More to legs than meets the eye: Presence and function of pheromone compounds on heliothine moth legs

Chemical communication is ubiquitous in nature and chemical signals convey species-specific messages. Despite their specificity, chemical signals may not be limited to only one function. Identifying alternative functions of chemical signals is key to understanding how chemical communication systems evolve. Here, we explored alternative functions of moth sex pheromone compounds. These chemicals are generally produced in, and emitted from, dedicated sex pheromone glands, but some have recently also been found on the insects' legs. We identified and quantified the chemicals in leg extracts of the three heliothine moth species Chloridea (Heliothis) virescens, Chloridea (Heliothis) subflexa and Helicoverpa armigera, compared their chemical profiles and explored the biological function of pheromone compounds on moth legs. Identical pheromone compounds were present on the legs in both sexes of all three species, with no striking interspecies or intersex differences. Surprisingly, we also found pheromone-related acetate esters in leg extracts of species that lack acetate esters in their female sex pheromone. When we assessed gene expression levels in the leg tissue, we found known and putative pheromone-biosynthesis genes expressed, which suggests that moth legs may be additional sites of pheromone production. To determine possible additional roles of the pheromone compounds on legs, we explored whether these may act as oviposition-deterring signals, which does not seem to be the case. However, when we tested whether these chemicals have antimicrobial properties, we found that two pheromone compounds (16:Ald and 16:OH) reduce bacterial growth. Such an additional function of previously identified pheromone compounds likely coincides with additional selection pressures and, thus, should be considered in scenarios on the evolution of these signals.     

Distinguishing signals and cues: bumblebees use general footprints to generate adaptive behaviour at flowers and nest

Chemicals used in communication are divided into signals and cues. Signals are moulded by natural selection to carry specific meanings in specific contexts. Cues, on the other hand, have not been moulded by natural selection to carry specific information for intended receivers. Distinguishing between these two modes of information transfer is difficult when animals do not perform obvious secretion behaviours. Although a number of insects have been suspected of leaving cues at food sites and nest entrances, studies have not attempted to experimentally distinguish between cues and signals. Here, we examine the chemical composition of the scent marks left by the bumblebee Bombus terrestris at food sites and compare it to those found at a neutral location. If bees are depositing a cue, we expect the same chemicals to be found at both sites, but if they deposit a signal we only expect to find the scent marks at the food site. We were also interested in identifying the chemicals left at the nest entrance to determine if they differed from those used to mark food sites. We find that bees deposit the same chemicals at food, nest and neutral sites. Therefore, bumblebees leave behind general chemical footprints everywhere they walk and we propose that they learn to use these footprints in a manner that ultimately enhances their fitness, for example, to improve their foraging efficiency and locate their nest. Experimentally, distinguishing these two modes of information transfer is crucial for understanding how they interact to shape animal behaviour and what chemical bouquets are under natural selection. Handling Editor: Heikki Hokkanen     

Heterogeneous tempo and mode of evolutionary diversification of compounds in lizard chemical signals

Important part of the multivariate selection shaping social and interspecific interactions among and within animal species emerges from communication. Therefore, understanding the diversification of signals for animal communication is a central endeavor in evolutionary biology. Over the last decade, the rapid development of phylogenetic approaches has promoted a stream of studies investigating evolution of communication signals. However, comparative research has primarily focused on visual and acoustic signals, while the evolution of chemical signals remains largely unstudied. An increasing interest in understanding the evolution of chemical communication has been inspired by the realization that chemical signals underlie some of the major interaction channels in a wide range of organisms. In lizards, in particular, chemosignals play paramount roles in female choice and male–male competition, and during community assembly and speciation. Here, using phylogenetic macro‐evolutionary modeling, we show for the very first time that multiple compounds of scents for communication in lizards have diversified following highly different evolutionary speeds and trajectories. Our results suggest that cholesterol, α‐tocopherol, and cholesta‐5,7‐dien‐3‐ol have been subject to stabilizing selection (Ornstein–Uhlenbeck model), whereas the remaining compounds are better described by Brownian motion modes of evolution. Additionally, the diversification of the individual compounds has accumulated substantial relative disparity over time. Thus, our study reveals that the chemical components of lizard chemosignals have proliferated across different species following compound‐specific directions.     

