Coordinated rhythms in animal species, including humans: Entrainment from bushcricket chorusing to the philharmonic orchestra.

Coordinated group displays featuring precise entrainment of rhythmic behavior between neighbors occur not only in human music, dance and drill, but in the acoustic or optical signaling of a number of species of arthropods and anurans. In this review we describe the mechanisms of phase resetting and phase and tempo adjustments that allow the periodic output of signaling individuals to be aligned in synchronized rhythmic group displays. These mechanisms are well described in some of the synchronizing arthropod species, in which conspecific signals reset an individual's endogenous output oscillators in such a way that the joint rhythmic signals are locked in phase. Some of these species are capable of mutually adjusting both the phase and tempo of their rhythmic signaling, thereby achieving what is called perfect synchrony, a capacity which otherwise is found only in humans. We discuss this disjoint phylogenetic distribution of inter-individual rhythmic entrainment in the context of the functions such entrainment might perform in the various species concerned, and the adaptive circumstances in which it might evolve.

Synchrony and rhythm interaction: from the brain to behavioural ecology.

This theme issue assembles current studies that ask how and why precise synchronization and related forms of rhythm interaction are expressed in a wide range of behaviour. The studies cover human activity, with an emphasis on music, and social behaviour, reproduction and communication in non-human animals. In most cases, the temporally aligned rhythms have short-from several seconds down to a fraction of a second-periods and are regulated by central nervous system pacemakers, but interactions involving rhythms that are 24 h or longer and originate in biological clocks also occur. Across this spectrum of activities, species and time scales, empirical work and modelling suggest that synchrony arises from a limited number of coupled-oscillator mechanisms with which individuals mutually entrain. Phylogenetic distribution of these common mechanisms points towards convergent evolution. Studies of animal communication indicate that many synchronous interactions between the signals of neighbouring individuals are specifically favoured by selection. However, synchronous displays are often emergent properties of entrainment between signalling individuals, and in some situations, the very signallers who produce a display might not gain any benefit from the collective timing of their production. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Rhythm interaction in animal groups: selective attention in communication networks.

Animals communicating interactively with conspecifics often time their broadcasts to avoid overlapping interference, to emit leading, as opposed to following, signals or to synchronize their signalling rhythms. Each of these adjustments becomes more difficult as the number of interactants increases beyond a pair. Among acoustic species, insects and anurans generally deal with the problem of group signalling by means of 'selective attention' in which they focus on several close or conspicuous neighbours and ignore the rest. In these animals, where signalling and receiving are often dictated by sex, the process of selective attention in signallers may have a parallel counterpart in receivers, which also focus on close neighbours. In birds and mammals, local groups tend to be extended families or clans, and group signalling may entail complex timing mechanisms that allow for attention to all individuals. In general, the mechanisms that allow animals to communicate in groups appear to be fully interwoven with the basic process of rhythmic signalling. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Interactive rhythms across species: the evolutionary biology of animal chorusing and turn-taking.

The study of human language is progressively moving toward comparative and interactive frameworks, extending the concept of turn-taking to animal communication. While such an endeavor will help us understand the interactive origins of language, any theoretical account for cross-species turn-taking should consider three key points. First, animal turn-taking must incorporate biological studies on animal chorusing, namely how different species coordinate their signals over time. Second, while concepts employed in human communication and turn-taking, such as intentionality, are still debated in animal behavior, lower level mechanisms with clear neurobiological bases can explain much of animal interactive behavior. Third, social behavior, interactivity, and cooperation can be orthogonal, and the alternation of animal signals need not be cooperative. Considering turn-taking a subset of chorusing in the rhythmic dimension may avoid overinterpretation and enhance the comparability of future empirical work.

Quantitative Genetic Mapping and Genome Assembly in the Lesser Wax Moth Achroia grisella.

