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Artificial white crest worn by male long-tailed finch ( left ) and male zebra finch ( right ) during mate choice trials. Photo credit: Kerry Clayman.
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Darwin first hypothesized that bright colors and elaborate ornamentation of male animals evolved in response to the "aesthetic" mate preferences of females. By this reasoning, potentially costly male secondary sexual traits may evolve not in response to selection for demonstration of vigor but, rather, in response to latent, nonfunctional preferenc...
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... occur in extant grassfinches, they did not coevolve with crests; rather, the preferences are either ‘‘preex- isting’’ or, if they evolved in some remote, crested ancestor, they have somehow survived vast spans of evolutionary time without expression. We tested the preferences for crested, opposite-sex conspecifics of two grassfinch species: zebra finches ( Taeniopygia guttata castanotis ) and long-tailed finches ( Poephila acuticauda ). These species have typically been considered congeners or members of sister genera (Goodwin 1982), but more recent analysis (Christitis 1987) suggests they may be somewhat less closely related. Zebra finches range widely over the continent of Australia ( fig. 1), but no regional variation in plumage patterns or soft-part coloration has been found (Keast 1958; N. T. Burley, unpublished data). Long-tailed finches live in a longitudinal belt across the Northern Territory and Western Australia. The zebra finch occurs, albeit uncommonly, through- out much of the breeding range of the long-tailed finch (fig. 1). Long-tailed finches are often characterized as having two distinct subspecies, hecki and acuticauda. Birds of the acuticauda type have yellow-orange beak, whereas those of the hecki type have bright red beaks. In actuality, beak color shows continuous variation in the Northern Territory. Moreover, populations trapped at intervals 100 km apart show other distinctive characteristics (N. T. Burley and R. Symanski, unpublished data). In 1992, we captured birds at two locations in the Northern Territory (fig. 1) and exported them under permit to the United States. Birds from Larrimah have bright red beaks, small bibs and are sexually indistinguishable (Burley 1981 a, 1986 a ). Birds from Newry have yellow-orange beaks, larger bibs, and are mildly sexually dimorphic in plumage traits. These differences persist among first and second laboratory-hatched generations; thus, major population differences are not the result of environmental variables such as diet. In captivity, birds will not readily form pair-bonds with individuals from the opposite population (N. T. Burley, unpublished data). Three experiments measured heterosexual social preferences using a design previously established to measure mate choice (Burley 1986 a; Burley et al. 1994, 1996). Birds were given choices of four opposite-sex social part- ners having randomly assigned experimental phenotypes (e.g., crests of various colors). The major goals of the experiments were to determine whether members of an uncrested lineage have preferences for or aversions to crests, and whether there are species and/or population differences in preference. An additional goal of the third experiment was to assess individual variation in preference for crests. Domesticated, wild-type zebra finches maintained in N. T. Burley’s laboratory (effective population size greater than 100 individuals) were presented with opposite- sex stimulus sets composed of four individuals. Stimulus sets were matched for natural phenotypic variation (beak color, weight, and activity level). Three birds within a set were assigned crests using a stratified random design; the fourth bird was not crested. Crest colors were selected on the basis of color-band preferences previously measured (Burley 1985) and reflect the range of responses to color bands shown by zebra finches. Each male stimulus set contained a red- crested individual (red leg bands are attractive to females), a white-crested one (white leg bands are neutral), and a green-crested bird (green is unattractive). The crest colors used for female zebra finch stimulus sets were sim- ilarly selected: black is a leg band color preferred by males, white is neutral, and light blue is unattractive. The general methodology for measuring preferences has been previously detailed (Burley 1986 a and references therein). Crests were made by weaving together tiny (‘‘seed’’) beads into a platform in which a feather, either a rectrix (from an estrildine or small psittacine) or contour feather (from a psittacine), was glued in an upright posi- tion. Platform color was closely matched to that of the feather, except for ‘‘black’’ crests, in which the bead platform was black, but the feather was dark gray. (Black feathers were not available.) Within stimulus sets, crests were closely matched for feather size and shape; trim- ming of feathers was sometimes employed to achieve uniformity. Feathers with uneven coloration were ‘‘tou- ched up’’ with artist-quality water-based markers. When this was done, marker was lightly and uniformly applied to the entire feather. The procedure was employed for all of the red feathers used, and about half of the gray feathers, but not the blue or green ones. Crests weighed about 0.3 g, or approximately 2.4% of bird weight. Crests were affixed with water-based glue to the crown feathers of stimulus birds (fig. 2). Most stimulus birds ‘‘accepted’’ (stopped trying to dislodge) their crest within 30 min of application; those that persisted in attempting to remove the crest were removed from the experiment. We repaired crests when feathers became bent, broken, or frayed. When a crest was damaged beyond repair or if a stimulus bird lost its crown feathers when its crest fell off, we discontinued use of the stimulus set. Never-mated adults in excellent phenotypic condition were used as test birds. After test birds were acclimated to the apparatus (Burley 1986 b ), test birds received 48 h of exposure to the test phenotypes (in the experimental apparatus) before testing. Then they were tested in 2-h trials. Trials were considered successful when test ...
