Sexual signal loss,pleiotropy, and maintenance of a male reproductive polymorphism in crickets

Pleiotropy between male signals and female preferences can facilitate evolution of sexual communication by maintaining coordination between the sexes. Alternatively, it can favor variation in the mating system, such as a reproductive polymorphism. It is unknown how common either of these scenarios is in nature. In Pacific field crickets (Teleogryllus oceanicus) on Kauai, Hawaii, a mutation (flatwing) that segregates as a single locus is responsible for the rapid loss of song production in males. We used outbred cricket colonies fixed for male wing morph to investigate whether homozygous flatwing and normal-wing (wild-type) females differ in responsiveness to male calling song and propensity to mate when paired with either a flatwing or normal-wing male in the presence or absence of courtship song. Flatwing females were less likely to mount a male than normal-wing females. Females of both genotypes showed a preference for normal-wing males and were more likely to mate in the presence of courtship song; normal-wing females were particularly likely to mate with song. Our results show that negative pleiotropy between obligate male silence and female mating behavior can constrain the evolution of sexual signal loss and contribute to the maintenance of a male reproductive polymorphism in the wild.     

The functions of multiple visual signals in a fiddler crab

In many species, it is common for animals to have multiple signals within one channel of communication. Multiple signals may, however, be inefficient if they are redundant in nature. Identifying the functional significance of these multiple signals is therefore important if we are to understand the evolution of such elaborated behaviours. We proposed to identify the roles of movement-based multiple signals in a model animal system. Male fiddler crabs wave their sexually dimorphic enlarged claw during social interactions. Some species present multiple signals, where the level of complexity of the movement changes. Males of Austruca mjoebergi can perform a double wave consisting of a high- followed by a low-elevation lifting of the claw, or a single wave consisting of the high-elevation movement alone. We first investigated structural differences between the double and single wave types, and found that single waves were lower in elevation than double waves. We then explored the adaptive meaning of the wave types by manipulating the social context in which males wave. We found that double waves were given in all contexts and in higher proportions at long distances, suggesting a function of broadcasting male location. Single waves, on the other hand, were mainly given at close range and in the presence of conspecifics, suggesting intraspecific communication. Female presence elicited the highest number and proportion of single waves, a likely result of a female preference for higher wave rates. Finally, we point out that there is an element of interaction between wave types that deserves future attention. This paper is an important contribution to expand our understanding of the adaptive meaning of multiple visual signals and help reach a unified theory of their evolution.     

Rapid and socially induced change of a badge of status

This paper reports a new aspect of male signalling in the green swordtail Xiphophorus hellerii. Males are highly ornamented and possess a sword (an extension of the caudal fin), as well as a lateral stripe that has been shown to be a badge of status. Males of one natural population, however, were found to quickly change the colour of their lateral stripe to red when socially dominant over other males and black when subdominant, thereby exploiting the female preference for red stripes while dominant, and avoiding the costs of male aggression while subdominant.     

Ecology and signal structure drive the evolution of synchronous displays*

Animal synchrony is found in phylogenetically distant animal groups, indicating behavioral adaptations to different selective pressures and in different signaling modalities. A notable example of synchronous display is found in fiddler crabs in that males wave their single enlarged claw during courtship. They present species-specific signals, which are composed of distinctive movement signatures. Given that synchronous waving has been reported for several fiddler crab species, the display pattern could influence the ability of a given species to sufficiently adjust wave timing to allow for synchrony. In this study, we quantified the wave displays of fiddler crabs to predict their synchronous behavior. We combined this information with the group's phylogenetic relationships to trace the evolution of display synchrony in an animal taxon. We found no phylogenetic signal in interspecific variation in predicted wave synchrony, which mirrors the general nonphylogenetic pattern of synchrony across animal taxa. Interestingly, our analyses show that the phenomenon of synchronization stems from the peculiarities of display pattern, mating systems, and the complexity of microhabitats. This is the first study to combine mathematical simulations and phylogenetic comparative methods to reveal how ecological factors and the mechanics of animal signals affect the evolution of the synchronous phenomena.     

