Modality interactions alter the shape of acoustic mate preference functions in gray treefrogs

Sexual selection takes place in complex environments where females evaluating male mating signals are confronted with stimuli from multiple sources and modalities. The pattern of expression of female preferences may be influenced by interactions between modalities, changing the shape of female preference functions, and thus ultimately altering the selective landscape acting on male signal evolution. We tested the hypothesis that the responses of female gray treefrogs, Hyla versicolor, to acoustic male advertisement calls are affected by interactions with visual stimuli. We measured preference functions for several call traits under two experimental conditions: unimodal (only acoustic signals presented), and multimodal (acoustic signals presented along with a video‐animated calling male). We found that females were more responsive to multimodal stimulus presentations and, compared to unimodal playbacks, had weaker preferences for temporal call characteristics. We compared the preference functions obtained in these two treatments to the distribution of male call characteristics to make inferences on the strength and direction of selection expected to act on male calls. Modality interactions have the potential to influence the course of signal evolution and thus are an important consideration in sexual selection studies.     

Temporal order and the evolution of complex acoustic signals

The evolution of complex signals may be favoured by hidden preferences or pre-existing sensory biases. Females of two species of grey treefrogs (Hyla chrysoscelis and Hyla versicolor) were tested with combinations of a conspecific advertisement call and acoustic appendages. Appendages consisted of aggressive calls and segments of advertisement calls from conspecific males and males of three other species and bursts of filtered noise. When a wide variety of these acoustic appendages followed the advertisement call, the resulting compound signal was often more attractive than the same advertisement call alone. When the same appendages led advertisement calls, however, the compound signal was never more attractive and sometimes less attractive. The order effect was especially strong in tests of H. versicolor in which advertisement-call duration was decreased. These results cannot be explained by a general pre-existing bias for extra stimulation per se. Rather, order and other effects may constrain the evolution and subsequent modification of complex and extravagant signals, examples of which have been reported for a wide range of taxa.     

Patterns of variability are consistent across signal types in the treefrog Dendropsophus ebraccatus

Animal signal characteristics vary at multiple levels, and this variation can be related to the selective forces acting on signal structure. However, the effectiveness of selection acting on any one signal type may depend on selective forces acting on the same characteristics in other signal types, particularly if the signals share a common physical production mechanism. In anurans, signal variability has been related to the potential for various forms of selection by female choice on the characteristics of male advertisement calls. The significance of variability in the characteristics of another vocalization type, the aggressive call, is less well understood. In the present stiudy, within‐ and between‐male variability was measured in several characteristics of both advertisement and aggressive calls in the treefrog Dendropsophus ebraccatus. Many characteristics of both call types were repeatable within males. Fine‐temporal and spectral characteristics generally had low variation within males, whereas gross‐temporal characteristics were more variable. Unexpectedly, there were strong correlations between both measures of variability and mean values of the call characteristics of advertisement and aggressive calls. Thus, despite potentially conflicting selection pressures acting on advertisement and aggressive calls, the characteristics of individuals' calls were consistent across these two signal types. The potential forces responsible for consistency across call types are discussed, including morphological constraints and behavioural syndromes that act across different signalling contexts. In general, it is argued that measurements of variability made across multiple signal types, as in the present study, can provide important insights into the evolution of signal structure in organisms with complex signal repertoires. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 131–145.     

