hypothesis, but the relationship between sympatry and signal divergence is likely nonlinear. Constraints on signal diversity may limit signal divergence, especially when large numbers of species are sympatric. We tested the effect of sympatric overlap on plumage colour and song divergence in wood-warblers (Parulidae), a speciose group with diverse visual and vocal signals. We also tested how number of sympatric species influences signal divergence. Allopatric species pairs had overall greater plumage and song divergence compared to sympatric species pairs. However, among sympatric species pairs, plumage divergence positively related to the degree of sympatric overlap in males and females, while male song bandwidth and syllable rate divergence negatively related to sympatric overlap. In addition, as the number of species in sympatry increased, average signal divergence among sympatric species decreased, which is likely due to constraints on warbler perceptual space and signal diversity. Our findings reveal that sympatry influences signal evolution in warblers, though not always as predicted, and that number of sympatric species can limit sympatry's influence on signal evolution.

Social and physiological drivers of rapid colour change in a tropical toad.

Dynamic sexual dichromatism occurs when males and females differ in colouration for a limited time. Although this trait has been primarily studied in cephalopods, chameleons, and fishes, recent analyses suggest that dynamic dichromatism is prevalent among anurans and may be mediated through sexual selection and sex recognition. Yellow toads, Incilius luetkenii, exhibit dynamic dichromatism during explosive breeding events at the onset of the rainy season: males change from a cryptic brown to a bright yellow and back again during the brief mating event. We tested the hypothesis that dynamic dichromatism in yellow toads is influenced by conspecific interactions and mediated through sex hormones and stress hormones. We placed male toads into one of four social treatments (with three other males, one male, one female, or no other toads). Immediately before and after each one-hour treatment, we quantified male colour with a reflectance spectrometer and we collected a blood sample to assess plasma concentrations of both testosterone and corticosterone. We found that males held with conspecific animals showed the brightest yellow colour and showed little or no change in their corticosterone levels. Across treatments, toads with duller yellow colour had higher levels of corticosterone. Male colour showed no association with testosterone. Interestingly, males showed substantial temporal variation in colour and corticosterone: toads were duller yellow and exhibited greater levels of corticosterone post-treatment across subsequent days at the onset of the rainy season. Our findings reveal that both conspecific interactions and corticosterone are involved in the dynamic colour change of yellow toads.

Baseline corticosterone does not reflect iridescent plumage traits in female tree swallows.

The production of high quality secondary sexual traits can be constrained by trade-offs in the allocation of energy and nutrients with other metabolic activities, and is mediated by physiological processes. In birds, the factors influencing male plumage quality have been well studied; however, factors affecting female plumage quality are poorly understood. Furthermore, it remains uncertain which physiological traits mediate the relationship between body condition and ornaments. In this three-year study of after-second-year female tree swallows (Tachycineta bicolor), we investigated (1) the relationship between baseline corticosterone near the end of the brood-rearing period (CORTBR) and feather colour characteristics (hue, saturation, brightness) the following year, and (2) the relationship between baseline corticosterone measured during incubation (CORTI) and brood rearing (CORTBR), and feather colour in the same year. To control for reproductive effort, we included reproductive parameters as covariates in all analyses. In this first study between CORT and the plumage colour characteristics of a species bearing iridescent feathers, we did not find any relationship between CORTBR and the colour of subsequently-produced feathers, nor did we find any relationship between CORT and the colour of feathers displayed during that breeding season. If CORT levels at the end of breeding carry over to influence the immediately subsequent moult period as we expect, our results generally indicate that structural plumage quality may not be as sensitive to circulating CORT levels compared to carotenoid-based colouration. Future studies, particularly those employing experimental manipulations of CORT during moult in species with iridescent traits, are necessary to fully determine the role glucocorticoids play in mediating the quality of secondary sexual characteristics.

Wild Birds Learn Songs from Experimental Vocal Tutors.

In eight groups of animals, including humans and songbirds, juveniles are understood to learn vocalizations by listening to adults [1-4]. Experimental studies of laboratory-reared animals support this hypothesis for vocal learning [5-7], yet we lack experimental evidence of vocal learning in wild animals. We developed an innovative playback technology involving automated loudspeakers that broadcast songs with distinctive acoustic signatures. We used this technology to simulate vocal tutors in the wild and conducted year-long tutoring sessions to five cohorts of free-living migratory Savannah Sparrows in eastern Canada. We confirm that wild birds learn songs by listening to adult conspecific animals, and we show that they pass these songs on to subsequent generations. Further, we provide the first experimental evidence in the wild that the timing of exposure to tutor song influences vocal learning: wild Savannah Sparrows preferentially learn songs heard during both their natal summer and at the outset of their first breeding season. This research provides direct experimental evidence of song learning by wild animals and shows that wild birds learn songs during two critical stages of development early in life. VIDEO ABSTRACT.