Nest building, sexual selection and parental investment

Avian nest building has traditionally been viewed as resulting in natural selection advantages, but it is also been associated with courtship and pair formation. We hypothesize that nest-building activity could be used as a sexually selected display, allowing each sex to obtain reliable information on the condition of the other. In this paper, we test the ‘good parent’ process in a scenario where nest size is a sexually selected trait. Thus, individuals with more extreme displays (larger nests) might obtain benefits in terms of either parental investment or differential parental investment by the partner. We predicted that: (1) species in which both sexes contribute to nest building have larger nests than those in which the nest is built only by one sex, because both sexes are using the nest-building process as a signal of their quality; (2) species in which both sexes work together in the nest-building process invest more in reproduction, because each can assess the other more reliably than in species where only one sex participates in nest building; and (3) in light of the two preceding predictions, nest size should be positively related to investment in parental care. A comparative analysis of 76 passerine species confirmed that nest size, relative to the species' body size, is larger when both sexes build the nest and that species with a larger nest relative to their body size invest more in reproduction. This revised version was published online in July 2006 with corrections to the Cover Date.     

Direct and indirect effects of sexual signal loss on female reproduction in the Pacific field cricket (Teleogryllus oceanicus)

Sexual signal evolution may present fitness consequences for the non‐signaling sex due to shared genes and altered social conditions, but this is rarely studied in natural populations. On the Hawaiian Island of Kauai, most male Teleogryllus oceanicus (Pacific field crickets) lack the ability to sing because of a novel wing mutation (flatwing) that arose and spread in <20 generations. Obligately silent flatwing males have been highly successful because they avoid detection by a deadly, acoustically‐orienting parasitoid fly. Little is known about how the flatwing mutation and resulting song‐less acoustic environment affects female fitness. We found that Kauai females carrying the flatwing allele invested less in reproductive tissues and experienced more instances of mating failure than normal‐wing‐carrying females, though total offspring production did not differ between female genotypes. Females from Oahu (HI, where the parasitoid and flatwing also occur) and Mangaia (an island in the Cook Islands which harbors neither the parasitoid nor flatwing) invested less in reproductive tissues when reared in a song‐less acoustic environment. Kauai females did not exhibit this plasticity, perhaps because they have experienced nearly song‐less conditions for the past ~15 years following the establishment of flatwing. We show that female T. oceanicus experience a mix of costly and beneficial effects of sexual signal loss, which should help maintain the wing polymorphism in the wild. Our results demonstrate that the non‐signaling sex can experience a nuanced set of phenotypic consequences resulting from signal evolution, which can further shape dynamics of sexual signal evolution.     

White tail spots in breeding Barn Swallows Hirundo rustica signal body condition during winter moult

The determinants and function of pigmentation of feathers and other tissues have been the focus of a large number of studies, particularly with respect to socio‐sexual communication. However, many birds exhibit depigmented white spots or bars on their feathers whose function is poorly understood. Here we assess whether white feather spots reflect phenotypic condition at the time of moult by investigating the covariation between spot size or shape and condition‐dependent feather growth rate, as gauged by width of the growth bars on the tail feathers of Barn Swallows. We found that feathers with higher growth rates had larger, less rounded white spots. In addition, variance in spot perimeter for a given spot area was larger in males than in females. This study is the first to provide evidence that features of white markings on feathers directly reflect body condition at the time of moult and can therefore reliably signal phenotypic quality in the context of socio‐sexual communication. In addition, the study highlights the potential communication function of the shape and not just the size of colour signals.     

Natural and sexual selection on a plumage signal of status and on morphology in house sparrows,Passer domesticus

Temporal patterns of natural and sexual selection on male badge size and body traits were studied in a population of house sparrows, Passer domesticus. Badge size was a heritable trait as revealed by a significant father-son regression. Survival during autumn dispersal and winter was not related to badge size or body traits in yearling male house sparrows. Badges that signal dominance status were affected positively by directional selection for mating. Adult male house sparrows suffered an opposing selection pressure on badge size during autumn. Contrary to males, female house sparrows did not experience significant directional or stabilizing selection on any body trait. Directional sexual selection on male badge size due to female choice moves male sparrows away from their survival optimum. Opposing directional natural selection on badge size due to autumn mortality caused by predation maintains a stable badge size.     

