Signal Traits Research Articles

Evolutionary loss of a signalling colour is linked to increased response to conspecific chemicals.

Behavioural responses to communicative signals combine input from multiple sensory modalities and signal compensation theory predicts that evolutionary shifts in one sensory modality could impact the response to signals in other sensory modalities. Here, we conducted two types of field experiments with 11 species spread across the lizard genus Sceloporus to test the hypothesis that the loss of visual signal elements affects behavioural responses to a chemical signal (conspecific scents) or to a predominantly visual signal (a conspecific lizard), both of which are used in intraspecific communication. We found that three species that have independently lost a visual signal trait, a colourful belly patch, responded to conspecific scents with increased chemosensory behaviour compared to a chemical control, while species with the belly patch did not. However, most species, with and without the belly patch, responded to live conspecifics with increased visual displays of similar magnitude. While aggressive responses to visual stimuli are taxonomically widespread in Sceloporus, our results suggest that increased chemosensory response behaviour is linked to colour patch loss. Thus, interactions across sensory modalities could constrain the evolution of complex signalling phenotypes, thereby influencing signal diversity.

Responses of butterflies to visual and olfactory signals of flowers of the bush lily Clivia miniata

Experimental studies of the use of visual and olfactory cues by flower-visiting animals can shed light on the evolution of floral signalling traits. We examined the functional significance of floral traits in Clivia miniata (Amaryllidaceae). This forest lily with large orange trumpet-shaped flowers is pollinated mainly by swallowtail butterflies and belongs to a lineage with ancestral bird pollination. We used C. miniata flowers varying in colour, orientation and scent, and arrays of artificial flowers varying in colour, pattern, orientation, size, shape, and scent to assess foraging preferences of the butterflies that pollinate C. miniata. Butterflies preferred orange over yellow colour morphs of C. miniata and preferred red and orange model flowers over yellow ones. Orange models with a central yellow target ‘nectar guide’ were favoured over plain orange models. Butterflies also favoured large over small model flowers and preferred to alight on upward-facing flowers. Addition of scent compounds emitted by C. miniata flowers increased butterfly visitation to model and natural flowers. These results identify the importance of particular combinations of visual and olfactory signals for attraction of swallowtail butterflies and shed light on the floral modifications associated with a shift from bird to butterfly pollination.

Evolutionary novelty in communication between the sexes.

The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.

Territorial males do not discriminate between local and novel plumage phenotypes in a tropical songbird species complex: implications for the role of social selection in trait evolution

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. 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.

Does the addition of a new signalling trait enhance receiver responses in diurnal geckos?

Animal signals in multiple modalities expands the opportunity for effective communication. Among diurnal geckos of the genus Cnemaspis, chemical signalling traits preceded the evolution of visual traits. Males of all species possess chemical secreting ventral glands, but only in some species, males also express yellow gular patches. This difference in the expression of unimodal or multimodal signalling traits between closely related species provided us with an opportunity to understand the use of multimodal signals for communication. We studied receiver responses in Cnemaspis indica, a sexually monochromatic species, and in C. littoralis, a species where males possess yellow gulars. We performed behavioural trials where individuals of each species were exposed to only chemical stimuli, only visual stimuli, or both chemical and visual stimuli simultaneously from male and female conspecifics. Our results show that only chemical stimuli were necessary and sufficient to elicit responses in males and females of C. indica as well as in females of C. littoralis. However, males of the dimorphic C. littoralis required the multimodal stimulus to elicit movement-based responses. Our results suggest that the evolution of colour traits in diurnal geckos is associated with a partial shift in some receiver responses toward multimodal communication, with no addition to the behavioural repertoire.

Asymmetric interspecific competition drives shifts in signalling traits in fan-throated lizards.

