Role In Sexual Signalling Research Articles

Decoupling of sexual signals and their underlying morphology facilitates rapid phenotypic diversification.

How novel phenotypes evolve is challenging to imagine because traits are often underlain by numerous integrated phenotypic components, and changes to any one form can disrupt the function of the entire module. Yet novel phenotypes do emerge, and research on adaptive phenotypic evolution suggests that complex traits can diverge while either maintaining existing form-function relationships or through innovations that alter form-function relationships. How these alternate routes contribute to sexual signal evolution is poorly understood, despite the role of sexual signals in generating biodiversity. In Hawaiian populations of the Pacific field cricket, male song attracts both female crickets and a deadly acoustically orienting parasitoid fly. In response to this conflict between natural and sexual selection, male crickets have evolved altered wing morphologies multiple times, resulting in loss and dramatic alteration of sexual signals. More recently, we and others have observed a radical increase in sexual signal variation and the underlying morphological structures that produce song. We conducted the first combined analysis of form (wing morphology), function (emergent signal), and receiver responses to characterize novel variation, test alternative hypotheses about form-function relationships (Form-Function Continuity vs. Form-Function Decoupling), and investigate underlying mechanistic changes and fitness consequences of novel signals. We identified three sound-producing male morphs (one previously undescribed, named "rattling") and found that relationships between morphology and signals have been rewired (Form-Function Decoupling), rapidly and repeatedly, through the gain, loss, and alteration of morphological structures, facilitating the production of signals that exist in novel phenotypic space. By integrating across a hierarchy of phenotypes, we uncovered divergent morphs with unique solutions to the challenge of attracting mates while evading fatal parasitism.

Evaluating genital skin color as a putative sexual signal in wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins.

Coevolution between signalers and receivers has played a significant role in the diversity of animal signals and sensory systems. Platyrrhines (monkeys in the Americas) exhibit a remarkable color vision polymorphism that may have been selected by both natural and sexual selection, but sociosexual color signaling among platyrrhines has received almost no attention. Here, we study the color of reproductive skin among different reproductive classes in free-ranging female saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins, modeling color spaces, and contrasts for the different visual systems. We find that the chromatic saturation and luminance of genital color vary between reproductive classes in saddleback tamarins. Chromatic contrast between the vulva and belly is lower in the parous females (PFs) relative to adult but not currently breeding females, while achromatic contrast is higher in PFs in saddleback tamarins relative to nonparous females. However, in emperor tamarins, genital color (saturation, hue, and luminance) does not vary between reproductive classes. Overall, genital skin color variation is present in tamarins and may play a role in sexual signaling. Nevertheless, the patterns are inconsistent between species, suggesting interspecific variation. Future studies should integrate the perceiver's behavioral responses and the physical and social signaling environments into comprehensive studies of communication as well as consider the role and interaction between multiple sensory modalities.

Effects of age and weather during moult on mountain bluebird Sialia currucoides structural colouration

Birds exhibit a vast array of colours and ornaments and while much work has focused on understanding the function and evolution of carotenoid-based colours (red, orange, yellow), structural colouration (blue, green, purple, iridescent) can also play a key role in sexual signaling. Several studies have examined how factors such age may influence structural colour, however few studies have looked at how structural colour may be influenced by environmental conditions such as variation in weather conditions experienced during moult. In this study, we examined variation in structural colour expression in relation to age as well as rainfall and temperature during post-breeding moult for a population of mountain bluebirds Sialia currucoides in western Canada over nine breeding seasons. Overall, we found structural colouration was explained by sex, age and weather patterns during moult. At a population level, tail and rump feathers from males were more colourful (higher brightness and chroma, hue values shifted more towards UV) than females, and adults were more colourful than juvenals. Male and female rump feathers generally became less colourful with age. Noise-receptor colour models revealed colour differences were discernible among sexes, suggesting bluebird colouration is an important sexual signal. Tail and rump plumage variation was associated with weather during moulting periods, though the effects were sex- and age-dependent. Female plumage was generally more colourful following wetter and warmer early summers, while males were more colourful following warmer late summers, and plumage of older birds was more resilient to colour variation due to weather patterns. We suggest that more rainfall may increase insect abundance and thus improve food intake and overall condition of mountain bluebirds. This is one of the first studies to examine how both age and weather conditions concurrently influence the expression of structural colours in birds.