Assessing Sexual Dicromatism: The Importance of Proper Parameterization in Tetrachromatic Visual Models.

Perceptual models of animal vision have greatly contributed to our understanding of animal-animal and plant-animal communication. The receptor-noise model of color contrasts has been central to this research as it quantifies the difference between two colors for any visual system of interest. However, if the properties of the visual system are unknown, assumptions regarding parameter values must be made, generally with unknown consequences. In this study, we conduct a sensitivity analysis of the receptor-noise model using avian visual system parameters to systematically investigate the influence of variation in light environment, photoreceptor sensitivities, photoreceptor densities, and light transmission properties of the ocular media and the oil droplets. We calculated the chromatic contrast of 15 plumage patches to quantify a dichromatism score for 70 species of Galliformes, a group of birds that display a wide range of sexual dimorphism. We found that the photoreceptor densities and the wavelength of maximum sensitivity of the short-wavelength-sensitive photoreceptor 1 (SWS1) can change dichromatism scores by 50% to 100%. In contrast, the light environment, transmission properties of the oil droplets, transmission properties of the ocular media, and the peak sensitivities of the cone photoreceptors had a smaller impact on the scores. By investigating the effect of varying two or more parameters simultaneously, we further demonstrate that improper parameterization could lead to differences between calculated and actual contrasts of more than 650%. Our findings demonstrate that improper parameterization of tetrachromatic visual models can have very large effects on measures of dichromatism scores, potentially leading to erroneous inferences. We urge more complete characterization of avian retinal properties and recommend that researchers either determine whether their species of interest possess an ultraviolet or near-ultraviolet sensitive SWS1 photoreceptor, or present models for both.

Mimics here and there, but not everywhere: Müllerian mimicry in Ceroglossus ground beetles?

The ground beetle genus Ceroglossus contains co-distributed species that show pronounced intraspecific diversity in the form of geographical colour morphs. While colour morphs among different species appear to match in some geographical regions, in others, there is little apparent colour matching. Mimicry is a potential explanation for covariation in colour patterns, but it is not clear whether the degree of sympatric colour matching is higher than expected by chance given the obvious mismatches among morphs in some regions. Here, we used reflectance spectrometry to quantify elytral coloration from the perspective of an avian predator to test whether colour similarity between species is, indeed, higher in sympatry. After finding no significant phylogenetic signal in the colour data, analyses showed strong statistical support for sympatric colour similarity between species despite the apparent lack of colour matching in some areas. We hypothesize Müllerian mimicry as the responsible mechanism for sympatric colour similarity in Ceroglossus and discuss potential explanations and future directions to elucidate why mimicry has not developed similar levels of interspecific colour resemblance across space.

Haematocrit, eggshell colouration and sexual signaling in the European starling (Sturnus vulgaris).

BACKGROUND: One hypothesis to explain the blue-green colour of the eggs of many bird species is that it is a sexually-selected signal of the laying female's quality, which males use to determine their investment. This hypothesis requires that eggshell pigmentation carries a cost or is otherwise linked to female quality. One potential cost is that biliverdin, a haem derivative and the pigment responsible for eggshell colouration, is limiting. To assess this potential cost, we attempted to manipulate haematocrit and haemoglobin in free-living European starlings (Sturnus vulgaris Linnaeus). Upon collecting unmanipulated first clutches, we treated females with phenylhydrazine (PHZ), a haemolytic agent, and measured the blue-green chroma and reproductive performance of replacement clutches. We also investigated whether eggshell colour was associated with haematocrit or haemoglobin levels in unmanipulated first clutches. To test whether eggshell colour might act as a sexual signal, we examined associations between eggshell colour and reproductive performance, as well as the provisioning rate of the male. RESULTS: PHZ-treatment did not affect eggshell colour in replacement clutches. In unmanipulated first clutches, eggshell colour was not correlated with haematocrit or haemoglobin levels. Eggshell colour was correlated with female mass in unmanipulated first clutches but not replacement clutches. Chicks from eggs with higher eggshell colour had higher haemoglobin levels and longer tarsi just prior to fledging, suggesting that eggshell colour could reflect brood quality. However, eggshell colour was not correlated with the provisioning rate of the male or any other measure of reproductive performance. CONCLUSIONS: We found no evidence to support the hypothesis that the availability of resources required for the synthesis of pigment limits eggshell colour in European starlings, or that eggshell colour is used by males to determine their level of reproductive investment. We found little evidence that eggshell colour is correlated with female or offspring quality in this species.