Specific characteristics of the male Achroia grisella acoustic mating signal determine a male's attractiveness toward females. These features are genetically variable in populations, and mapping experiments have been used to identify loci contributing to song variation, and understand the evolutionary forces acting on this important sexual trait. Here we built on this foundation and carried out QTL (Quantitative Trait Locus) mapping using >1,000 recombinant individuals, genotyping this large cohort at thousands of sequence-based markers covering the entire collection of 30 A. grisella chromosomes. This dense marker set, coupled with our development of an annotated, draft genome of A. grisella, allowed us to link >3,000 genome scaffolds, >10,000 predicted genes, and close to 275Mb of genome sequence to chromosomes. Our QTL mapping confirmed a fraction of the QTL identified in a previous study, and additionally revealed novel loci. Collectively, QTL explained only small fractions of the phenotypic variance, suggesting many more causative factors remain below the detection threshold of our study. A surprising, and ultimately challenging feature of our study was the low level of intrachromosomal recombination present in our mapping population. This led to difficulty ordering markers along linkage groups, necessitating a chromosome-by-chromosome mapping approach, rather than true interval mapping, and precluded confident ordering/orienting of scaffolds along each chromosome. Nonetheless, our study increased the genomic resources available for the A. grisella system. Enabled by ever more powerful technologies, future investigators will be able to leverage our data to provide more detailed genetic dissection of male song variation in A. grisella.

Evolution of directional hearing in moths via conversion of bat detection devices to asymmetric pressure gradient receivers.

Small animals typically localize sound sources by means of complex internal connections and baffles that effectively increase time or intensity differences between the two ears. However, some miniature acoustic species achieve directional hearing without such devices, indicating that other mechanisms have evolved. Using 3D laser vibrometry to measure tympanum deflection, we show that female lesser waxmoths (Achroia grisella) can orient toward the 100-kHz male song, because each ear functions independently as an asymmetric pressure gradient receiver that responds sharply to high-frequency sound arriving from an azimuth angle 30° contralateral to the animal's midline. We found that females presented with a song stimulus while running on a locomotion compensation sphere follow a trajectory 20°-40° to the left or right of the stimulus heading but not directly toward it, movement consistent with the tympanum deflections and suggestive of a monaural mechanism of auditory tracking. Moreover, females losing their track typically regain it by auditory scanning-sudden, wide deviations in their heading-and females initially facing away from the stimulus quickly change their general heading toward it, orientation indicating superior ability to resolve the front-rear ambiguity in source location. X-ray computer-aided tomography (CT) scans of the moths did not reveal any internal coupling between the two ears, confirming that an acoustic insect can localize a sound source based solely on the distinct features of each ear.

Animal choruses emerge from receiver psychology.

Synchrony and alternation in large animal choruses are often viewed as adaptations by which cooperating males increase their attractiveness to females or evade predators. Alternatively, these seemingly composed productions may simply emerge by default from the receiver psychology of mate choice. This second, emergent property hypothesis has been inferred from findings that females in various acoustic species ignore male calls that follow a neighbor's by a brief interval, that males often adjust the timing of their call rhythm and reduce the incidence of ineffective, following calls, and from simulations modeling the collective outcome of male adjustments. However, the purported connection between male song timing and female preference has never been tested experimentally, and the emergent property hypothesis has remained speculative. Studying a distinctive katydid species genetically structured as isolated populations, we conducted a comparative phylogenetic analysis of the correlation between male call timing and female preference. We report that across 17 sampled populations male adjustments match the interval over which females prefer leading calls; moreover, this correlation holds after correction for phylogenetic signal. Our study is the first demonstration that male adjustments coevolved with female preferences and thereby confirms the critical link in the emergent property model of chorus evolution.

Development of a Genomic Resource and Quantitative Trait Loci Mapping of Male Calling Traits in the Lesser Wax Moth, Achroia grisella.

In the study of sexual selection among insects, the Lesser Waxmoth, Achroia grisella (Lepidoptera: Pyralidae), has been one of the more intensively studied species over the past 20 years. Studies have focused on how the male calling song functions in pair formation and on the quantitative genetics of male song characters and female preference for the song. Recent QTL studies have attempted to elucidate the genetic architecture of male song and female preference traits using AFLP markers. We continued these QTL studies using SNP markers derived from an EST library that allowed us to measure both DNA sequence variation and map loci with respect to the lepidopteran genome. We report that the level of sequence variation within A. grisella is typical among other Lepidoptera that have been examined, and that comparison with the Bombyx mori genome shows that macrosynteny is conserved. Our QTL map shows that a QTL for a male song trait, pulse-pair rate, is situated on the Z chromosome, a prediction for sexually selected traits in Lepidoptera. Our findings will be useful for future studies of genetic architecture of this model species and may help identify the genetics associated with the evolution of its novel acoustic communication.