Facial band colour in the mangrove crab Parasesarma peninsulare Shahdadi, Ng & Schubart, 2018 plays a role in mate recognition

Various crab taxa are known to use their external colouration as visual courtship signals. Early research on the mangrove crab Parasesarma peninsulare Shahdadi et al., 2018 indicated a potential role in sexual signalling for its bright blue-green facial bands, which are highly conspicuous against mangrove mud. To advance this work, we conducted experiments investigating both male responses to female stimuli and female responses to male stimuli. Two sets of binary choice experiments were performed—one with live crabs and one using androgyne images where the only sex-specific cue was facial band colour—to test whether the crabs could distinguish between male and female conspecifics based on the colour of their facial band alone, i.e. independent of auditory, chemical and other visual cues. In both cases, the crabs showed a significantly greater preference for conspecifics of the opposite sex (i.e. males preferred females and vice versa). These results provide evidence for colour vision in Parasesarma and suggest that the facial bands are used by the crabs for sexual discrimination and mate recognition.

Male Bicyclus anynana Butterflies Choose Females on the Basis of Their Ventral UV-Reflective Eyespot Centers.

Butterflies often use their dorsal and ventral wing color patterns for distinct signaling functions. Color patterns on hidden dorsal wing surfaces are often used in sexual signaling, while exposed ventral patterns are often used to ward off predator attacks. At rest, however, part of the ventral forewings are often hidden by the hindwings, allowing individuals to also use the patterns on this wing surface for sexual signaling. Here, we test this hypothesis in Bicyclus anynana (Butler, Lepidoptera, Nymphalidae) butterflies by first determining the degree of sexual dimorphism in ventral forewing patterns, focusing on the eyespots, from both wet and dry season forms, and then testing the role of the larger ventral forewing eyespots of dry season females in male mate choice. We also test male investment in reproduction. We show that ventral forewing UV-reflective eyespot centers, in addition to dorsal forewing eyespot centers previously examined in this species, play a role in sexual signaling as males preferentially mated with females with their ventral eyespot centers intact instead of blocked with black paint. This male preference, however, did not translate into a detectable higher reproductive investment via a single mating toward ornamented females. This study provides an example of how ventral forewing patterns, often hidden by hindwings, are used in sexual communication, in this case by females to attract males.

Plumage brightness and uropygial gland secretions in barn swallows.

The uropygial gland has been hypothesized to play a role in sexual signaling through a “make-up” function derived from the effects of secretions from the gland on the appearance of the plumage and bare parts of the body. Here we show that plumage brightness of dorsal feathers of individual barn swallows Hirundo rustica was greater in mated than in unmated individuals. In addition, plumage brightness increased with colony size. Furthermore, plumage brightness was positively correlated with the amount of wax in the uropygial gland, negatively correlated with time of sampling of uropygial wax (perhaps because more wax is present early in the morning after an entire night of wax production without any preening), and negatively correlated with the number of chewing lice that degrade the plumage. Experimentally preventing barn swallows from access to the uropygial gland reduced plumage brightness, showing a causal link between secretions from the uropygial gland and plumage brightness. These findings provide evidence consistent with a role of uropygial secretions in signaling plumage brightness.

Insect Cuticular Hydrocarbons as Dynamic Traits in Sexual Communication

Recent research has demonstrated extensive within-species variation in pheromone expression in insect species, contrary to the view that pheromones are largely invariant within species. In fact, many studies on insect cuticular hydrocarbons (CHCs) show that pheromones can be highly dynamic traits that can express significant short-term plasticity across both abiotic and social environments. It is likely that this variability in CHC expression contributes to their important role in sexual signaling and mate choice. In this review, I discuss CHC plasticity and how this might influence sexual communication. I also highlight two important avenues for future research: examining plasticity in how individuals respond to CHC signals, and testing how sexual communication varies across abiotic and social environments.