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Darwin first hypothesized that bright colors and elaborate ornamentation of male animals evolved in response to the “aesthetic” mate preferences of females. By this reasoning, potentially costly male secondary sexual traits may evolve not in response to selection for demonstration of vigor but, rather, in response to latent, nonfunctional preferenc...
Male and female parents often provide different type and amount of care to their offspring. Three major drivers have been proposed to explain parental sex roles: (i) differential gametic investment by males and females that precipitates into sex difference in care, (ii) different intensity of sexual selection acting on males and females, and (iii)...
Parental care in birds consists of elaborate forms across stages, including nest building, incubation, and offspring provision. Despite their evolutionary importance, knowledge gaps exist in the extent to which parents contribute disproportionately to these forms and factors that are associated with variations in care patterns between sexes. Here,...
Citations
... One caveat of our system is the effect of markers. It have been reported that zebra finches have color preferences for artificially attached leg band or feather crest on their head 29,30 . To minimize this effect, our analyses were conducted after sufficient acclimation of the markers on their head, with consistent usage of maker colors. ...
Understanding animal behavior is crucial in behavioral neuroscience, which aims to unravel the mechanism driving these behaviors. A milestone in this field is the analysis of behavioral reactions among animals engaging in social interactions. Although many studies have revealed the fundamental roles of social interaction in social learning, the behavioral aspects of these interactions remain poorly understood, largely due to the lack of tools for analyzing complex behaviors and the attention of subjects in naturalistic, free-moving conditions. Here, we introduce a high-precision system for behavior analysis in songbirds using a marker-based motion capture technique. This system accurately tracks the body location and head direction of freely moving finches and is applicable to multiple subjects during social interaction. With this system, we have quantitatively analyzed behaviors of zebra finches ( Taeniopygia guttata ) related to visual attention. Our analysis revealed variations in the use of right and left eyes, as well as the duration of sight, among the individuals presented. Further analysis and comparison of their behaviors during both virtual and live presentation identified the similarities and differences in their behavioral reactions. Additionally, we observed changes in their behavioral reactions during a conditioned learning paradigm. This system provides an efficient and easy-to-use tool for advanced behavioral analysis in songbirds, providing an objective method to infer their focus of attention
... This latter result may highlight the origin of latent aesthetic preferences, which are preferences for yet-to-exist traits. Latent aesthetic preferences for complex stimuli, such as the preference for artificial crests in Australian finches (Burley & Symanski (1998), are often assumed to emerge incidentally. Our males' preferences suggest that such latent preferences might instead be determined by their visual environment and reflect a sensory bias, thus supporting a sensory drive origin of latent preferences (Endler, 1992;Endler & Basolo, 1998;Seehausen et al., 2008). ...
The sensory drive hypothesis of animal signal evolution suggests that animal communication signals evolve in response to environmental pressures. While classical approaches to testing this hypothesis focus on one aspect of the signal, deep learning techniques like generative models can create and manipulate stimuli without targeting a specific feature. Here, we used a technique called style transfer to experimentally test preferences for colour patterns in a fish. We manipulated how similar or dissimilar male body patterns were to their habitats using the Neural Style Transfer (NST) algorithm. We predicted that males whose body patterns are similar to their habitats are easier to process and thus preferred by conspecifics. Our findings suggest that both males and females tend to be sensitive to habitat congruence in their preferences, but to different extents, requiring additional investigation. Nonetheless, this study demonstrates the potential of deep learning techniques in testing hypotheses about animal communication signals.