Interspecific competition can occur when species are unable to distinguish between conspecific and heterospecific mates or competitors when they occur in sympatry. Selection in response to interspecific competition can lead to shifts in signalling traits-a process called agonistic character displacement. In two fan-throated lizard species-Sitana laticeps and Sarada darwini-females are morphologically indistinguishable and male agonistic signalling behaviour is similar. Consequently, in areas where these species overlap, males engage in interspecific aggressive interactions. To test whether interspecific male aggression between Si. laticeps and Sa. darwini results in agonistic character displacement, we quantified species recognition and signalling behaviour using staged encounter assays with both conspecifics and heterospecifics across sympatric and allopatric populations of both species. We found an asymmetric pattern, wherein males of Si. laticeps but not Sa. darwini showed differences in competitor recognition and agonistic signalling traits (morphology and behaviour) in sympatry compared with allopatry. This asymmetric shift in traits is probably due to differences in competitive abilities between species and can minimize competitive interactions in zones of sympatry. Overall, our results support agonistic character displacement, and highlight the role of asymmetric interspecific competition in driving shifts in social signals.

Asymmetric interspecific competition drives shifts in signalling traits in fan-throated lizards: Signal divergence in lizards

Asymmetric interspecific competition drives shifts in signalling traits in fan-throated lizards: Signal divergence in lizards

Exploring a novel substrate‐borne vibratory signal in the wolf spider Schizocosa floridana

AbstractAnimals communicate using a diversity of signals produced by a wide array of physical structures. Determining how a signal is produced provides key insights into signal evolution. Here, we examine a complex vibratory mating display produced by male Schizocosa floridana wolf spiders. This display contains three discrete substrate‐borne acoustic components (known as “thumps”, “taps”, and “chirps”), each of which is anecdotally associated with the movement of a different body part (the pedipalps, legs, and abdomen respectively). In order to determine the method of production, we employ a combination of high‐speed video/audio recordings and SEM imaging of possible sound‐producing structures. Previous work has suggested that the “chirp” component is tonal, a signal trait that would be potentially unique in the genus. We measured signal tonality for all courtship components, as well as for courtship components from sixteen other Schizocosa wolf spiders. Our results suggest that S. floridana produces courtship song using a combination of shared (palpal stridulation and foreleg percussion) and novel (abdominal movement) sound production mechanisms. Of particular interest, the “chirp”, which is produced using a novel abdominal production mechanism, is the only known tonal signal with acoustic properties that are unique within the genus. We argue that the potential evolution of a novel sound production mechanism has opened up a new axis of signaling trait space in this species, with important implications for how this signal is likely to function and evolve.

Sex-specific relationships between urbanization, parasitism, and plumage coloration in house finches

Abstract Historically, studies of condition-dependent signals in animals have been male-centric, but recent work suggests that female ornaments can also communicate individual quality (e.g., disease state, fecundity). There also has been a surge of interest in how urbanization alters signaling traits, but we know little about if and how cities affect signal expression in female animals. We measured carotenoid-based plumage coloration and coccidian (Isospora spp.) parasite burden in desert and city populations of house finches Haemorhous mexicanus to examine links between urbanization, health state, and feather pigmentation in males and females. In earlier work, we showed that male house finches are less colorful and more parasitized in the city, and we again detected such patterns in this study for males; however, urban females were less colorful, but not more parasitized, than rural females. Moreover, contrary to rural populations, we found that urban birds (regardless of sex) with larger patches of carotenoid coloration were also more heavily infected with coccidia. These results show that urban environments can disrupt condition-dependent color expression and highlight the need for more studies on how cities affect disease and signaling traits in both male and female animals.

Motorway age is linked to larger body size, but not song carrier frequency, in male grasshoppers from roadside populations

Producing calls with increased minimum carrier frequency is well documented in sound communicating species confronted with noise pollution, possibly helping them to avoid acoustic masking of low-frequency signals. However, the lack of studies on invertebrates limits our understanding of the potentially adverse effects of anthropogenic noise on natural populations. While males of the grasshopper Chorthippus biguttulus are known to produce courtship signals with elevated low-frequency local maxima (LFLM) in roadside populations, previous studies provided no insight into morphological traits underlying LFLM shifts. Although developmental plasticity was identified as one main factor accounting for elevated LFLM, an additional role for a more hard-wired trait architecture was proposed, possibly as a result of adaptation to traffic noise. Our current study therefore aims to assess (1) whether the position of LFLM is related to male body size, (2) whether body size is correlated with motorway age, and (3) whether the position of LFLM is correlated with motorway age in C. biguttulus males from roadside populations. In addition to substantial variation in LFLM among C. biguttulus males, we found that larger males produced signals with lower LFLM, suggesting a potential role in female choice as a predictor of male quality. While we found no significant correlation between LFLM and motorway age, C. biguttulus males were larger near older motorway sections. This positive correlation may be due to several reasons, including: (1) higher nutrient concentration and availability in plant tissues due to eutrophication of roadside habitats; (2) temporal succession of male size phenotypes during colonization processes; and/or (3) selection for larger body size in roadside populations. Our results highlight the multifaceted and often complex nature of the relationships between morphology, signal traits and anthropogenic pressures on sound communication in invertebrates.