Dynamic sexual dichromatism produces a sex signal in an explosively breeding Neotropical toad: A model presentation experiment.

Many animals breed in large mating aggregations, where males must rapidly discriminate between prospective mates and rivals. Selection may favour features that facilitate rapid discrimination in these aggregations. The explosively breeding Neotropical Yellow Toad, Incilius luetkenii, exhibits a rapid and dramatic colour change; males change from a cryptic brown to a conspicuous lemon yellow for their brief breeding period. Females, in contrast, remain cryptic brown throughout the year. The function of this temporary, sex-specific colour change is unknown. We tested the hypothesis that yellow colouration displayed by male I. luetkenii facilitates sex recognition during both daytime and nighttime mating aggregations. We created yellow and brown model toads and presented them to males during a breeding event. Male I. luetkenii responded significantly more intensely to brown models compared to yellow models, approaching them and making more amplexus attempts on the brown versus yellow models. This strong pattern held true regardless of ambient light intensity, making this the first study to expose a dynamic colour signal that operates during both day and night. Our results indicate that male I. luetkenii use colouration to quickly discriminate between males and females during their brief, explosive mating aggregations. Our findings suggest that the rapid, dramatic colour change of male I. luetkenii facilitates sex recognition, which could provide a significant fitness advantage to males in the form of reduced energy expenditure and reduced risk of injury by other males. Dynamic dichromatism may provide similar fitness benefits in any organisms that mate in large, competitive aggregations.

Analysis of plumage, morphology, and voice reveals species-level differences between two subspecies of Prevost's Ground-sparrow Melozone biarcuata (Prévost and Des Murs) (Aves: Emberizidae).

Melozone biarcuata (Prevost's Ground-sparrow) has traditionally been divided into two allopatric groups based on differences in vocalizations and plumage characteristics: M. b. cabanisi in Costa Rica and M. b. biarcuata/M. b. hartwegi in northern Central America. However, the relationship between these subspecies has not been studied using a modern taxonomic approach. In this study, our objective was to provide the first detailed taxonomic comparison between these three subspecies using an integrative multi-trait analysis. We analyzed morphometric features, qualitative plumage patterns, and quantitative plumage measurements using spectral reflectance from all three subspecies, and we analyzed vocalizations for subspecies M. b. biarcuata and M. b. cabanisi. Our results show that M. b. cabanisi can be readily distinguished from the two other subspecies on the basis of morphometrics (M. b. cabanisi are smaller), plumage patterns (M. b. cabanisi have different facial markings and plumage patches), color differences (M. b. cabanisi have plumage patches that differ in color and brightness), and vocalizations (M. b. cabanisi have songs and calls that are acoustically distinct from those of M. b. biarcuata). By contrast, the two northern subspecies M. b. biarcuata and M. b. hartwegi were very similar for most traits, supporting previous suggestions that the two northern subspecies should be considered a single subspecies. Our data reveal that the differentiation in phenotypic characteristics between M. b. cabanisi versus M. b. biarcuata and M. b. hartwegi is similar to that reported for other complexes of subspecies where species status has been recognized. We argue that M. b. cabanisi should be treated as a species separate from M. biarcuata and propose that it be called Melozone cabanisi, White-faced Ground-sparrow. Our findings will contribute to the conservation efforts of the White-faced Ground-sparrow, which is endemic to Costa Rica's Central Valley and Turrialba Valley, by bringing focus to conservation policies that preserve ground-sparrow habitat (thickets, shade coffee plantations, and young secondary forest).

A molecular phylogenetic hypothesis for the manakins (Aves: Pipridae).

Phylogenetic relationships among the 14 manakin genera were inferred from DNA sequence data obtained from both mitochondrial and nuclear DNA loci. Phylogenetic analysis resulted in a well-supported hypothesis that corroborates a sister relationship between tyrant-manakins and the "core" manakins (Antilophia, Chiroxiphia, Corapipo, Dixiphia, Heterocercus, Ilicura, Lepidothrix, Manacus, Masius, Machaeropterus, Pipra, and Xenopipo). Our data strongly support these core manakin genera as a monophyletic group. Consistent with previous work, we find two major clades within the core manakins, although the placement of the genus Xenopipo with regards to these two clades is ambiguous. Generic relationships within these clades are generally well resolved. Although we find some concordance between our study and a previous manakin phylogeny based on syringeal characters, we note several fundamental differences between the phylogenies. Thus, we offer a new phylogenetic hypothesis for Pipridae.

Dynamic sexual dichromatism in an explosively breeding Neotropical toad.

