Nestling coloration is adjusted to parent visual performance in altricial birds irrespective of assumptions on vision system for Laniidae and owls,a reply to Renoult et al.

We have recently published support to the hypothesis that visual systems of parents could affect nestling detectability and, consequently, influences the evolution of nestling colour designs in altricial birds. We provided comparative evidence of an adjustment of nestling colour designs to the visual system of parents that we have found in a comparative study on 22 altricial bird species. In this issue, however, Renoult et al. ( J. Evol. Biol., 2009 ) question some of the assumptions and statistical approaches in our study. Their argumentation relied on two major points: (1) an incorrect assignment of vision system to four out of 22 sampled species in our study; and (2) the use of an incorrect approach for phylogenetic correction of the predicted associations. Here, we discuss in detail re‐assignation of vision systems in that study and propose alternative interpretation for current knowledge on spectrophotometric data of avian pigments. We reanalysed the data by using phylogenetic generalized least squares analyses that account for the alluded limitations of phylogenetically independent contrasts and, in accordance with the hypothesis, confirmed a significant influence of parental visual system on gape coloration. Our results proved to be robust to the assumptions on visual system evolution for Laniidae and nocturnal owls that Renoult et al. ( J. Evol. Biol., 2009 ) study suggested may have flawed our early findings. Thus, the hypothesis that selection has resulted in increased detectability of nestling by adjusting gape coloration to parental visual systems is currently supported by our comparative data.     

When assumptions on visual system evolution matter: nestling colouration and parental visual performance in birds

Comparative studies in visual ecology of birds often rely on several assumptions on the evolution of avian vision. In this study, we show that when these assumptions are not upheld, conclusions may be strongly affected. To illustrate this purpose, we reanalysed the data of Avilés & Soler (J. Evol. Biol. 22 : 376–386, 2009) who demonstrated that nestling gape colouration in altricial birds is associated with visual system. We show that a slight change in analysis methodology leads to opposite conclusions. Such conflicting result raises the problem of applying powerful methods developed for continuous variables to a small sample and a small number of independent events of qualitative visual system shift in comparative analyses. Further, we show that the current trend to assume strong phylogenetic inertia of avian visual systems is contradicted by data and that the sequencing of the SWS1 opsin gene should be considered as an alternative approach.     

Quantitative estimates of visual performance features in fossil birds

Eyeball structures such as the lens diameter (LD) and axial length are generally assumed to be highly correlated with optically meaningful parameters. However, these optical constraints on eyeball macroanatomy have never been tested explicitly. Tradeoffs between benefits of improved visual performance and cost of adaptation from an increase of tissue production predict that when eyeball size increases, optical parameters such as posterior nodal distance and maximum entrance pupil diameter should increase isometrically with eyeball axial length and LD, respectively. Here I show quantitatively that the interspecific allometry of the avian eye largely follows this predicted isometry. Additionally, I elaborate a method to estimate optically significant eyeball soft‐tissue dimensions from scleral ring and orbit morphology based on analyses of interspecific allometry in Aves. The stringent correlations between avian eyeball morphology and optical function render this system ideal for the analysis of form–function relationships and allow for an accurate estimate of optically significant eyeball soft‐tissue dimensions such as diameter, axial length, and LD in fossil species. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

Lizards speed up visual displays in noisy motion habitats

Extensive research over the last few decades has revealed that many acoustically communicating animals compensate for the masking effect of background noise by changing the structure of their signals. Familiar examples include birds using acoustic properties that enhance the transmission of vocalizations in noisy habitats. Here, we show that the effects of background noise on communication signals are not limited to the acoustic modality, and that visual noise from windblown vegetation has an equally important influence on the production of dynamic visual displays. We found that two species of Puerto Rican lizard, Anolis cristatellus and A. gundlachi, increase the speed of body movements used in territorial signalling to apparently improve communication in visually 'noisy' environments of rapidly moving vegetation. This is the first evidence that animals change how they produce dynamic visual signals when communicating in noisy motion habitats. Taken together with previous work on acoustic communication, our results show that animals with very different sensory ecologies can face similar environmental constraints and adopt remarkably similar strategies to overcome these constraints.     