A MULTIVARIATE ANALYSIS OF GENETIC VARIATION IN THE ADVERTISEMENT CALL OF THE GRAY TREEFROG,HYLA VERSICOLOR

Genetic variation in sexual displays is crucial for an evolutionary response to sexual selection, but can be eroded by strong selection. Identifying the magnitude and sources of additive genetic variance underlying sexually selected traits is thus an important issue in evolutionary biology. We conducted a quantitative genetics experiment with gray treefrogs (Hyla versicolor) to investigate genetic variances and covariances among features of the male advertisement call. Two energetically expensive traits showed significant genetic variation: call duration, expressed as number of pulses per call, and call rate, represented by its inverse, call period. These two properties also showed significant genetic covariance, consistent with an energetic constraint to call production. Combining the genetic variance–covariance matrix with previous estimates of directional sexual selection imposed by female preferences predicts a limited increase in call duration but no change in call rate despite significant selection on both traits. In addition to constraints imposed by the genetic covariance structure, an evolutionary response to sexual selection may also be limited by high energetic costs of long‐duration calls and by preferences that act most strongly against very short‐duration calls. Meanwhile, the persistence of these preferences could be explained by costs of mating with males with especially unattractive calls.     

FORMS OF CALL OVERLAP AND THEIR IMPACT ON ADVERTISEMENT CALL ATTRACTIVENESS TO FEMALES OF THE GRAY TREEFROG,HYLA VERSICOLOR

ABSTRACT

Male gray Lreefrogs, Hyla versicolor, advertise for females in choruses in which calls often overlap. Previous research has demonstrated that such acoustic interference among conspecifics can impair the ability of a male to attract a mate. However, the stimulus set used in those studies was quite limited. Here we performed single-speaker and two-speaker tests of phonotaxis with female Hyla versicolor to explore the impact of different degrees and forms of call overlap on the relative attractiveness of male signals. We found that: (1) overlapped calls are recognized as acceptable signals by females, although they are less attractive than calls that are not overlapped; (2) the relative phase of the overlapping calls matters. When calls were time-shifted by 50% of their pulse-period (180 degree offset), attractiveness of overlapped calls was reduced relative to non-overlapped calls as much as it would be by a reduction in intensity of about 12 dB SPL or a drop in call duration of between one third to one half. A 90 degree phase offset was equivalent to a 3 dB drop in SPL; (3) partial call overlap may not impair call attractiveness if one third or less of the call is overlapped; (4) if the ending portion of a call is overlapped it may impair attractiveness less than if previous segments of a call are obscured; (5) if most (three fourths or more) of a male's calls are free of interference, overlap of his remaining calls does not significantly impair his attractiveness.     

THE FUNCTION OF CALL ALTERNATION IN ANURAN AMPHIBIANS: A TEST OF THREE HYPOTHESES

Males of many species of anurans alternate calls with those of their neighbors in a chorus. This pattern of calling reduces signal interference and may: 1) facilitate intermale spacing because males can better gauge the intensity of neighbors' calls if these calls do not overlap with their own; 2) help preserve species-specific temporal information in calls required to attract females; and/or 3) make it easier for females to localize males in the chorus. I tested these hypotheses with three species that exhibit call alternation, Hyla crucifer, H. versicolor, and H. microcephala. Males of all three species gave more aggressive calls to high-intensity synthetic stimuli that alternated with their calls than to those that overlapped their calls. These results support the first hypothesis. Results of four-speaker female choice experiments using alternating and overlapping calls indicate that preservation of signal integrity also is important in H. versicolor and H. microcephala, species that have fine-scale temporal information in their calls. However, the third hypothesis was not supported; females failed to discriminate among alternating and overlapping calls if the problem of signal disruption was eliminated or irrelevant.     

Spatially-mediated call pattern recognition and the cocktail party problem in treefrog choruses: can call frequency differences help during signal overlap?

Male gray treefrogs, Hyla versicolor, advertise for mates in dense assemblages characterized by high levels of noise and acoustic clutter. In pairwise interactions, males alternate pulsatile advertisement calls and so reduce call overlap to levels below that expected by chance. However, in choruses consisting of more than two males, acoustic interference increases dramatically. Moreover, males do not seem to exhibit selective attention in a way that reduces call interference among nearest neighbours. Previous research has also demonstrated that although females discriminate strongly against overlapped calls, negative effects of call overlap can be attenuated by a large angular separation between signal sources. However, call stimuli employed were identical in spectrum and so this situation differs from that likely in nature. Based on studies of ‘auditory stream segregation’ with other taxa, we hypothesized that realistic differences in the frequencies of overlapping calls could improve the ability of females to discern critical call features during overlap of separated call sources. We found that, although, under some circumstances, differences in call frequency may help females distinguish among neighbouring males giving temporally proximate calls, naturalistic spectral differences do not seem to help females perceptually separate the overlapping calls of neighbouring conspecific males.     