... Whereas we know that colorful lures attract prey, it remains unclear how attraction scales with variation away from the characteristics of extant stimuli. This encompasses uncharted possibilities such as whether novel attractant stimuli may occur along the color spectrum (yet remain possibly "out of reach" of spiders; sensu Burley and Symanski 1998) and whether supernormal stimulus variation (Gwynne and Rentz 1983) could actually elevate catch rates. More generally, the field lacks a quantitative statement relating spectral characteristics to prey attractiveness for any colorbased lure system. ...
Many species – humans included – employ color as an instrument of deception. One intriguing example of this resides in the conspicuous abstract color patterns displayed on the bodies of female orb weaving spiders. These displays increase prey interception rates and thereby function at least as visual lures. Their chromatic properties however vary extensively, both across and within species, with discrete forms often co-existing in the manner of a stable polymorphism. Variation is principally expressed in terms of signal hue (color per se), but it is unclear how attractiveness scales with this property and if extant morphs are maximally attractive relative to a graded range of potential alternatives. We examined these questions by assessing catch rates among color-manipulated females of the dimorphic jeweled spider Gasteracantha fornicata in their natural webs. The manipulation altered dorsal appearance in a manner akin to adding six new variants of their existing white/yellow phenotypes. This magnified the natural variation in stimulus hue independently of chroma (saturation) across a range spanning most of the color spectrum. Catch rate varied across treatments in simple accordance with how greatly stimulus hue deviated from either of the two extant spider phenotypes. Predictions based on fly-perceived chromatic and achromatic background contrast were clearly unsupported despite dipterans constituting ~60 % of identifiable prey. This study supports the importance of signal coloration per se in G. fornicata and suggests that extant lure phenotypes reside in a broadly optimal spectral range for stimulating their aggregate prey community.
... refs. [19][20][21][22][23][24]. Such hidden preferences originate from preexisting biases unrelated to the current distribution of courter traits (e.g. ...
Inadvertent cues can be refined into signals through coevolution between signalers and receivers, yet the earliest steps in this process remain elusive. In Hawaiian populations of the Pacific field cricket, a new morph producing a novel and incredibly variable song (purring) has spread across islands. Here we characterize the current sexual and natural selection landscape acting on the novel signal by (1) determining fitness advantages of purring through attraction to mates and protection from a prominent deadly natural enemy, and (2) testing alternative hypotheses about the strength and form of selection acting on the novel signal. In field studies, female crickets respond positively to purrs, but eavesdropping parasitoid flies do not, suggesting purring may allow private communication among crickets. Contrary to the sensory bias and preference for novelty hypotheses, preference functions (selective pressure) are nearly flat, driven by extreme inter-individual variation in function shape. Our study offers a rare empirical test of the roles of natural and sexual selection in the earliest stages of signal evolution.
... Multiple studies have examined the role of plumage traits in contexts of social dominance and mate choice within populations of birds (Senar 1999;Griffith et al. 2006;Uy et al. 2018). However, little attention has been devoted to testing whether newly evolved traits are recognized (hence potentially favored or selected against) or not by conspecifics (Burley et al. 1982;Burley and Symanski 1998;Witte et al. 2000), with studies showing mixed results. For example, in two pairs of allopatric Monarcha flycatchers from the Solomon Islands, males were more aggressive to local than to novel plumage patterns found in other populations (Uy et al. 2009). ...
... Experimental studies often indicate that females prefer traits from their own population over traits from other populations (Baker and Baker 1990; Patten et al. 2004), yet females of several species may prefer traits not naturally exhibited by local males including both artificial (i.e. novel) ornaments (Burley et al. 1982;Burley and Symanski 1998) as well as exaggerated traits (Andersson 1982;Burley and Coopersmith 1987;Baldassarre and Webster 2013). Therefore, compounded with the fact that different mutations influencing male plumage may stochastically appear in different populations (Chapman 1923), geographic variation in female preferences (e.g. ...