Investment in attending to cues and the evolution of amplifiers

Signals and cues are extensively used in social interactions across diverse communication systems. Here, we extend an existing theoretical framework to explore investment by emitters and perceivers in the fidelity with which cues and signals associated with the former are detected by the latter. Traits of the emitter that improve cue or signal fidelity without adding information are termed ‘amplifiers’. We assume that each party can invest in improving fidelity but that it is increasingly costly the more fidelity is improved. Our model predicts that evolution of amplifier traits of a pre‐existing cue occurs over a broader range of circumstances than evolution of signalling in situations where the emitter offered no pre‐existing cue to the perceiver. It further predicts that the greater the intrinsic informational value of a cue, the more likely it is that the perceiver (and not the emitter) will invest in the fidelity of detecting that cue. A consequence of this predicted asymmetry is that true communication with reciprocal adaptations in emitters and perceivers to improve signal fidelity is likely to occur predominantly for traits of intermediate reliability. The corollary is that uncertainty of the perceiver will then be a key feature of communication. Uncertainty can arise because perceivers misinterpret signals or do not perceive them correctly, but here we argue that uncertainty is more fundamentally at the root of communication because traits that are intrinsically highly informative will induce only the perceiver and not the emitter to invest in improved fidelity of perception of that trait.     

Volatile communication among sagebrush branches affects herbivory: timing of active cues

Airborne communication can affect systemic induced resistance to herbivory on neighboring branches and individual plants. Sagebrush is the best known example of this phenomenon although the mechanisms of this communication system remain unidentified. We do not know the timing of emission or the chemical nature of the active cue. We investigated the timing of this phenomenon by using plastic bags to prevent propagation of volatile compounds and experimentally manipulated the timing of removal of these bags. We found that blocking the volatiles prevented systemic induced resistance. Experimentally allowing clipped branches to release cues for up to 3 days after clipping caused a reduction in damage in neighboring branches on the clipped plants. This indicates that active cues are released from the time we clipped for the next 3 days or that cues released immediately remained active over this time period. As we continue to evaluate potential chemicals as active cues in plant communication, this prolonged effectiveness may provide an important screen against which to evaluate any putative signals. Handling editor: Robert Glinwood     

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.     

Wax,sex and the origin of species: Dual roles of insect cuticular hydrocarbons in adaptation and mating

Evolutionary changes in traits that affect both ecological divergence and mating signals could lead to reproductive isolation and the formation of new species. Insect cuticular hydrocarbons (CHCs) are potential examples of such dual traits. They form a waxy layer on the cuticle of the insect to maintain water balance and prevent desiccation, while also acting as signaling molecules in mate recognition and chemical communication. Because the synthesis of these hydrocarbons in insect oenocytes occurs through a common biochemical pathway, natural or sexual selection on one role may affect the other. In this review, we explore how ecological divergence in insect CHCs can lead to divergence in mating signals and reproductive isolation. We suggest that the evolution of insect CHCs may be ripe models for understanding ecological speciation.     

Your attention please: increasing ambient noise levels elicits a change in communication behaviour in humpback whales (Megaptera novaeangliae)

High background noise is an important obstacle in successful signal detection and perception of an intended acoustic signal. To overcome this problem, many animals modify their acoustic signal by increasing the repetition rate, duration, amplitude or frequency range of the signal. An alternative method to ensure successful signal reception, yet to be tested in animals, involves the use of two different types of signal, where one signal type may enhance the other in periods of high background noise. Humpback whale communication signals comprise two different types: vocal signals, and surface-generated signals such as ‘breaching’ or ‘pectoral slapping’. We found that humpback whales gradually switched from primarily vocal to primarily surface-generated communication in increasing wind speeds and background noise levels, though kept both signal types in their repertoire. Vocal signals have the advantage of having higher information content but may have the disadvantage of loosing this information in a noisy environment. Surface-generated sounds have energy distributed over a greater frequency range and may be less likely to become confused in periods of high wind-generated noise but have less information content when compared with vocal sounds. Therefore, surface-generated sounds may improve detection or enhance the perception of vocal signals in a noisy environment.     

The evolutionary stability of attenuators that mask information about animals that social partners can exploit

Signals and cues are fundamental to social interactions. A well‐established concept in the study of animal communication is an amplifier, defined as a trait that does not add extra information to that already present in the original cue or signal, but rather enhances the fidelity with which variation in the original cue or signal is correctly perceived. Attenuators as the logical compliment of amplifiers: attenuators act to reduce the fidelity with which variation in a signal or cue can be reliably evaluated by the perceivers. Where amplifiers reduce the effect of noise on the perception of variation, attenuators add noise. Attenuators have been subject to much less consideration than amplifiers; however, they will be the focus of our theoretical study. We utilize an extension of a well‐established model incorporated signal or cue inaccuracy and costly investments by emitter and perceiver in sending and attending to the signal or cue. We present broad conditions involving some conflict of interest between emitter and perceiver where it may be advantageous for emitters to invest in costly attenuators to mask cues from potential perceivers, and a subset of these conditions where the perceiver may be willing to invest in costly anti‐attenuators to mitigate the loss of information to them. We demonstrate that attenuators can be evolutionary stable even if they are costly, even if they are sometimes disadvantageous and even if a perceiver can mount counter‐measures to them. As such, we feel that attenuators of cues may be deserving of much more research attention.     