Testosterone induces plumage ornamentation followed by enhanced territoriality in a female songbird

AbstractWe know little of the proximate mechanisms underlying the expression of signaling traits in female vertebrates. Across males, the expression of sexual and competitive traits, including ornamentation and aggressive behavior, is often mediated by testosterone. In the white-shouldered fairywren (Malurus alboscapulatus) of New Guinea, females of different subspecies differ in the presence or absence of white shoulder patches and melanic plumage, whereas males are uniformly ornamented. Previous work has shown that ornamented females circulate more testosterone and exhibit more territorial aggression than do unornamented females. We investigated the degree to which testosterone regulates the expression of ornamental plumage and territorial behavior by implanting free-living unornamented females with testosterone. Every testosterone-treated female produced a male-like cloacal protuberance, and 15 of 20 replaced experimentally plucked brown with white shoulder patch feathers but did not typically produce melanic plumage characteristic of ornamented females. Testosterone treatment did not elevate territorial behavior prior to the production of the plumage ornament or during the active life of the implant. However, females with experimentally induced ornamentation, but exhausted implants, increased the vocal components of territory defense relative to the pretreatment period and also to testosterone-implanted females that did not produce ornamentation. Our results suggest that testosterone induces partial acquisition of the ornamental female plumage phenotype and that ornament expression, rather than testosterone alone, results in elevations of some territorial behaviors.

Altered mechanisms of genital development identified through integration of DNA methylation and genomic measures in hypospadias

Hypospadias is a common birth defect where the urethral opening forms on the ventral side of the penis. We performed integrative methylomic, genomic, and transcriptomic analyses to characterize sites of DNA methylation that influence genital development. In case–control and case-only epigenome-wide association studies (EWAS) of preputial tissue we identified 25 CpGs associated with hypospadias characteristics and used one-sample two stage least squares Mendelian randomization (2SLS MR) to show a causal relationship for 21 of the CpGs. The largest difference was 15.7% lower beta-value at cg14436889 among hypospadias cases than controls (EWAS P = 5.4e−7) and is likely causal (2SLS MR P = 9.8e−15). Integrative annotation using two-sample Mendelian randomization of these methylation regions highlight potentially causal roles of genes involved in germ layer differentiation (WDHD1, DNM1L, TULP3), beta-catenin signaling (PKP2, UBE2R2, TNKS), androgens (CYP4A11, CYP4A22, CYP4B1, CYP4X1, CYP4Z2P, EPHX1, CD33/SIGLEC3, SIGLEC5, SIGLEC7, KLK5, KLK7, KLK10, KLK13, KLK14), and reproductive traits (ACAA1, PLCD1, EFCAB4B, GMCL1, MKRN2, DNM1L, TEAD4, TSPAN9, KLK family). This study identified CpGs that remained differentially methylated after urogenital development and used the most relevant tissue sample available to study hypospadias. We identified multiple methylation sites and candidate genes that can be further evaluated for their roles in regulating urogenital development.

Addressing incomplete lineage sorting and paralogy in the inference of uncertain salmonid phylogenetic relationships.

Recent and continued progress in the scale and sophistication of phylogenetic research has yielded substantial advances in knowledge of the tree of life; however, segments of that tree remain unresolved and continue to produce contradicting or unstable results. These poorly resolved relationships may be the product of methodological shortcomings or of an evolutionary history that did not generate the signal traits needed for its eventual reconstruction. Relationships within the euteleost fish family Salmonidae have proven challenging to resolve in molecular phylogenetics studies in part due to ancestral autopolyploidy contributing to conflicting gene trees. We examine a sequence capture dataset from salmonids and use alternative strategies to accommodate the effects of gene tree conflict based on aspects of salmonid genome history and the multispecies coalescent. We investigate in detail three uncertain relationships: (1) subfamily branching, (2) monophyly of Coregonus and (3) placement of Parahucho. Coregoninae and Thymallinae are resolved as sister taxa, although conflicting topologies are found across analytical strategies. We find inconsistent and generally low support for the monophyly of Coregonus, including in results of analyses with the most extensive dataset and complex model. The most consistent placement of Parahucho is as sister lineage of Salmo.