Temperature coupling as an emergent property: parallel thermal effects on male song and female response do not contribute to species recognition in an acoustic moth

Temperature coupling exists when changes in male signal production with temperature are paralleled by changes in female response. Such thermal effects have been observed in various ectothermic animals producing acoustic, visual, and electric signals in which the signal rate may be subject to stabilizing selection imposed by female preference. Often, coupling was considered as an adaptive function wherein male and female thermal effects coevolved under selection pressure favoring species recognition, although this assumption has not been tested definitively. We investigated thermal effects on pulse-pair rate in male song and female acceptance threshold for male song rate in an acoustic moth, Achroia grisella, in which male song rate is subject to directional selection. Male song rate and female acceptance threshold do exhibit parallel increases as temperature rises from 18 degrees C to 30 degrees C, but female thresholds are much lower than male song rates and the thermal effect on female response cannot augment species recognition. In further investigations using inbred lines of A. grisella we found that the male and female thermal effects are genetically correlated, and we discuss the likely sources of this covariance. We consider several explanations for the occurrence of temperature coupling in this species and suggest that it represents an emergent property arising from the neuromuscular responses to temperature that are common to several physiological systems.     

Stealing behavior and the maintenance of a visual display in the satin bowerbird

Honest signals that indicate male quality have been observedin many species and are thought to have evolved to allow malesto assess rivals accurately and respond to "cheaters." Femalescould potentially also use the same honest signals as reliableindicators of male quality. In bowerbirds, the numbers of specificbower decorations may serve as an honest signal of male quality:this study investigates whether decoration stealing among malesatin bowerbirds at the Bunya Mountains, Australia, may alsoinvolve honest signals. In this study, we aimed to determine1) predictors for the degree to which individual male satinbowerbirds steal, and are stolen from, and 2) predictors forwhy some male pairs interact by stealing, whereas other pairsdo not. We also assessed how experimentally standardizing thenumber of decorations on bowers would affect the 1) frequencyof stealing, 2) specific interactions among males, and 3) distributionof decorations across bowers. Bower decorations were labeledand tracked through one breeding season. Males that were successfulstealers, stole from other successful stealers, had many feathersand bottle tops on their bowers and painted their bower wallsoften. Male pairs were more likely to interact by stealing iftheir bowers were in close proximity. Most of the stealing observedwas of a reciprocal nature. After we standardized the numbersand types of decorations on a small group of males' bowers,the mean number of daily stealing gains and the total numberof males interacting by stealing did not change. In addition,no significant novel stealing interactions were initiated afterthe manipulation. The average number of all bower decorationsand the average number of rosella feathers on a given male'sbower prior to the manipulation were proportional to the averagenumbers for the period after the manipulation. Furthermore,males that originally had better collections of decorationstended to suffer fewer losses due to stealing after the manipulation.Our results suggest that the total number of decorations, thetotal number of rosella feathers on a male's bower, and possiblystealing behavior, may form part of the basis of an honest signalindicating male quality and therefore might be correlated withmating success.     

Phylogenetic Correlation Between Male Nuptial Color and Behavioral Responses to Color Across a Diverse and Colorful Genus of Freshwater Fish (Etheostoma spp., Teleostei: Percidae)

Sexual selection theory predicts that preferences in both sexes select for the elaboration of male nuptial coloration, with empirical evidence supporting these predictions. Empirical studies are often limited in their taxonomic inclusiveness, however, and typically do not examine how male and female preferences contribute to macroevolutionary patterns of male color variation across multiple lineages in a clade. This study examined color preferences in a group of dichromatic freshwater fishes known as darters (genus Etheostoma) that vary in the presence of male coloration. The strengths of attraction to black, blue, gray, and red models were tested in females of 18 species, in addition to males of five species. We found a positive association between the presence of red or orange on the body and the amount of time associating with red models, suggesting color variation is at least in part due to variation in female preferences between species. Males also spent more time associating with colors that most closely resembled conspecifics, suggesting that preferential responses to color in males also can contribute to the diversity of nuptial coloration in darters.     