Macroevolution of perfume signalling in orchid bees

Theory predicts that both stabilising selection and diversifying selection jointly contribute to the evolution of sexual signalling traits by (1) maintaining the integrity of communication signals within species and (2) promoting the diversification of traits among lineages. However, for many important signalling traits, little is known about whether these dynamics translate into predictable macroevolutionary signatures. Here, we test for macroevolutionary patterns consistent with sexual signalling theory in the perfume signals of neotropical orchid bees, a group well studied for their chemical sexual communication. Our results revealed both high species‐specificity and elevated rates of evolution in perfume signals compared to nonsignalling traits. Perfume complexity was correlated with the number of congeners in a species’ range, suggesting that perfume evolution may be tied to the remarkably high number of orchid bee species coexisting together in some neotropical communities. Finally, sister‐pair comparisons were consistent with both rapid divergence at speciation and character displacement upon secondary contact. Together, our results provide new insight into the macroevolution of sexual signalling in insects.     

Molecular diagnostics reveal spiders that exploit prey vibrational signals used in sexual communication

Vibrational signalling is a widespread form of animal communication and, in the form of sexual communication, has been generally regarded as inherently short‐range and a private communication channel, free from eavesdropping by generalist predators. A combination of fieldwork and laboratory experiments was used to test the hypothesis that predators can intercept and exploit such signals. First, we developed and characterized PCR primers specific for leafhoppers of the genus Aphrodes and specifically for the species Aphrodes makarovi. Spiders were collected from sites where leafhoppers were present and screened with these primers to establish which spider species were significant predators of this species during the mating period of these leafhoppers. Analysis using PCR of the gut contents of tangle‐web spiders, Enoplognatha ovata (Theridiidae), showed that they consume leafhoppers in the field at a greater rate when signalling adults were present than when nymphs were dominant, suggesting that the spiders were using these vibrations signals to find their prey. Playback and microcosm experiments then showed that E. ovata can use the vibrational signals of male leafhoppers as a cue during foraging and, as a result, killed significantly more male than female A. makarovi. Our results show, for the first time, that arthropod predators can exploit prey vibrational communication to obtain information about prey availability and use this information to locate and capture prey. This may be a widespread mechanism for prey location, one that is likely to be a major unrecognized driver of evolution in both predators and prey.     

Signalling of information that is neither cryptic nor private

It is commonly assumed that in order for animal signals to be advantageous, the information being signalled could not have been obtained otherwise, and is therefore ‘cryptic’ or ‘private’. Here, we suggest a scenario in which individuals can gain an advantage by signalling ‘public’ information that is neither cryptic nor private. In that scenario, signalling increases the efficiency with which that ‘public’ information is transmitted. We formalize our idea with a game in which offspring can signal their condition to their parents. Specifically, we consider a resource‐strapped parent who can only invest in one of its two offspring, and we allow offspring the chance to influence parental investment through a signal. A parent in the game seeks to invest in the higher‐quality offspring, which it could identify either through a publicly available cue, such as body size, or by relying on a signal provided by the offspring. We find that if the signal can convey information about offspring quality more efficiently than cues, then signalling of condition between offspring and parents can be favoured by selection, even though parents could potentially have acquired the same information from the cue. Our results suggest that the biological function of signals may be broader than currently considered, and provide a scenario where low cost signalling can be favoured. More generally, efficiency benefits could explain signalling across a range of biological and economic scenarios.     