Inter-annual variation in American redstart (Setophaga ruticilla) plumage colour is associated with rainfall and temperature during moult: an 11-year study.

Carotenoid-based colouration plays an important role in sexual signaling in animals as an honest indicator of individual quality during mate choice and competitive interactions. However, few studies have examined how natural variation in weather conditions influences inter-annual variation in the expression of ornamentation, potentially through affecting the dietary availability of carotenoids. In this study, we examine variation in the expression of carotenoid-based plumage colouration in relation to temperature and rainfall during the pre-moulting and moulting period over 11 years in a population of American redstarts, Setophaga ruticilla, breeding in eastern Canada. We used reflectance spectrometry of tail feathers collected from male and female redstarts to relate feather colour with weather conditions the previous breeding season during the months over which redstarts are likely to moult (June-September). At a population level, birds expressed feathers with higher red chroma and lower brightness in years following high July rainfall and low August temperature. The pattern was stronger in males, but was generally consistent across ages and sexes. Analyses of feathers from repeatedly captured birds indicated that the above patterns could be explained by individual change in feather colour. We suggest that higher rainfall during the moulting period may increase insect abundance and the availability of dietary carotenoids. This is among the first studies to show effects of weather conditions on a sexual signalling trait, which may have important consequences for sexual selection, mate choice, and the reliability of putative signals.

Covariation between bill colouration and fitness components in a nocturnal bird

Vividly coloured chromatic signals play a key role in social and sexual signalling in diurnal birds, but their role is considered negligible in favour of achromatic (i.e. white, pure grey and black colourations) signals in nocturnal species. Here we studied colour variation and potential signalling of the yellow bill – a trait functioning as sexual signal in diurnal raptors during the breeding season in females of a truly nocturnal raptor, the little owl Athene noctua. We found that yellow‐red chroma of the bill was highly variable between individuals and positively correlated with female fitness prospects (i.e. brood size at fledging). In addition, we found that females with brighter bills were larger in size and produced owlets with a higher mass at fledging. This study suggests that yellow bill colouration in female little owls may potentially play a role in sexual signalling and may constitute the first evidence of chromatic colour signalling in a nocturnal bird.

Secretions of pre-anal glands of house-dwelling geckos (Family: Gekkonidae) contain monoglycerides and 1,3-alkanediol. A comparative chemical ecology study

Abstract Squamate reptiles sense chemical stimuli carrying information about several biological properties of the sender. Despite the fact that sex recognition is often based on colour signals, such pheromone communication occurs in many species of lizards. Epidermal gland secretions of reptiles can have pheromone properties and might play an important role in sexual signalling and territorial scent marking. The house-dwelling geckos Hemidactylus turcicus , Hemidactylus flaviviridis , and Cyrtopodion scabrum are good examples of geckos having pre-anal glands in males only. We used GC–MS chemical analysis of gland secretions, compared secretions of different species, and compared secretions from two populations of H. turcicus . Surprisingly, we detected monoglycerides of fatty acids, and one 1,3-alkanediol. These compounds have been detected once before in reptiles. In addition, carboxylic acids, alcohols, steroids, alkanes, amides, one aldehyde, carboxylic acid esters, hydrocarbons, and squalene occurred. Polyol glycerol seems to play a role in the composition of the secretions probably as an adhesive of some kind for the secretion as a whole. The data supports our hypothesis that geckos can potentially use femoral gland secretions in chemical communication. Further studies are needed to test activities of these compounds in behavioural assays to eventually identify their possible role in communication.

The contribution of structural‐, psittacofulvin‐ and melanin‐based colouration to sexual dichromatism in Australasian parrots