Geographical variation in male advertisement calls and female preference of the wide‐ranging canyon treefrog,Hyla arenicolor

We surveyed the geographical variation in male advertisement calls of the wide‐ranging canyon treefrog, Hyla arenicolor, and found large call differences among geographically distant lineages that had been characterized by a recent phylogeographical study. To test whether these call differences were biologically relevant and could allow reproductive isolation of different lineages should they come into secondary contact, we assessed female preference in a lineage occurring in southern Utah and north‐western Arizona, USA. These females exhibited a strong preference for their own lineage's call type over the calls of two Mexican lineages, but not over the calls from the geographically nearest lineage. We also identified traits that female frogs probably use to discriminate between lineage‐specific advertisement calls. Our behavioural results, together with recent molecular estimates of phylogenetic relationships among lineages, will guide future work addressing the evolutionary forces that have led to this biologically significant variation in male sexual signals. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Inbreeding and courtship calling in the cricket Teleogryllus commodus

Male field crickets produce two acoustic signals for mating: advertisement calls and courtship calls. While the importance of advertisement calling in mate attraction is well understood, the function of courtship calling is less clear. Here, we tested if the courtship call of male crickets Teleogryllus commodus signals aspects of male quality by comparing the calls of inbred and outbred males. We examined the effect of one generation of full sibling mating on fine‐scale call structure, along with several life history traits. Inbreeding reduced nymph survival but had no significant effect on weight or development time. Inbreeding resulted in a small but significant change in two of the six call parameters measured. We then tested if inbreeding affects call trait combinations that are important to females by using the results of a previous selection analysis to compare the multivariate attractiveness of the calls of inbred and outbred males. There was no difference. We conclude that the courtship call of T. commodus is not a reliable signal of aspects of male quality that are affected by inbreeding (which generally reduces fitness‐enhancing traits). It might, however, signal components of male fitness that are not affected by changes in heterozygosity.     

Tight hormonal phenotypic integration ensures honesty of the electric signal of male and female Brachyhypopomus gauderio

Hormones mediate sexually selected traits including advertisement signals. Hormonal co-regulation links the signal to other hormonally-mediated traits such that the tighter the integration, the more reliable the signal is as a predictor of those other traits. Androgen administration increases the duration of the communication signal pulse in both sexes of the electric fish Brachyhypopomus gauderio. To determine whether the duration of the signal pulse could function as an honest indicator of androgen levels and other androgen-mediated traits, we measured the variation in sex steroids, signal pulse duration, and sexual development throughout the breeding season of B. gauderio in marshes in Uruguay. Although the sexes had different hormone titres and signal characteristics, in both sexes circulating levels of the androgens testosterone (T) and 11-ketotestosterone (11-KT) were strongly related to signal pulse duration. Consequently, signal pulse duration can serve as an honest indicator of circulating androgens in males and females alike. Additionally, through phenotypic integration, signal pulse duration also predicts other sexual traits directly related to androgen production: gonad size in males and estradiol (E2) levels in females. Our findings show that tight hormonal phenotypic integration between advertisement signal and other sex steroid-mediated traits renders the advertisement signal an honest indicator of a suite of reproductive traits.     