Eavesdropping on visual secrets

Private communication may benefit signalers by reducing the costs imposed by potential eavesdroppers such as parasites, predators, prey, or rivals. It is likely that private communication channels are influenced by the evolution of signalers, intended receivers, and potential eavesdroppers, but most studies only examine how private communication benefits signalers. Here, we address this shortcoming by examining visual private communication from a potential eavesdropper’s perspective. Specifically, we ask if a signaler would face fitness consequences if a potential eavesdropper could detect its signal more clearly. By integrating studies on private communication with those on the evolution of vision, we suggest that published studies find few taxon-based constraints that could keep potential eavesdroppers from detecting most hypothesized forms of visual private communication. However, we find that private signals may persist over evolutionary time if the benefits of detecting a particular signal do not outweigh the functional costs a potential eavesdropper would suffer from evolving the ability to detect it. We also suggest that all undetectable signals are not necessarily private signals: potential eavesdroppers may not benefit from detecting a signal if it co-occurs with signals in other more detectable sensory modalities. In future work, we suggest that researchers consider how the evolution of potential eavesdroppers’ sensory systems influences private communication. Specifically, we suggest that examining the fitness correlates and evolution of potential eavesdroppers can help (1) determine the likelihood that private communication channels are stable over evolutionary time, and (2) demonstrate that undetectable signals are private signals by showing that signalers benefit from a reduction in detection by potential eavesdroppers.     

Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response

In spite of the importance of chemoreception in sexual selection of lizards, only a few studies have examined the composition of chemical signals, and it is unknown whether and how chemicals provide honest information. Chemical signals might be honest if there were a trade-off between sexual advertisement and the immune system. Here, we show that proportions of cholesta-5,7-dien-3-ol in femoral secretions of male Iberian wall lizards (Podarcis hispanica) were related to their T-cell-mediated immune response. Thus, only males with a good immune system may allocate higher amounts of this chemical to signalling. Furthermore, females selected scents of males with higher proportions of cholesta-5,7-dien-3-ol and lower proportions of cholesterol. Thus, females might base their mate choice on the males' quality as indicated by the composition of their chemical signals.     

Enhanced growth at low population density in Daphnia: the absence of crowding effects or relief from visual predation?

1. It has been suggested that chemical information from crowded populations of an animal such as Daphnia carries a cue indicating imminent food limitation, and we suggest that in the presence of fish kairomones, it may also convey a hint of the need to enhance antipredation defences. 2. We performed two‐factorial experiments with Daphnia grown in flow‐through plankton chambers in medium containing high levels of Scenedesmus food plus chemical information on either low or high population density levels and in the presence or absence of fish chemical cues (kairomones) and recorded (i) the effects on Daphnia growth rate and reproduction, and (ii) the effects on Daphnia depth selection. Further depth‐selection experiments were performed to test the reaction of Daphnia to crowding information at different Daphnia concentrations and to test its effect on daytime and night‐time depth selection by different Daphnia instars in the presence of kairomones. 3. The effects of crowding information alone (in the absence of kairomones) were weak and were not significantly strengthened by the addition of kairomones. The effects of kairomones alone (in the absence of crowding information) were much stronger and were increased by the presence of crowding chemicals: Daphnia selected greater depths in daylight (the later the instar and the larger its body size, the greater the depth), their body growth was slower and daily reproductive investment reduced, compared with Daphnia grown in the absence of crowding information. This suggested that crowding chemicals carry a cue indicating the need to invest more into antipredation defences. 4. The adaptive significance of these effects was confirmed by the differential vulnerability to predation of the Daphnia when offered as prey to live roach after being grown for 6 days either in the presence (higher vulnerability) or in the absence (lower vulnerability) of information on high density. 5. The strong interaction between crowding information and fish kairomones may be explained either as the reaction to a cue indicating impending food stress or as the reaction to a signal of increased predation risk. While the former scenario is already known from crowding studies, the latter is a novel idea that stems from the old concept of ‘low‐density anti‐predation refuge’. The two scenarios are not mutually exclusive: each stems from the need to invest in survival rather than in growth and reproduction [Corrections were made to this paragraph after first online publication on 4 April 2012].     

Reproductive behaviour and vibratory communication of the neotropical predatory stink bug Podisus nigrispinus

Vibratory communication during reproductive behaviour is less well described in predatory (Asopinae) than in phytophagous (Pentatominae) stink bugs. Different steps in the mating behaviour of the predatory stink bug Podisus nigrispinus (Dallas) (Hemiptera: Pentatomidae; Asopinae) are described in the present study, together with vibratory signals emitted on artificial and natural substrate during courtship and copulation. Vibratory signals in Podisus nigrispinus have a decisive role in copulation success and are produced in both sexes by abdominal vibration and tremulation. In P. nigrispinus, one species‐specific female and two male songs, which do not show the calling function typically found in phytophagous stink bugs, are produced by abdominal vibration and are emitted during reproductive behaviour. Additionally, P. nigrispinus produces tremulatory signals that have no species or sex specificity. Tremulatory signals emitted spontaneously on a plant as a sequence of readily repeated pulses are similar to the calling songs of the Pentatominae stink bug. These signals may carry information on the presence of a mate; however, in other behavioural contexts, they may have a different function, such as advertisement or even alarm signals. Plants transmit vibratory signals produced by both mechanisms as a low‐pass filter, increasing the amount of low‐frequency components. The results of the present study raise important questions about the interaction between chemical and vibratory signals in the mating behaviour of predatory stink bugs.     