Sexual selection often promotes the evolution of elaborate colour signals in males, but the importance of sexually selected colour signals remains poorly studied in amphibians. We used reflectance spectrometry to document pronounced sexual dichromatism and dramatic colour change in Bufo luetkenii, a toad that breeds in large aggregations at the onset of the rainy season in Costa Rica. Our observations suggest that males fade rapidly from a vibrant lemon yellow to a dull brown once they have paired with a female. We demonstrate this by showing that males are much brighter than females and that unpaired males are more colourful than males in amplexus. We also show that coloration fades rapidly when males are briefly held captive. This is, to our knowledge, the first study to document such dynamic change in male coloration and sexual dichromatism in anurans.

Iridescence: a functional perspective.

In animals, iridescence is generated by the interaction of light with biological tissues that are nanostructured to produce thin films or diffraction gratings. Uniquely among animal visual signals, the study of iridescent coloration contributes to biological and physical sciences by enhancing our understanding of the evolution of communication strategies, and by providing insights into physical optics and inspiring biomimetic technologies useful to humans. Iridescent colours are found in a broad diversity of animal taxa ranging from diminutive marine copepods to terrestrial insects and birds. Iridescent coloration has received a surge of research interest of late, and studies have focused on both characterizing the nanostructures responsible for producing iridescence and identifying the behavioural functions of iridescent colours. In this paper, we begin with a brief description of colour production mechanisms in animals and provide a general overview of the taxonomic distribution of iridescent colours. We then highlight unique properties of iridescent signals and review the proposed functions of iridescent coloration, focusing, in particular, on the ways in which iridescent colours allow animals to communicate with conspecifics and avoid predators. We conclude with a brief overview of non-communicative functions of iridescence in animals. Despite the vast amount of recent work on animal iridescence, our review reveals that many proposed functions of iridescent coloration remain virtually unexplored, and this area is clearly ripe for future research.

The Evolution of Signal Design in Manakin Plumage Ornaments.

Animal signals are characterized by two design components: efficacy (detectability) and content (message being conveyed). Selection for efficient signal perception should favor the evolution of traits that exhibit an optimal balance between these two design components. We examined the evolution of signal design in the colorful plumage ornaments of manakins (Aves: Pipridae). We used a model of avian color space to quantify how differences in plumage coloration would be perceived by a typical passerine bird and examined patterns of coloration across 50 species of manakin. Using phylogenetically independent contrasts, we show that plumage contrast against the background increases with sexual dichromatism in males but not females, suggesting that sexual selection has favored the evolution of male plumage ornaments that enhance signal efficacy. Plumage contrast within individuals also increased with dichromatism in males but not females. Finally, plumage colors produced by different mechanisms, which may reveal different aspects of quality, resulted in different degrees of contrast against the background. Our findings suggest that selection for signal efficacy and content may sometimes be opposing, creating a trade-off between these two components of signal design. Manakins may mediate this trade-off by combining multiple plumage ornaments that differ in efficacy and content.

Iridescent plumage in satin bowerbirds: structure, mechanisms and nanostructural predictors of individual variation in colour.

Iridescence is produced by coherent scattering of light waves from alternating layers of materials of different refractive indices. In birds, iridescent colours are produced by feather barbules when light is scattered from alternating layers of keratin, melanin and air. The structure and organization of these layers, and hence the appearance of bird species with different types of plumage iridescence, varies extensively. One principal distinction between different types of iridescent colours is whether they are produced by a single pair of layers or by multiple pairs of layers. Multi-layer iridescence, such as that displayed by hummingbirds, has been relatively well characterized, but single-layer iridescence has only recently been modeled successfully. Here we use electron microscopy, spectrometry and thin-film optical modeling to investigate the glossy, ultraviolet-blue iridescent plumage colouration of adult male satin bowerbirds Ptilonorhynchus violaceus minor. The flattened barbules of adult males are composed of a superficial keratin layer overlying a melanin layer that is several granules thick. A thin-film model based on the thickness of the keratin layer and its two associated interfaces (air/keratin and keratin/melanin) generates predicted reflectance spectra that closely match measured spectra. In addition, hues predicted from this model are positively correlated with measured hues. As predicted from our thin-film model, measured hues shifted to shorter wavelengths at increasing angles of incidence and reflectance. Moreover, we found that individual variation in barbule nanostructure can predict measured variation in both hue and UV-chroma. Thus, we have characterized the microstructure of satin bowerbird barbules, uncovered the mechanisms responsible for producing ultraviolet iridescence in these barbules, and provided the first evidence of a nanostructural basis for individual variation in iridescent plumage colour.