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.     

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.     

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.     

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.     

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.     

Sometimes slower is better: slow-exploring birds are more sensitive to changes in a vocal discrimination task

Animal personality, defined as consistent individual differences across context and time, has attracted much recent research interest in the study of animal behaviour. More recently, this field has begun to examine how such variation arose and is maintained within populations. The habitat-dependent selection hypothesis, which posits that animals with differing personality types may fare better (i.e. have a fitness advantage) in different habitats, suggests one possible mechanism. In the current experiment, we tested whether slow- and fast-exploring black-capped chickadees (Poecile atricapillus), determined by performance in a novel environment exploration task, perform differentially when the demands of an acoustic operant discrimination (cognitive) task were altered following successful task acquisition. We found that slow-exploring birds learn to reverse previously learned natural category rules more quickly than faster exploring conspecifics. In accordance with the habitat-dependent selection hypothesis, and previous work with great tits (Parus major), a close relative of the black-capped chickadee, our results suggest that fast-exploring birds may perform better in stable, predictable environments where forming a routine is advantageous, while slow-exploring birds are favoured in unstable, unpredictable environments, where task demands often change. Our results also support a hypothesis derived from previous work with great tits; slow-exploring birds may be generally more flexible (i.e. able to modify their behaviour in accordance with changes in environmental stimuli) in some learning tasks.     

Same-sex sexual behavior in birds: expression is related to social mating system and state of development at hatching

We report the findings of a phylogenetic comparative analysisexamining patterns and frequency of occurrence of same-sex courtshipand mounting behavior in birds. Our analysis has shown associationsbetween same-sex sexual behavior and both mating system anddegree of precociousness at hatching. The patterns of expressionand frequency of occurrence of same-sex sexual behavior differedmarkedly for males and females. Patterns of same-sex sexualexpression reflected the competitive sexes that actively solicitsexual interactions in heterosexual encounters. Male–male(MM) sexual behavior occurred across all mating systems, butMM mounting was significantly more prevalent in those specieswith facultative polygamy. The frequency of MM sexual behaviorincreased with degree of polygamy. Female–female (FF)sexual behavior (especially courtship) occurred most frequentlyin socially monogamous species and rarely occurred in speciesthat display obligate polygamy (predominantly polygynous species).Both expression and frequency of FF sexual behavior was stronglyrelated to the precocial state of development at hatching. FFsexual behavior is more likely to occur in species in whichmonogamy occurs together with the production of precocial offspring;that is, in monogamous species that are exceptions to the morecommon altricial mode of development. We suggest that requirementof biparental care in monogamous species may influence the greaterexpression of FF sexual behavior and longer term associations.Both spatial and behavioral dispersion of females and engagementin uniparental care may be important in explaining the lowerincidence of FF sexual behavior in polygynous species. Socialcontexts where males congregate at communal leks or displayareas may influence the greater expression and frequency ofMM sexual behavior in polygynous species.     

Colourful stripes send mixed messages to safe and risky partners in a diffuse cleaning mutualism

The steps by which neutral, random and/or negative biological interactions evolve into mutualistic ones remain poorly understood. Here, we study Elacatinus gobies and the ‘client’ fishes they clean. Colourful stripes are common to mutualist cleaners and noncleaning sister species. Blue stripes are unique to cleaners and are more conspicuous to predators than are basal yellow or green stripes. In turn, we focused on the role of colour as a potentially specialized signal. We show that cleaners may possess a chemical defence and demonstrate that stripes are sufficient to elicit client posing behaviour and to deter attack, corroborating the putative role of chemistry. Analysis of previously published records shows that yellow cleaners interact with predatory clients less often compared to green and blue cleaners. Our results highlight evolution from predator resistance to advertising with conspicuous signals. Similar trajectories, via recognizable signals to risky partners, may be common in other diffuse mutualisms.