Whether novel traits involved in animal communication are favored or not by social selection depends on how receivers respond to them. If alternative traits arise at different locations or the same traits are perceived differently, then populations may diverge even when occupying similar environments. Aggressiveness towards bearers of novel versus familiar traits is informative about how male-male competition may drive phenotypic evolution, yet few studies have tested the function of signaling traits in social selection across populations. We assessed the role of a black pectoral band during territorial contests in two allopatric species of Neotropical passerine birds in the genus Arremon either having or lacking this plumage trait. Field experiments using taxidermic mounts and playback of conspecific songs revealed that males of both species were equally aggressive towards phenotypes bearing or lacking a pectoral band. Although evaluating physiological and social costs of bearing alternative traits and assessing female preferences is required to further examine the roles of social and sexual mechanisms in the evolution of plumage and geographic variation, our results indicate that social selection via male-male interactions is an unlikely driver of phenotypic divergence among populations of Arremon.
Significance
Social selection via intrasexual competition for resources may drive phenotypic divergence and population differentation in animals, but few studies have tested predictions of this hypothesis by examining how alternative traits varying geographically are perceived in contexts of male-male competition. We assessed the behavioral response of territorial males in two species of Neotropical songbirds to taxidermic mounts having or lacking a black pectoral band, a geographically variable plumage trait. Irrespective of their own phenotype, males of both species were similarly aggressive to potential intruders bearing or lacking the pectoral band. In contrast with work suggesting male-male interactions may mediate trait evolution, our results indicate that pectoral bands in this system are unlikely targets of social selection via contests in which males compete for territories, and call for studies assessing long-term costs of bearing alternative traits or female choice as selective forces driving phenotypic evolution.
... The vocal sac has also been shown to strongly modulate female preference for calls, depending on light conditions (Cronin et al., 2019) and the degree of temporal synchrony between the vocal sac movement and call (Taylor et al., 2011;Taylor and Ryan, 2013). Collectively, these data show that the vocal sac plays an important role in modulating female mating decisions (Reichert and Höbel, 2015), but it does not act as a simple ornament, in the classical sense of sexual selection (Burley and Symanski, 1998), by adding attractiveness to an otherwise unattractive call. ...
Noise is a common problem in animal communication. We know little, however, about how animals communicate in noise using multimodal signals. Multimodal signals are hypothesized to be favoured by evolution because they increase the efficacy of detection/discrimination in noisy environments. We tested the hypothesis that female túngara frogs’ responses to attractive male advertisement calls are improved in noise when a visual signal component is added to the available choices. We tested this at two levels of decision complexity (two and three choices). In a two-choice test, the presence of noise did not reduce female preferences for attractive calls. The visual component of a calling male, associated with an unattractive call, also did not reduce preference for attractive calls in the absence of noise. In the presence of noise, however, females were more likely to choose an unattractive call coupled with the visual component. In three-choice tests, the presence of noise alone reduced female responses to attractive calls and this was not strongly affected by the presence or absence of visual components. The responses in these experiments fail to support the multimodal signal efficacy hypothesis. Instead, the data suggest that audio-visual perception and cognitive processing, related to mate choice decisions, are dependent on the complexity of the sensory scene.
... Several other avian studies in line with the sensory exploitation hypothesis focused on the presence of sensory bias, but did not investigate whether males actually deceive females (e.g. Burley & Symanski 1998;Collins 1999;Jones & Hunter 1999). ...
Conspicuous colour patterns of animals, such as dots or stripes, can function as sexual and/or social signals. Their evolution is often explained by honest indicator mechanisms or the sensory exploitation hypothesis. In birds, however, the latter scenario has been scarcely tested. According to the sensory exploitation hypothesis, prey-like colour patterns can evolve when they contribute to attracting opposite-sex conspecifics by hitchhiking pre-existing sensory systems (sensory bias) that help foraging. Even without cheating scenarios, visual systems can serve as an underlying factor that facilitates the evolution of both foraging behaviours and colour patterns on the body. To test this idea, we examined the relationship between bird plumage patterns and diet using phylogenetic comparative approaches. Specifically, we focused on white polka-dot plumage patterns in estrildid finches and tested whether such patterns evolved for visual sensory systems that help foraging termites and other gregarious whitish small round prey items. Although we predicted that white polka-dots exist in termite-eater species, and that termite-eating evolved before the white polka-dot pattern, ancestral reconstruction did not reveal clear ancestral states for termite-eating. However, the phylogenetic regression model showed that species with conspicuous white polka-dots tended to be termite-eaters. We also found that estrildids with white polka-dots were likely to become termite-eaters, while those without white polka-dots were likely to become non-termite eaters, according to evolutionary transition analysis. These results are in contrast to the prediction of sensory exploitation hypothesis, wherein diet is believed to trigger the evolution of plumage patterns. However, the results presented here suggest that pre-existing sensory bias for white dots may have promoted the evolution of both termite-eating and white polka-dot plumage patterns in estrildids.