Colour ornamentation in animals is exceptionally diverse, but some colours may provide better signals of individual quality or more efficient visual stimuli and, thus, be more often used as sexual signals. This may depend on physiological costs, which depend on the mechanism of colour production (e.g. exogenously acquired colouration in passerine birds appears to be most sexually dichromatic). We studied sexual dichromatism in a sample of 27 Australasian parrot species with pigment- (melanin and psittacofulvin) and structural-based colouration, to test whether some of these types of colouration are more prominent in sexual ornamentation. Unlike passerines, in which long wavelength colouration (yellow to red) usually involves exogenous and costly carotenoid pigments, yellow to red colouration in parrots is based on endogenously synthesized psittacofulvin pigments. This allows us to assess whether costly exogenous pigments are necessary for these plumage colours to have a prominent role in sexual signalling. Structural blue colouration showed the largest and most consistent sexual dichromatism, both in area and perceptually relevant chromatic differences, indicating that it is often ornamental in parrots. By contrast, we found little evidence for consistent sexual dichromatism in melanin-based colouration. Unlike passerines, yellow to red colouration was not strongly sexually dichromatic: although the area of colouration was generally larger in males, colour differences between the sexes were on average imperceptible to parrots. This is consistent with the idea that the prominent yellow to red sexual dichromatism in passerines is related to the use of carotenoid pigments, rather than resulting from sensory bias for these colours.

Optical properties of the uropygial gland secretion: no evidence for UV cosmetics in birds

Ultraviolet (UV) reflectance of the plumage is common in birds and plays an important role in sexual signalling. Recently, it has been proposed that birds are able to modify plumage UV reflectance by the application of uropygial gland secretion. Based on a survey of the optical properties of this secretion from 51 species belonging to 12 avian orders, we show that two main types of uropygial secretions exist, one predominantly found in passerines and one in non-passerines, both reducing relative UV reflectance of a white background (Teflon tape). We quantified how each type of secretion (exemplified by blue tit and mallard) affected feather UV reflectance. Both secretions reduced overall brightness and relative UV reflectance of white mallard feathers but hardly affected the reflectance of UV/blue blue tit crown feathers. According to models of avian colour vision, changes in reflectance due to application of the secretion were at or below the discrimination threshold of most birds. We conclude that the uropygial secretion is unlikely to play a major role in modifying plumage UV reflectance. However, the optical properties of the uropygial secretion may have been selected to interfere as little as possible with visual signaling through plumage reflectance.

Obligate asex in a rotifer and the role of sexual signals

Transitions to asexuality have occurred in many animals and plants, yet the biological mechanisms causing such transitions have often remained unclear. Cyclical parthenogens, such as cladocerans, rotifers or aphids often give rise to obligate asexual lineages. In many rotifers, chemical signals that accumulate during population crowding trigger the induction of sexual stages. In this study, I tested two hypotheses on the origin of obligate parthenogenesis in the rotifer Brachionus calyciflorus: (i) that obligate parthenogens have lost the responsiveness to the sexual signal; and (ii) that obligate parthenogens have lost the ability to produce the sexual signal. Pairwise cross-induction assays among three obligate parthenogenetic strains and two cyclically parthenogenetic (sexual) strains were used to test these hypotheses. I found that obligate parthenogens can induce sexual reproduction in sexual strains, but not vice versa. This demonstrates that obligate parthenogens do still produce the sexual signal, but have lost responsiveness to that signal.

Ultraviolet Ornamentation and Male Mating Success in a High-Density Assemblage of the Butterfly Colias eurytheme

Ultraviolet (UV) colour patterns, particularly those deriving from surface structures, serve a role in sexual signalling and mate choice in a range of animal groups. In the butterfly Colias eurytheme (Pieridae), male-limited iridescent UV functions in species recognition, and has potential as an intraspecific sexual signal of mate quality. I compared the dorsal colouration and body size of males discovered ‘in-copula’ (N = 95) with a random sample of free-flying individuals (N = 129), both collected from a high density agricultural population located in Chandler, U.S.A. Despite reasonable variance in each trait, I found no among-group differences in UV characters (brightness, hue and angular visibility) or in the coincident pigmentary yellowish-orange (brightness and saturation). Statistical power was sufficient to detect all but the smallest among-group differences, and there was a marginally significant tendency for in-copula males to be larger. These data do not support the hypothesis for intraspecific female choice upon male dorsal colouration. However, I discuss how the density and apparently very young age of individuals in the sampling population may have pre-disposed this result, and thus, how sexual selection on male colouration may operate in a density dependent manner.