Sex-specific visual performance: female lizards outperform males in motion detection

In animal communication, complex displays usually have multiple functions and, male and female receivers often differ in their utilization and response to different aspects of these displays. The perceptual variability hypothesis suggests that different aspects of complex signals differ in their ability to be detected and processed by different receivers. Here, we tested whether receiver male and female Sceloporus graciosus lizards differ in visual motion detection by measuring the latency to the visual grasp response to a motion stimulus. We demonstrate that in lizards that largely exhibit complex motions as courtship signals, female lizards are faster than males at visually detecting motion. These results highlight that differential signal utilization by the sexes may be driven by variability in the capacity to detect different display properties.     

Evolution and spectral tuning of visual pigments in birds and mammals

Variation in the types and spectral characteristics of visual pigments is a common mechanism for the adaptation of the vertebrate visual system to prevailing light conditions. The extent of this diversity in mammals and birds is discussed in detail in this review, alongside an in-depth consideration of the molecular changes involved. In mammals, a nocturnal stage in early evolution is thought to underlie the reduction in the number of classes of cone visual pigment genes from four to only two, with the secondary loss of one of these genes in many monochromatic nocturnal and marine species. The trichromacy seen in many primates arises from either a polymorphism or duplication of one of these genes. In contrast, birds have retained the four ancestral cone visual pigment genes, with a generally conserved expression in either single or double cone classes. The loss of sensitivity to ultraviolet (UV) irradiation is a feature of both mammalian and avian visual evolution, with UV sensitivity retained among mammals by only a subset of rodents and marsupials. Where it is found in birds, it is not ancestral but newly acquired.     

Nestling immune response to phytohaemagglutinin is not heritable in collared flycatchers

The response to intradermally injected phytohaemagglutinin (PHA-response) is a commonly used quantification of avian immunocompetence (the ability to resist pathogens). Parasite-mediated sexual selection requires heritable immunocompetence, but evidence for heritability of PHA-response in birds largely stems from full-sib comparisons. Using an animal model approach, we quantified the narrow-sense heritability of PHA-response in 1626 collared flycatcher (Ficedula albicollis) nestlings from 332 families, most of which were cross-fostered. Nestling PHA-response was not significantly heritable (h2=0.06+/-0.10), but was subject to non-heritable nest-of-origin effects (10% of variation). Our findings illustrate that full-sib comparisons of immunological measures may lead to an inflated estimate of heritability and also reveal a limited role of nestling PHA-response for sexual selection in this population.     

The evolution of pattern camouflage strategies in waterfowl and game birds

Visual patterns are common in animals. A broad survey of the literature has revealed that different patterns have distinct functions. Irregular patterns (e.g., stipples) typically function in static camouflage, whereas regular patterns (e.g., stripes) have a dual function in both motion camouflage and communication. Moreover, irregular and regular patterns located on different body regions (“bimodal” patterning) can provide an effective compromise between camouflage and communication and/or enhanced concealment via both static and motion camouflage. Here, we compared the frequency of these three pattern types and traced their evolutionary history using Bayesian comparative modeling in aquatic waterfowl (Anseriformes: 118 spp.), which typically escape predators by flight, and terrestrial game birds (Galliformes: 170 spp.), which mainly use a “sit and hide” strategy to avoid predation. Given these life histories, we predicted that selection would favor regular patterning in Anseriformes and irregular or bimodal patterning in Galliformes and that pattern function complexity should increase over the course of evolution. Regular patterns were predominant in Anseriformes whereas regular and bimodal patterns were most frequent in Galliformes, suggesting that patterns with multiple functions are broadly favored by selection over patterns with a single function in static camouflage. We found that the first patterns to evolve were either regular or bimodal in Anseriformes and either irregular or regular in Galliformes. In both orders, irregular patterns could evolve into regular patterns but not the reverse. Our hypothesis of increasing complexity in pattern camouflage function was supported in Galliformes but not in Anseriformes. These results reveal a trajectory of pattern evolution linked to increasing function complexity in Galliformes although not in Anseriformes, suggesting that both ecology and function complexity can have a profound influence on pattern evolution.     

Signal convergence in fruits: a result of selection by frugivores?