Amino acid composition of the bushcricket spermatophore and the function of courtship feeding: Variable composition suggests a dynamic role of the nuptial gift.

Nuptial gifts are packages of non-gametic material transferred by males to females at mating. These gifts are common in bushcrickets, where males produce a complex spermatophore consisting in a sperm-containing ampulla and an edible sperm-free spermatophylax. Two non-mutually exclusive hypotheses have been suggested to explain the function of the spermatophylax: the paternal investment hypothesis proposes that it represents a male nutritional investment in offspring; the mating effort hypothesis proposes that the spermatophylax maximizes the male's sperm transfer. Because gift production may represent significant energy expenditure, males are expected to adjust their investment relative to the perceived quality of the female. In this study, we first examined the free amino acid composition and protein-bound amino acid composition of the nuptial gift in the bushcricket, Ephippiger diurnus (Orthoptera: Tettigoniidae). Second, we investigated whether this composition was altered according to female age and body weight. Our study represents the first investigation of both free and protein-bound amino acid fractions of a bushcricket spermatophylax. We found that composition of the nuptial gift varied both qualitatively and quantitatively with respect to traits of the receiving female: older females received larger amounts of protein-bound amino acids (both essential and non-essential), less water and less free glycine. This result suggests that gift composition is highly labile in E. diurnus, and we propose that gift allocation might represent a form of cryptic male mate choice, allowing males to maximize their chances of paternity according to the risk of sperm competition that is associated with mate quality.

Signal interactions and interference in insect choruses: singing and listening in the social environment.

Acoustic insects usually sing amidst conspecifics, thereby creating a social environment-the chorus-in which individuals communicate, find mates, and avoid predation. A temporal structure may arise in a chorus because of competitive and cooperative factors that favor certain signal interactions between neighbors. This temporal structure can generate significant acoustic interference among singers that pose problems for communication, mate finding, and predator detection. Acoustic insects can reduce interference by means of selective attention to only their nearest neighbors and by alternating calls with neighbors. Alternatively, they may synchronize, allowing them to preserve call rhythm and also to listen for predators during the silent intervals between calls. Moreover, males singing in choruses may benefit from reduced per capita predation risk as well as enhanced vigilance. They may also enjoy greater per capita attractiveness to females, particularly in the case of synchronous choruses. In many cases, however, the overall temporal structure of the chorus is only an emergent property of simple, pairwise interactions between neighbors. Nonetheless, the chorus that emerges can impose significant selection pressure on the singing of those individual males. Thus, feedback loops may occur and potentially influence traits at both individual and group levels in a chorus.

The dilemma of Fisherian sexual selection: mate choice for indirect benefits despite rarity and overall weakness of trait-preference genetic correlation.

Fisher's mechanism of sexual selection is a fundamental element of evolutionary theory. In it nonrandom mate choice causes a genetic covariance between a male trait and female preference for that trait and thereby generates a positive feedback process sustaining accelerated coevolution of the trait and preference. Numerous theoretical models of Fisher's mechanism have confirmed its mathematical underpinnings, yet biologists have often failed to find evidence for trait-preference genetic correlation in populations in which the mechanism was expected to function. We undertook a survey of the literature to conduct a formal meta-analysis probing the incidence and strength of trait-preference correlation among animal species. Our meta-analysis found significant positive genetic correlations in fewer than 20% of the species studied and an overall weighted correlation that is slightly positive. Importantly, a significant positive correlation was not found in any thorough study that included multiple subgroups. We discuss several ways in which the dynamic, multivariate nature of mate choice may reduce the trait-preference genetic correlation predicted by Fisher's mechanism. We then entertain the possibilities that Fisherian-like processes sometimes function without genetic correlation, and that mate choice may persist in a population as long as genetic correlation, and therefore Fisher's mechanism, occurs intermittently.

Genetic architecture of sexual selection: QTL mapping of male song and female receiver traits in an acoustic moth.