Achromatic Plumage Reflectance, Social Dominance and Female Mate Preference in Black‐Capped Chickadees (Poecile atricapillus)

AbstractIndividual variation in achromatic plumage reflectance of male Black‐capped Chickadees (Poecile atricapillus) is correlated with social rank and reproductive success, suggesting it may play an important role in sexual signaling. We asked whether female chickadees could assess male quality based on plumage, in the absence of information about relative social dominance. Sexually mature but inexperienced females captured during the pair formation period in late fall and early winter were presented with a choice of two unfamiliar, sexually experienced males in separate compartments of an outdoor mate choice arena. Following each preference trial, we released the males into a single compartment and scored their pairwise dominance interactions. In 10 of 11 trials, females spent significantly more time with the male subsequently identified as dominant, despite not witnessing the males interact. Spectral analysis of male plumage reflectance revealed that UV‐chroma of dark body regions (bib, cap and mantle) was significantly greater in dominant, preferred males and that dominant, preferred males had significantly brighter white cheek patches. There were no differences in vocalization rates of preferred and non‐preferred males. These results show that female chickadees can rapidly assess unfamiliar males based on visual cues, and suggest that variation in achromatic plumage functions in sexual signaling.

Ultra‐violet reflectance of male and female red grouse, Lagopus lagopus scoticus, sexual ornaments reflect nematode parasite intensity

In many birds, females prefer males with the biggest or brightest sexual ornaments, which might reflect a higher phenotypic quality, such as fewer parasites. Unlike humans, most birds detect near‐ultraviolet (UV) light, and UV signals can play an important role in sexual signalling and mate choice. Using a spectrophotometer, we analysed the colour of red grouse Lagopus lagopus scoticus sexual ornaments (their combs). We first show that combs reflect both in the red (600–700 nm) and UV (300–400 nm) part of the spectrum. Second, we investigated whether comb size and colour, and UV reflectance in particular, reflected an aspect of individual quality: the intensity of infection by a main nematode parasite, the caecal threadworm Trichostrongylus tenuis. We first analysed comb size and colour variation, and parasite intensity variation, in relation to sex and age. Males had bigger and redder combs than females, but UV brightness was greater for female than for male combs. Comb colour also differed between age groups, with young birds of both sexes showing brighter UV than old birds. Young grouse also had fewer T. tenuis worms than old grouse. We further tested whether intensity of infection could be predicted from comb characteristics (size and colour) in male and female red grouse. We found that parasite intensity was not significantly related to comb size or red brightness, but fewer worms were predicted from brighter UV in combs, in both males and females. The results indicate that UV reflectance of combs have a quality revealing function and might play an important role in grouse mate choice: UV brightness of combs could enable both male and female red grouse to assess the parasite loads of a potential mate.

Achromatic plumage reflectance predicts reproductive success in male black-capped chickadees

The size of achromatic (black, white, gray) plumage patches serves as a male status signal in many species of birds, but variation in the colors of these patches has received little attention. We assessed the relation between achromatic plumage reflectance, dominance rank, body condition, and reproductive success in male black-capped chickadees, Poecile atricapillus. We measured plumage reflectance for five body regions of 40 male chickadees in late winter and monitored these males throughout the following breeding season to determine whether they survived to breed, whether they successfully paired, whether their partner laid eggs, and both their apparent and realized reproductive success. As expected from past studies, a male's dominance rank significantly predicted whether his partner laid eggs. However, only achromatic plumage reflectance significantly predicted other measures of male reproductive performance. Among males who fledged at least one offspring, both the brightness of white plumage regions and the UV-chroma of melanin-based plumage regions were significant predictors of the proportion of within-pair young in their nests. When we consider all males we measured, assigning zero values to males who failed to sire any offspring, the UV-chroma of melanin-based plumage regions was a significant predictor of realized reproductive success. Bib size was also related to male realized reproductive success. Our findings suggest that individual variation in achromatic plumage may play an important role in sexual signaling in chickadees.