The Dispersal Syndrome hypothesis remains contentious, stating that apparently nonrandom associations of fruit characteristics result from selection by seed dispersers. We examine a key assumption under this hypothesis, i.e. that fruit traits can be used as reliable signals by frugivores. We first test this assumption by looking at whether fruit colour allows birds and primates to distinguish between fruits commonly dispersed by birds or primates. Second, we test whether the colours of fruits dispersed by primates are more contrasting to primates than the colours of bird‐dispersed fruits, expected if fruit colour is an adaptation to facilitate the detection by seed dispersers. Third, we test whether fruit colour has converged in unrelated plant species dispersed by similar frugivores. We use vision models based on peak sensitivities of birds’ and primates’ cone cells. We base our analyses on the visual systems of two types of birds (violet and ultraviolet based) and three types of primates (trichromatic primates from the Old and the New Worlds, and a dichromatic New World monkey). Using a Discriminant Function Analysis, we find that all frugivore groups can reliably discriminate between bird‐ and primate‐dispersed fruits. Fruit colour can be a reliable signal to different seed dispersers. However, the colours of primate‐dispersed fruits are less contrasting to primates than those of bird‐dispersed fruits. Fruit colour convergence in unrelated plants is independent of phylogeny and can be better explained by disperser type, which supports the hypothesis that frugivores are important in fruit evolution. We discuss adaptive and nonadaptive hypotheses that can potentially explain the pattern we found.     

Evolution and plasticity: Divergence of song discrimination is faster in birds with innate song than in song learners in Neotropical passerine birds

Plasticity is often thought to accelerate trait evolution and speciation. For example, plasticity in birdsong may partially explain why clades of song learners are more diverse than related clades with innate song. This “song learning” hypothesis predicts that (1) differences in song traits evolve faster in song learners, and (2) behavioral discrimination against allopatric song (a proxy for premating reproductive isolation) evolves faster in song learners. We tested these predictions by analyzing acoustic traits and conducting playback experiments in allopatric Central American sister pairs of song learning oscines (N = 42) and nonlearning suboscines (N = 27). We found that nonlearners evolved mean acoustic differences slightly faster than did leaners, and that the mean evolutionary rate of song discrimination was 4.3 times faster in nonlearners than in learners. These unexpected results may be a consequence of significantly greater variability in song traits in song learners (by 54–79%) that requires song‐learning oscines to evolve greater absolute differences in song before achieving the same level of behavioral song discrimination as nonlearning suboscines. This points to “a downside of learning” for the evolution of species discrimination, and represents an important example of plasticity reducing the rate of evolution and diversification by increasing variability.     

Using visual modelling to study the evolution of lizard coloration: sexual selection drives the evolution of sexual dichromatism in lacertids

Sexual selection has been invoked as a major force in the evolution of secondary sexual traits, including sexually dimorphic colourations. For example, previous studies have shown that display complexity and elaborate ornamentation in lizards are associated with variables that reflect the intensity of intrasexual selection. However, these studies have relied on techniques of colour analysis based on human – rather than lizard – visual perception. Here, we use reflectance spectrophotometry and visual modelling to quantify sexual dichromatism considering the overall colour patterns of lacertids, a lizard clade in which visual signalling has traditionally been underrated. These objective methods of colour analysis reveal a large, previously unreported, degree of sexual dichromatism in lacertids. Using a comparative phylogenetic approach, we further demonstrate that sexual dichromatism is positively associated with body size dimorphism (an index of intrasexual selection), suggesting that conspicuous coloration in male lacertids has evolved to improve opponent assessment under conditions of intense male–male competition. Our findings provide the first evidence for the covariation of sexual dichromatism and sexual size dimorphism in lacertids and suggest that the prevalent role of intrasexual selection in the evolution of ornamental coloration is not restricted to the iguanian lineage, but rather may be a general trend common to many diurnal lizards.     

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.     