Models of indirect (genetic) benefits sexual selection predict linkage disequilibria between genes that influence male traits and female preferences, owing to non-random mate choice or physical linkage. Such linkage disequilibria can accelerate the evolution of traits and preferences to exaggerated levels. Both theory and recent empirical findings on species recognition suggest that such linkage disequilibria may result from physical linkage or pleiotropy, but very little work has addressed this possibility within the context of sexual selection. We studied the genetic architecture of sexually selected traits by analyzing signals and preferences in an acoustic moth, Achroia grisella, in which males attract females with a train of ultrasound pulses and females prefer loud songs and a fast pulse rhythm. Both male signal characters and female preferences are repeatable and heritable traits. Moreover, female choice is based largely on male song, while males do not appear to provide direct benefits at mating. Thus, some genetic correlation between song and preference traits is expected. We employed a standard crossing design between inbred lines and used AFLP markers to build a linkage map for this species and locate quantitative trait loci (QTL) that influence male song and female preference. Our analyses mostly revealed QTLs of moderate strength that influence various male signal and female receiver traits, but one QTL was found that exerts a major influence on the pulse-pair rate of male song, a critical trait in female attraction. However, we found no evidence of specific co-localization of QTLs influencing male signal and female receiver traits on the same linkage groups. This finding suggests that the sexual selection process would proceed at a modest rate in A. grisella and that evolution toward exaggerated character states may be tempered. We suggest that this equilibrium state may be more the norm than the exception among animal species.

Genotype × environment interaction, environmental heterogeneity and the lek paradox.

Substantial additive genetic variance (V(A)) often exists for male signalling traits in spite of the directional selection that female choice imposes. One solution to this problem, a conundrum generally termed the 'lek paradox', is that genotype × environment interaction (GEI) occurs and generates a 'crossover' of reaction norms in which no one genotype performs in a superior manner in all environments. Theoretical work indicates that such crossover can sustain genetic variance provided that either (i) spatial heterogeneity in environmental conditions combined with limited migration among populations or (ii) temporal heterogeneity in environmental conditions combined with occasional generation overlap is present. Whereas some recent studies have revealed the intersection of reaction norms for sexually selected traits in laboratory and in natural populations, associated information on environmental heterogeneity, migration and generation overlap has not been investigated. We studied this question in an acoustic pyralid moth, Achroia grisella, in which previous work indicated GEI and crossover of reaction norms for several parameters of the male song evaluated by females. We measured reaction norms for male song as expressed when development was completed under different environmental conditions in four neighbouring, yet isolated, populations during 1 year and in one of these populations during consecutive years. Crossover occurred for the various song parameters in the several populations, but we did not observe a higher incidence of crossover between genotypes taken from two different populations than from the same population. However, for several key song parameters, crossover between genotypes taken from two different years was higher than that between genotypes from the same year. We suggest that temporal heterogeneity in the form of varying selection could potentially conserve V(A) in A. grisella, but we also note other factors that might contribute.

Indirect genetic effects and the lek paradox: inter-genotypic competition may strengthen genotype x environment interactions and conserve genetic variance.

Understanding the evolutionary mechanisms that maintain genetic variation in natural populations is one of the fundamental goals of evolutionary biology. There is growing evidence that genotype-by-environment interaction (G x E) can maintain additive genetic variance (V (A)), but we lack information on the relative performance of genotypes under the competitive situations encountered in the field. Competing genotypes may influence each other, and this interaction is also subject to selection through indirect genetic effects (IGE). Here, we explore how genotypes perform when interacting and evaluate IGE in order to understand its influence on V (A) for sexually-selected traits in the lesser waxmoth, Achroia grisella. We found that inter-genotype differences and crossover interactions under joint rearing are equal to or greater than values when reared separately. A focal genotype exhibited different performances when jointly reared with various genotypes-suggesting that IGE may be responsible for the increased levels of crossover and differences in performance observed. We suggest that some genotypes are superior competitors for food acquisition in the larval stage, and that these differences influence the development and evolution of other genotypes through IGE. We reaffirm the role of G x E in maintaining V (A) and note the general importance of IGE in studies of evolutionary mechanisms.

Mechanisms and evolution of synchronous chorusing: emergent properties and adaptive functions in Neoconocephalus katydids (Orthoptera: Tettigoniidae).