Male adaptations to minimize sexual cannibalism during reproduction in the funnel‐web spider Hololena curta

Males of many spider species risk being attacked and cannibalized while searching for, courting, and mating with conspecific females. However, there are exceptions. We show that the funnel‐web spider, Hololena curta, has 3 adaptations that minimize risk to males during courtship and mating, and enhance reproductive success. First, males detected chemical or tactile signals associated with webs of virgin females, and differentiated them from webs of mated females, enabling males to increase encounter rates with virgin females and avoid aggressive mated females. Second, males produced stereotyped vibrational signals during courting which induced female quiescence and suppressed female aggression. Third, when touched by males, sexually receptive females entered a cataleptic state, allowing males to safely approach and copulate. Because males can mate multiple times and the sex ratio in natural populations of H. curta is female biased, overall reproductive output is likely increased by males of this species avoiding sexual cannibalism.     

Genetic independence of female signal form and male receiver design in the almond moth, Cadra cautella

Efficient signalling requires coordination of signal form and receiver design. To maintain signal function, parallel changes in signaller and receiver traits are required. Genetic correlation and co-evolution among signal and response traits have been proposed to preserve signal function (i.e. coordination) during the evolution of mate recognition systems. Empirical studies have provided support for both mechanisms; however, there is debate regarding the interpretation of some of these studies. Tests for a genetic correlation typically hybridize divergent signalling systems and look at hybrid signal form and receiver design, or impose artificial selection on signal form and look for an indirect response to selection in receiver design. Some of the hybridization studies did not achieve reassortment of genes from the parental types, whereas some of the artificial selection studies incorporated random mating in their designs. As a result of these limitations, the hybridization studies cannot discriminate between genetic correlation and co-evolution with primarily additive genetic effects underlying signal and response traits. Similarly, the artificial selection experiments cannot discriminate between genetic correlation because of linkage disequilibrium and co-evolution. This study examined the mating preferences of male almond moths, Cadra cautella, before and after female moths were artificially selected (using a design incorporating assortative mating) for novel pheromone blend ratios. Our results demonstrate the absence of a genetic correlation between signal and response traits in the almond moth.     

Detection of female mating status using chemical signals and cues

Males of many species choose their mate according to the female's reproductive status, and there is now increasing evidence that male fitness can depend on this discrimination. However, females will also aim to regulate their mating activity so as to maximize their own fitness. As such, both sexes may attempt to dictate the frequency and timing of female mating, reflecting the potentially different costs of female signaling to both sexes. Here, I review evidence that chemical cues and signals are used widely by males to discriminate between mated and unmated females, and explore the mechanisms by which female odour changes post‐mating. There is substantial empirical evidence that mated and unmated females differ in their chemical profile, and that this variation provides males with information on a female's mating status. Although there appears to be large variation among species regarding the mechanisms by which female odour is altered post‐mating, the transfer of male substances to females during or subsequent to copulation appear to play a major role. This transfer of substances by males may be part of their strategy to suppress reproduction by competing males, particularly in species where females mate more than once.     

Variation and repeatability of ultrasonic sexual advertisement signals inAchroia grisella (Lepidoptera: Pyralidae)

MaleAchroia grisella (Lepidoptera: Pyralidae) produce ultrasonic advertisement signals for pair formation. The signals are generated by wing-fanning and consist of pairs of approximately 100-μs pulses of 70- to 130-kHz sound. In a previous study, playback experiments showed that femaleA. grisella preferred signals whose pulses were louder, longer, and delivered at a higher rate and included longer silent (asynchrony) intervals within pairs. To understand the variation and repeatability of these signal characters, acoustic signals of 18A. grisella males were recorded twice daily on the first 4 days and the seventh day after adult eclosion. ANOVA and MANOVA revealed significant among-individual and among-age variation for all signal characters. Peak amplitude, average amplitude, rate, and pulse length peaked 2–3 days after eclosion and then decreased. Asynchrony interval, however, continued to increase as males aged. Repeatabilities of peak amplitude, average amplitude, rate, and asynchrony interval were all relatively high (>0.5).     