Variation in carotenoid-containing retinal oil droplets correlates with variation in perception of carotenoid coloration

In the context of mate choice, males may vary continuously in their expression of assessment signals, typically reflecting information about variation in mate quality. Similarly, females may exhibit variation in mate preference, which could be due to differences in how individual females perceive signals. The extent to which perception varies across individuals, however, and whether differences in sensory physiology underlie perceptual differences is poorly understood. Carotenoid pigments create the orange-red coloration of many assessment signals, and they also play a role in color discrimination in many vertebrates via their presence in retinal oil droplets. Here, we link variation in oil droplet carotenoid concentration with the ability of female zebra finches (Taeniopygia guttata) to discriminate an orange-red color continuum that parallels variation in male beak color, a mate assessment signal. We have shown previously that zebra finch females perceive this color range categorically, meaning they label color stimuli from this continuum as belonging to two categories and exhibit better discrimination between colors from different categories as compared with equally different colors from within a category. We quantified behavioral color discrimination and R-type (red) cone oil droplet spectral absorption, a proxy for carotenoid concentration. Oil droplet absorption was strongly predictive of variation in behavioral color discrimination ability. In particular, higher carotenoid concentration in oil droplets correlated with increased discrimination of colors from different sides of the previously identified category boundary. These data show that differences in the sensory periphery can correlate with individual variation in perception of a signal-relevant color range.Significance statementSignal receivers vary in their preferences for signaling traits, but whether this is due to variation in how different receivers perceive signals is not well-understood. We show that variation between individual zebra finch females in perception of an orange-red continuum range correlates with the carotenoid concentration of retinal oil droplets. These data provide the first direct evidence that individual variation in oil droplet carotenoid concentration can lead to variation in color discrimination ability. Linking variation in signal-relevant color discrimination ability with variation in retinal physiology suggests a potential mechanism contributing to individual variation in signal assessment.

Does breeding season variation affect evolution of a sexual signaling trait in a tropical lizard clade?

Sexually selected traits can be expected to increase in importance when the period of sexual behavior is constrained, such as in seasonally restricted breeders. Anolis lizard male dewlaps are classic examples of multifaceted signaling traits, with demonstrated intraspecific reproductive function reflected in courtship behavior. Fitch and Hillis found a correlation between dewlap size and seasonality in mainland Anolis using traditional statistical methods and suggested that seasonally restricted breeding seasons enhanced the differentiation of this signaling trait. Here, we present two tests of the Fitch–Hillis Hypothesis using new phylogenetic and morphological data sets for 44 species of Mexican Anolis. A significant relationship between dewlap size and seasonality is evident in phylogenetically uncorrected analyses but erodes once phylogeny is accounted for. This loss of strong statistical support for a relationship between a key aspect of dewlap morphology and seasonality also occurs within a species complex (A. sericeus group) that inhabits seasonal and aseasonal environments. Our results fail to support seasonality as a strong driver of evolution of Anolis dewlap size. We discuss the implications of our results and the difficulty of disentangling the strength of single mechanisms on trait evolution when multiple selection pressures are likely at play.

The influence of predation risk on mate signaling and mate choice in the lesser waxmoth Achroia grisella

Mating signals are often conspicuous and can be eavesdropped on by predators. Therefore, it is expected that predation risk will shape the evolution of sexual communication in both senders and receivers. Males of the lesser waxmoth Achroia grisella produce ultrasonic signals to attract females, and females have preferences for certain signal traits. When they detect predator cues such as bat echolocation calls, males typically stop signaling and females freeze. Here we examine different ways in which predation risk affects male signaling and female choice. We exposed calling males to predator cues under three different treatments: in isolation, within a simulated lek composed of attractive males, or within a simulated lek of unattractive males. We also tested if female choice depends on predation risk by submitting females to a two-choice test between an attractive and an unattractive signal, in the presence and the absence of predator cues. We found that risk-taking behavior is not only impacted by the presence of competitors, but by the competitors’ attractiveness as well. Additionally, more attractive males take more risks when calling in isolation, but not when lekking. In females, we found that preference for the more attractive call disappeared when the attractive call was associated with higher predation risk. These results reinforce the trade-off between traits that increase survival and mate attraction, and bring new insight into the evolution of leks in this species.