Nonlinear acoustic complexity in a fish 'two-voice' system

Acoustic signals play essential roles in social communication and show a strong selection for novel morphologies leading to increased call complexity in many taxa. Among vertebrates, repeated innovations in the larynges of frogs and mammals and the syrinx of songbirds have enhanced the spectro-temporal content, and hence the diversity of vocalizations. This acoustic diversification includes nonlinear characteristics that expand frequency profiles beyond the traditional categorization of harmonic and broadband calls. Fishes have remained a notable exception to evidence for such acoustic innovations among vertebrates, despite their being the largest group of living vertebrates that also exhibit widespread evolution of sound production. Here, we combine rigorous acoustic and mathematical analyses with experimental silencing of the vocal motor system to show how a novel swim bladder mechanism in a toadfish enables it to generate calls exhibiting nonlinearities like those found among frogs, birds and mammals, including primates. By showing that fishes have evolved nonlinear acoustic signalling like all other major lineages of vocal vertebrates, these results suggest strong selection pressure favouring this mechanism to enrich the spectro-temporal content and complexity of vocal signals.     

植物化学通讯研究进展

 生物的信息传递是生命科学中引人入胜的研究领域之一,生物种间种内和个体内都存在着物理和化学等各种信息交流方式。植物种间种内是否通过物理信号进行通讯交流还是一个未知数,但邻近的同种或异种植物通过化学物质为媒介的通讯关系确是客观存在的。最近,愈来愈多的研究证明：许多陆生植物种可以合成并释放特定的次生物质,这些次生物质可以通过空气和土壤两种载体进行信息传递,尤其是在植物受到侵袭和寄生条件下。茉莉酮酸甲酯、水杨酸甲酯和乙烯等挥发性次生物质被确证为以空气为媒介进行植物种间和种内通讯的化学信号分子。植物根分泌的黄酮和氢醌等分子也可以经土壤媒介传递信息。由于在自然条件下植物根系分泌物的收集和活性信号分子的俘获及鉴定技术还未能突破,这增加了以土壤为媒介的植物种间和种内化学通讯关系研究的难度。但不论如何,植物的化学通讯是植物种间和种内交流的主要方式,植物间的化学通讯关系的研究还处于突破的前夜,这方面的任一研究成果都会引起世界性的关注。因此,破译植物种间和种内化学通讯密码具有重要的学术价值。     

Putting information back into biological communication

At the heart of many debates on communication is the concept of information. There is an intuitive sense in which communication implies the transfer of some kind of information, probably the reason why information is an essential ingredient in most definitions of communication. However, information has also been an endless source of misunderstandings, and recent accounts have proposed that information should be dropped from a formal definition of communication. In this article, we re‐evaluate the merits and the internal logic of information‐based vs. information‐free approaches and conclude that information‐free approaches are conceptually incomplete and operationally hindered. Instead, we propose a functional notion of information that follows logically from previous adaptationist accounts. The ensuing definition of communication provides a wider, more inclusive theoretical scope that reflects more accurately the evolutionary scenario shaping animal signals. Additionally, it is a definition better equipped to deal with the extraordinary diversity of animal signals, facilitates the distinction of honest and deceptive signals at a proximate level and accommodates a number of conceptual and practical issues (e.g. redundancy, alerting components) that are lost when we fail to acknowledge the informative content of animal signals.     

Platyrrhine color signals: New horizons to pursue

Like catarrhines, some platyrrhines show exposed and reddish skin, raising the possibility that reddish signals have evolved convergently. This variation in skin exposure and color combined with sex‐linked polymorphic color vision in platyrrhines presents a unique, and yet underexplored, opportunity to investigate the relative importance of chromatic versus achromatic signals, the influence of color perception on signal evolution, and to understand primate communication broadly. By coding the facial skin exposure and color of 96 platyrrhines, 28 catarrhines, 7 strepsirrhines, 1 tarsiiform, and 13 nonprimates, and by simulating the ancestral character states for these traits, we provide the first analysis of the distribution and evolution of facial skin exposure and color in platyrrhini. We highlight ways in which studying the presence and use of color signals by platyrrhines and other primates will enhance our understanding of the evolution of color signals, and the forces shaping color vision.