Synchronous interactions arise in various animal species that rhythmically broadcast acoustic, vibratory, and visual signals. These interactions are characterized by a coincidence in both rate and phase of the rhythms of neighboring signalers. Theory predicts several ways in which synchronized rhythms may specifically benefit the interacting signalers. However, synchrony may also arise as an emergent property, a default phenomenon that is neither preferred by conspecific receivers evaluating the signals nor advantageous to the signalers themselves. Here, we examine several well-studied cases of acoustic synchrony in Neoconocephalus katydids (Orthoptera: Tettigoniidae), a New World genus wherein males broadcast loud advertisement songs. We report that call synchrony found in N. spiza and N. nebrascensis results from two rather different mechanisms of rhythm adjustment. Moreover, synchrony in the former species appears to represent an incidental byproduct of signal competition between evenly matched males, whereas in the latter species synchrony functions as a specific adaptation in which cooperating males ensure that critical call features can be perceived by females. We discuss the separate evolutionary trajectories that may have led to similar outcomes, synchronous chorusing by advertising males, in these closely related species.

Reaction norm variants for male calling song in populations of Achroia grisella (Lepidoptera: Pyralidae): toward a resolution of the lek paradox.

Significant additive genetic variance often occurs for male advertisement traits in spite of the directional selection imposed by female choice, a problem generally known in evolutionary biology as the lek paradox. One hypothesis, which has limited support from recent studies, for the resolution of this paradox is the role of genotype x environment interaction in which no one genotype exhibits the superior performance in all environments--a crossover of reaction norms. However, these studies have not characterized the actual variation of reaction norms present in natural populations, and the extent to which crossover maintains genetic variance remains unknown. Here, we present a study of genotype x environment interaction for the male calling song in populations of Achroia grisella (Lepidoptera: Pyralidae; lesser waxmoth). We report significant variance among reaction norms for male calling song in two North American populations of A. grisella as measured along temperature, food availability, and density gradients, and there is a relatively high incidence of crossover of the temperature reaction norms. This range of reaction norm variants and their crossover may reflect the co-occurrence of plastic and canalized genotypes, and we argue that the different responses of these variants along environmental gradients may contribute toward the maintenance of genetic variance for male song.

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.

Perception of conspecific female pheromone stimulates female calling in an arctiid moth, Utetheisa ornatrix.

Perception of the female sex pheromone in Utetheisa ornatrix (Lepidoptera: Arctiidae) is responsible for induction and adjustment of calling by females and the collective phenomenon termed "female pheromonal chorusing". We found five olfactory-active compounds in the U. ornatrix female gland. When females were exposed to the entire pheromone or to two of its (synthetically prepared) components, (Z,Z,Z)-3,6,9-eicosatriene and (Z,Z,Z)-3,6,9-heneicosatriene, they were more likely to call during a given night, begin calling earlier, and briefly increase signal frequency with which they extrude their abdomen, an observable indication of calling in this species. Some females even initiated calling during photophase when exposed to the pheromone components. In general, female U. ornatrix are more sensitive to the complete blend of pheromone than to its individual compounds. We also tested the hypotheses: 1) that abdominal extrusion per se increases the rate of pheromone release; and 2) that greater abdominal pumping rhythm increases pheromone release rate. Contrary to our expectations: 1) females did not respond more strongly to a pulsed pheromone stimulus than to the constant release of pheromone at the same average release rate; and 2) we did not find a relationship between the frequency of abdominal pumping and pheromone release rate. Possible explanations for these unexpected findings are discussed.

The contribution of tympanic transmission to fine temporal signal evaluation in an ultrasonic moth.

In lesser waxmoths Achroia grisella, pair formation and female mate choice involve very fine discrimination of male ultrasonic signals. Female A. grisella prefer male signals with longer pulses and longer ;asynchrony intervals', and evaluate differences in these characteristics in the range of 80-260 mus. The first step in the evaluation of these characteristics is the tympanic transmission of stimuli. We used laser vibrometry to describe the mode of vibration, frequency tuning and stimulus transmission of the tympana of A. grisella. The tympanic response consisted of a rotational mode of vibration, in which the anterior and posterior sections moved out of phase; the posterior section of the tympanum vibrated with all points moving in phase and maximum displacement at the attachment point of the scoloparium that contains the receptor cells. The tympana of A. grisella were tuned to high ultrasonic frequencies and had an estimated time constant (i.e. the limit to their temporal acuity) of about 20-50 mus. Pulse length and all but the shortest asynchrony interval were thus well resolved by the tympanum. We discuss implications for the evaluation of pulse length and asynchrony interval.