The evolution of sexual signaling is linked to odorant receptor tuning in perfume-collecting orchid bees

Sexual signaling is an important reproductive barrier known to evolve early during the formation of new species, but the genetic mechanisms that facilitate the divergence of sexual signals remain elusive. Here we isolate a gene linked to the rapid evolution of a signaling trait in a pair of nascent neotropical orchid bee lineages, Euglossa dilemma and E. viridissima. Male orchid bees acquire chemical compounds from their environment to concoct species-specific perfumes to later expose during courtship. We find that the two lineages acquire chemically distinct perfumes and are reproductively isolated despite low levels of genome-wide differentiation. Remarkably, variation in perfume chemistry coincides with rapid divergence in few odorant receptor (OR) genes. Using functional assays, we demonstrate that the derived variant of Or41 in E. dilemma is specific towards its species-specific major perfume compound, whereas the ancestral variant in E. viridissima is broadly tuned to multiple odorants. Our results show that OR evolution likely played a role in the divergence of sexual communication in natural populations.

Speech-based automatic personality trait prediction analysis

Automatic personality perception is the prediction of personality that others attribute to a person in a given situation. The aim of automatic personality perception is to predict the personality of the speaker perceived by the listener from nonverbal behaviour. Extroversion, conscientiousness, agreeableness, neuroticism, and openness are the speaker traits used for personality assessment. In this work, a speaker trait prediction approach for automatic personality assessment has been proposed. This approach is based on modelling the relationship between speech signal and personality traits. The experiments are performed over the SSPNet speaker personality corpus. For speaker trait prediction, support vector machines (SVM), multilayer perceptron (MLP), and instance-based k-nearest neighbour were analysed with multiple features. Various features have been analysed to find suitable feature for various speaker traits. The analyses have been conducted using pitch, formant, and mel frequency cepstral coefficients (MFCC) and the analysis results are presented. The accuracy of 100% has been obtained for MFCC features with 19 coefficients.

Habitat structure drives the evolution of aerial displays in birds.

John Endler's sensory drive hypothesis posits that physical properties of the environment may shape signalling traits by determining how effective they are in communicating. Evidence abounds of signalling environment driving selection on colours and vocalizations, yet little is known about its influence on visual signals produced via body movements (i.e., gestural displays). Here, we aimed to perform the most taxonomically comprehensive assessment of sensory drive by testing the hypothesis that habitat structure drives the evolution of aerial sexual displays in passerine birds (order Passeriformes). We base this hypothesis on physical properties of habitats that should allow aerial displays to transmit more broadly in open habitats. To test the hypothesis, we performed Bayesian phylogenetic comparative analyses using species-level phylogenetic trees and a dataset of 469 species from across the Americas. We found that evolutionary gain of aerial displays is on average six times more frequent in open-habitat passerines than in forest ones. The influence of habitat structure on the evolution of aerial sexual displays attests to the importance of sensory drive as a deterministic evolutionary force within sexual selection, as opposed to models that assume a purely arbitrary direction of sexual trait evolution.

Heightened perception of competition hastens courtship

AbstractWhen animals use costly labile display or signal traits to display to the opposite sex, they face complex decisions regarding the degree and timing of their investment in separate instances of trait expression. Such decisions may be informed by not only the focal individual’s condition (or pool of available resources) but also aspects of the social environment, such as perceptions of same-sex competition or the quality of available mates. However, the relative importance of these factors to investment decisions remains unclear. Here, we use manipulations of condition (through dietary nutrition), recent social environment (exposure to a silenced male, nonsilenced male, female, or isolation), and female mating history (single or multiple male) to test how quickly male decorated crickets (Gryllodes sigillatus) decide to begin courting an available female. We find that males that were previously housed with nonsilenced males started courting the female earlier than other males. Females only mounted males after courtship began. Our results suggest a strong effect of the perception of competition on the decision to invest resources in sexual signaling behavior and that females might exert directional selection on its timing.