Harmonic calls and indifferent females: no preference for human consonance in an anuran

The human music faculty might have evolved from rudimentary components that occur in non-human animals. The evolutionary history of these rudimentary perceptual features is not well understood and rarely extends beyond a consideration of vertebrates that possess a cochlea. One such antecedent is a preferential response to what humans perceive as consonant harmonic sounds, which are common in many animal vocal repertoires. We tested the phonotactic response of female túngara frogs (Physalaemus pustulosus) to variations in the frequency ratios of their harmonically structured mating call to determine whether frequency ratio influences attraction to acoustic stimuli in this vertebrate that lacks a cochlea. We found that the ratio of frequencies present in acoustic stimuli did not influence female response. Instead, the amount of inner ear stimulation predicted female preference behaviour. We conclude that the harmonic relationships that characterize the vocalizations of these frogs did not evolve in response to a preference for frequency intervals with low-integer ratios. Instead, the presence of harmonics in their mating call, and perhaps in the vocalizations of many other animals, is more likely due to the biomechanics of sound production rather than any preference for ‘more musical’ sounds.     

Aphids do not attend to leaf colour as visual signal, but to the handicap of reproductive investment

The evolution of visual warning signals is well known in animals but has received scant attention in plants. The coevolutionary hypothesis is the most influential hypothesis on warning signals in plants proposing that red and yellow leaf colours in autumn signal defensive strength to herbivores. So far, evidence in support of the hypothesis, which assumes a coevolutionary origin of autumnal leaf colours, is correlative and open to alternative explanations. We therefore tested the coevolutionary hypothesis experimentally by colouring the leaves either red or green of same-aged mountain ash (Sorbus aucuparia) individuals. We monitored the response of winged aphids to leaf colour using insect glue on branches with natural and artificial leaf colours in each individual. In contrast to the prediction of the coevolutionary hypothesis, aphid numbers did not differ between the individuals with artificial green or artificial red leaves. Likewise, at the within-plant level, aphids did not colonize branches with natural green leaves preferentially. However, we suggest that plants emitted warning signals because aphids colonized the hosts non-randomly. We found a strong positive correlation between aphid numbers and fruit production, suggesting an allocation trade-off between investment in plant defence and reproduction. Our study demonstrates that aphids use warning signals or cues in host selection, probably volatiles, but that they did not use leaf colour.     

Intentional communication: solving methodological issues to assigning first-order intentional signalling

Intentional signalling plays a fundamental role in human communication. Mapping the taxonomic distribution of comparable capacities may thus shed light on the selective pressures that enabled the evolution of human communication. Nonetheless, severe methodological issues undermine comparisons among studies, species and communicative modalities. Here, we discuss three main obstacles that hinder comparative research of ‘first-order’ intentional signalling (i.e. voluntary signalling in pursuit of a cognitively represented goal): (i) inconsistency in how behavioural hallmarks are defined and operationalised, (ii) testing of behavioural hallmarks without statistical comparison to control conditions, and (iii) bias against the publication of negative results. To address these obstacles, we present a four-step scheme with 20 statistical operational criteria to distinguish between non-intentional and first-order intentional signalling. Our unified scheme applies to visual and audible signals, thereby validating comparison across communicative modalities and species. This, in turn, promotes the generation and testing of hypotheses about the evolution of intentional communication.     

The subtlety of simple eyes: the tuning of visual fields to perceptual challenges in birds

Birds show interspecific variation both in the size of the fields of individual eyes and in the ways that these fields are brought together to produce the total visual field. Variation is found in the dimensions of all main parameters: binocular region, cyclopean field and blind areas. There is a phylogenetic signal with respect to maximum width of the binocular field in that passerine species have significantly broader field widths than non-passerines; broadest fields are found among crows (Corvidae). Among non-passerines, visual fields show considerable variation within families and even within some genera. It is argued that (i) the main drivers of differences in visual fields are associated with perceptual challenges that arise through different modes of foraging, and (ii) the primary function of binocularity in birds lies in the control of bill position rather than in the control of locomotion. The informational function of binocular vision does not lie in binocularity per se (two eyes receiving slightly different information simultaneously about the same objects from which higher-order depth information is extracted), but in the contralateral projection of the visual field of each eye. Contralateral projection ensures that each eye receives information from a symmetrically expanding optic flow-field from which direction of travel and time to contact targets can be extracted, particularly with respect to the control of bill position.