... Experimenters have demonstrated how such preferences can transfer from a non-sexual context to a sexual context by artificially adding hitherto unknown traits to males in lab settings. For instance, when male Zebra finches are adorned with black or pink leg bands they become increasingly attractive to females (Burley & Symanski, 1998), suggesting that the brain of the female Zebra finch is already equipped with a preference for pink and black. Similarly, Ryan and his colleagues played a wide assortment of sounds as part of the male túngara frog's courtship call and found that females were attracted to males associated with sounds not expressed by any living túngara frog (Ryan, Bernal & Rand, 2010). ...
... The presence of novel preferences for non-existent male traits has been observed in a range of species, including in birds for males with white crests [16], and in grasshoppers for particular complexities of courtship song [17]. A previously proposed mechanism whereby novel preference-trait combinations could arise is sensory bias. ...
Males in many species have elaborated sexual traits that females strongly prefer, and these traits often conspicuously differ among species. How novel preferences and traits originate, however, is a challenging evolutionary problem because the initial appearance of only the female preference or only the male trait should reduce the ability to find a suitable mate, which could reduce fitness for individuals possessing those novel alleles. Here, we present a hypothesis for how novel preferences, as well as the novel male traits that females prefer, can originate, be favoured and spread in polyandrous species. Novel preference mutations can arise as 'veiled preferences' that are not expressed when the corresponding male trait is not present in the population, allowing preferences to be hidden from selection, and thus persist. In those cases when a male trait is present, veiled preferences provide a selective advantage, and females disproportionately produce offspring from preferred males through either mate choice or cryptic female choice. This tips the fitness advantage for novel males, allowing both preference and trait to spread, and limiting selection against them in the absence of the corresponding trait or preference. © 2019 The Author(s) Published by the Royal Society. All rights reserved.
... Feather head crests have been found in fossils of some dinosaurs and early birds as well as a wide variety of living species of birds [9,10]. While feather crests have usually been studied for their roles as possible visual signals [11][12][13][14], recent behavioral studies of two auklet species have shown that their erect head crest feathers can play a mechanosensory role during tactile navigation similar to that of mammalian whiskers and arthropod antennae [14,15]. These findings suggest that feather crests in other birds also might play a previously unrecognized mechanosensory functional role. ...
Feathers act as vibrotactile sensors that can detect mechanical stimuli during avian flight and tactile navigation, suggesting that they may also detect stimuli during social displays. In this study, we present the first measurements of the biomechanical properties of the feather crests found on the heads of birds, with an emphasis on those from the Indian peafowl (Pavo cristatus). We show that in peafowl these crest feathers are coupled to filoplumes, small feathers known to function as mechanosensors. We also determined that airborne stimuli with the frequencies used during peafowl courtship and social displays couple efficiently via resonance to the vibrational response of their feather crests. Specifically, vibrational measurements showed that although different types of feathers have a wide range of fundamental resonant frequencies, peafowl crests are driven near-optimally by the shaking frequencies used by peacocks performing train-rattling displays. Peafowl crests were also driven to vibrate near resonance in a playback experiment that mimicked the effect of these mechanical sounds in the acoustic very near-field, reproducing the way peafowl displays are experienced at distances ≤ 1.5m in vivo. When peacock wing-shaking courtship behaviour was simulated in the laboratory, the resulting airflow excited measurable vibrations of crest feathers. These results demonstrate that peafowl crests have mechanical properties that allow them to respond to airborne stimuli at the frequencies typical of this species’ social displays. This suggests a new hypothesis that mechanosensory stimuli could complement acoustic and visual perception and/or proprioception of social displays in peafowl and other bird species. We suggest behavioral studies to explore these ideas and their functional implications.