The Role of Ultraviolet‐A Reflectance and Ultraviolet‐A‐Induced Fluorescence in Budgerigar Mate Choice

AbstractMany parrots have plumage that either reflects strongly in the ultraviolet‐A (UVA) waveband, between 315–400 nm, or exhibits UVA‐induced fluorescence. Previous experimental work on budgerigars (Melopsittacus undulatus) suggests that UVA reflectance plays a role in mate choice, as in other diurnal birds, but evidence for fluorescent cues playing a role is unconvincing. Here we report two experiments on budgerigars, designed to determine whether fluorescent cues play a role in signalling when UVA reflectances are absent, an approach which separates removal of UVA reflectance from removal of fluorescence. First, we determined whether the choices of different females are correlated under these treatment conditions. Secondly, we investigated female preferences for fluorescing and non‐fluorescing males when UVA reflections are absent, to determine whether the yellow emissions of fluorescence are playing a role in mate choice. Results from experiment 1 do not suggest that females agree on which males are attractive when UVA reflectances are absent, with only half of the subjects choosing the same male. Neither did different females make the same choices in experiment 2. This lack of agreement provides further evidence that UVA reflectances from males play an important role in female choice in this species. Experiment 2 provides no evidence to suggest that UVA‐induced fluorescence plays a role in mate choice. Overall, our study supports previous findings showing that UVA reflectance plays a role in sexual signalling in this species, but provides no evidence to suggest the same for fluorescence when UVA reflectances are absent.

The role of ultraviolet-A reflectance and ultraviolet-A induced fluorescence in the appearance of budgerigar plumage: insights from spectrofluorometry and reflectance spectrophotometry.

Fluorescence has so far been found in 52 parrot species when illuminated with ultraviolet-A (UVA) 'black' lamps, and two attempts have been made to determine whether such fluorescence plays any role in sexual signalling. However, the contribution of the reflectance versus fluorescence to the total radiance from feathers, even in the most studied species to date (budgerigars), is unclear. Nor has the plumage of this study species been systematically assessed to determine the distribution of fluorescent patches. We therefore used spectrofluorometry to determine which areas of budgerigars fluoresce and the excitation and emission spectra involved; this is the first time that such a technique has been applied to avian plumage. We found that both the yellow crown and (normally hidden) white downy chest feathers exhibit strong UVA-induced fluorescence, with peak emissions at 527 nm and 436 nm, respectively. Conversely, the bright-green chest and dark-blue tail feathers do not fluoresce. When comparing reflectance spectra (400-700 nm) from the yellow crown using illuminants with a proportion of UVA comparable to daylight, and illuminants with all UVA removed, no measurable difference resulting from fluorescence was found. This suggests that under normal daylight the contribution of fluorescence to radiance is probably trivial. Furthermore, these spectra revealed that males had fluorescent crowns with substantially higher reflectance than those of females, in both the UV waveband and at longer wavelengths. Reflectance spectrophotometry was also performed on a number of live wild-type male budgerigars to investigate the chromatic contrast between the different plumage areas. This showed that many plumage regions are highly UV-reflective. Overall our results suggest that rapid surveys using UVA black lamps may overestimate the contribution of fluorescence to plumage coloration, and that any signalling role of fluorescence emissions, at least from the yellow crown of budgerigars, may not be as important as previously thought.

Male courtship song frequency as an indicator of male genetic quality in an insect species, Drosophila montana.

Most theoretical models on evolution of male secondary sexual characters and female preferences for these characters suggest that the male characters evolve in response to female preferences that may themselves evolve in response to direct or indirect benefits of choice. In Drosophila montana (a species of the D. virilis group), females use male song in their mate choice, preferring males that produce songs with short sound pulses and a high carrier frequency. We demonstrate here that the females get indirect benefits from their choice: in our data the frequency of the male song correlated with the survival rate of the male's progeny from egg to adulthood (indirect benefit for the female), but not with the fecundity of his mating partner (no direct benefit for the female). Male wing centroid asymmetry did not correlate with male wing song characters, nor with female egg production nor the fitness of her progeny, suggesting that fluctuating asymmetry in male wings does not play a major role in sexual signalling. The fact that the male song gives the female information on the male's condition/genetic quality in D. montana suggests that in this species the evolution of female preferences for male song characters could have evolved through condition-dependent viability selection presented in some 'good genes' models.