Experimental stress during molt suggests the evolution of condition‐dependent and condition‐independent ornaments in the king penguin

Sexual selection and social selection are two important theories proposed for explaining the evolution of colorful ornamental traits in animals. Understanding signal honesty requires studying how environmental and physiological factors during development influence the showy nature of sexual and social ornaments. We experimentally manipulated physiological stress and immunity status during the molt in adult king penguins (Aptenodytes patagonicus), and studied the consequences of our treatments on colourful ornaments (yellow‐orange and UV beak spots and yellow‐orange auricular feather patches) known to be used in sexual and social contexts in this species. Whereas some ornamental features showed strong condition‐dependence (yellow auricular feather chroma, yellow and UV chroma of the beak), others were condition‐independent and remained highly correlated before and after the molt (auricular patch size and beak UV hue). Our study provides a rare examination of the links between ornament determinism and selection processes in the wild. We highlight the coexistence of ornaments costly to produce that may be honest signals used in mate choice, and ornaments for which honesty may be enforced by social mediation or rely on genetic constraints.     

Sexual dimorphism in conspicuousness and ornamentation in the enigmatic leaf‐nosed lizard Ceratophora tennentii from Sri Lanka

Measures of physiological performance capacity, such as bite force, form the functional basis of sexual selection. Information about fighting ability may be conveyed through a structural feature such as a rostrum (i.e. horn) or a colour signal and thereby help reduce costly conflict. We quantified sexual dimorphism in key traits likely to be the targets of sexual selection in Tennent's leaf‐nosed lizard (Ceratophora tennentii) from Sri Lanka, and examined their relationship to bite force and body condition. We found body length and bite force to be similar for males and females. However, head length was significantly greater in males and they had significantly more conspicuous throats and labials (chromatic contrast and luminance) than females. Males also had a proportionally larger rostrum, which we predicted could be an important source of information about male quality for both sexes. Rostrum length was correlated with throat chromatic contrast in males but not females. Nonetheless, the rostrum and aspects of coloration did not correlate with bite force or body condition as we predicted. We have no information on contest escalation in this species but if they rarely bite, as suggested by a lack of difference in bite force between males and females, then bite force and any associated signals would not be a target of selection. Finally, males and females had similar spectral reflectance of the mouth and tongue and both had a peak in the ultra‐violet, and were conspicuous to birds. Lizards only gaped their mouths during capture and not when threatened by a potential predator (hand waving). We hypothesize that conspicuous mouth colour may act as a deimatic signal, startling a potential predator, although this will need careful experimental testing in the future.     

Sprint speed is not reduced by exaggerated male weapons in a flower beetle Dicronocephalus wallichii

Exaggerated sexually selected traits are assumed to decrease the mobility of bearers. However, previous empirical studies have often failed to support this assumption, possibly because locomotor performance represents the integration of numerous morphological, physiological and behavioural traits. Males of a flower beetle Dicronocephalus wallichii Pouillaude 1914 (Coleoptera: Scarabaeidae: Cetoniinae) possess elongated forelegs and a pair of exaggerated horns, which are used as dual weapons in male–male competition for mates. We investigated whether these two sexual traits impede the maximum sprint speed on bamboo branches with different angles and thicknesses under laboratory conditions. Our results suggested that no negative relationship exists between relative foreleg length or horn length and sprint speed. Elongated forelegs and horns may entail negligible locomotor costs. Males with longer horns and forelegs were found to have longer midlegs and hindlegs independent of body size. Thus, elongated midlegs and hindlegs in males may enhance balance, stabilize running on bamboo branches and compensate for the locomotor costs of bearing exaggerated weapons. Furthermore, a positive relationship was found between horn length and sprint speed on a horizontal branch. Males with longer horns probably have more energy and/or invest more heavily in appendage musculature. As is known in other animals, male horns of D. wallichii may act as honest indicators of body condition.