ADVERTISEMENT CALLS OF THE TREE FROGS,HYLA ARBOREA AND HYLA SAVIGNYI (ANURA: HYLIDAE) IN TURKEY

ABSTRACT

The systematic classification of tree frogs (Hyla) inhabiting different regions of the country of Turkey is unclear. Recordings of natural advertisement calls of individual male tree frogs in different locations in Turkey were analyzed to determine variation in acoustic features that may be related to taxonomic status. Multivariate analysis of covariance showed that call duration, intercali interval and number of pulses per call varied significantly between frogs in different locales. Call duration, intercall interval, and number of pulses per call were related to air temperature. Dominant frequency differed significantly between different groups of frogs, and was temperature-independent. These data are consistent with the hypothesis that tree frogs in Turkey represent two distinct species, Hyla arborea and Hyla savignyi.     

THE IMPORTANCE OF FEMALE CHOICE,MALE–MALE COMPETITION,AND SIGNAL TRANSMISSION AS CAUSES OF SELECTION ON MALE MATING SIGNALS

Selection on advertisement signals arises from interacting sources including female choice, male–male competition, and the communication channel (i.e., the signaling environment). To identify the contribution of individual sources of selection, we used previously quantified relationships between signal traits and each putative source to predict relationships between signal variation and fitness in Enchenopa binotata treehoppers (Hemiptera: Membracidae). We then measured phenotypic selection on signals and compared predicted and realized relationships between signal traits and mating success. We recorded male signals, then measured lifetime mating success at two population densities in a realistic environment in which sources of selection could interact. We identified which sources best predicted the relationship between signal variation and mating success using a multiple regression approach. All signal traits were under selection in at least one of the two breeding seasons measured, and in some cases selection was variable between years. Female preference was the strongest source of selection shaping male signals. The E. binotata species complex is a model of ecological speciation initiated by host shifts. Signal and preference divergence contribute to behavioral isolation within the complex, and the finding that female mate preferences drive signal evolution suggests that speciation in this group results from both ecological divergence and sexual selection.     

Geographic variation in advertisement calls of a Microhylid frog – testing the role of drift and ecology

Acoustic signals for mating are important traits that could drive population differentiation and speciation. Ecology may play a role in acoustic divergence through direct selection (e.g., local adaptation to abiotic environment), constraint of correlated traits (e.g., acoustic traits linked to another trait under selection), and/or interspecific competition (e.g., character displacement). However, genetic drift alone can also drive acoustic divergence. It is not always easy to differentiate the role of ecology versus drift in acoustic divergence. In this study, we tested the role of ecology and drift in shaping geographic variation in the advertisement calls of Microhyla fissipes. We examined three predictions based on ecological processes: (1) the correlation between temperature and call properties across M. fissipes populations; (2) the correlation between call properties and body size across M. fissipes populations; and (3) reproductive character displacement (RCD) in call properties between M. fissipes populations that are sympatric with and allopatric to a congener M. heymonsi. To test genetic drift, we examined correlations among call divergence, geographic distance, and genetic distance across M. fissipes populations. We recorded the advertisement calls from 11 populations of M. fissipes in Taiwan, five of which are sympatrically distributed with M. heymonsi. We found geographic variation in both temporal and spectral properties of the advertisement calls of M. fissipes. However, the call properties were not correlated with local temperature or the callers' body size. Furthermore, we did not detect RCD. By contrast, call divergence, geographic distance, and genetic distance between M. fissipes populations were all positively correlated. The comparisons between phenotypic Q_st (P_st) and F_st values did not show significant differences, suggesting a role of drift. We concluded that genetic drift, rather than ecological processes, is the more likely driver for the geographic variation in the advertisement calls of M. fissipes.     

The potential influence of morphology on the evolutionary divergence of an acoustic signal

The evolution of acoustic behaviour and that of the morphological traits mediating its production are often coupled. Lack of variation in the underlying morphology of signalling traits has the potential to constrain signal evolution. This relationship is particularly likely in field crickets, where males produce acoustic advertisement signals to attract females by stridulating with specialized structures on their forewings. In this study, we characterize the size and geometric shape of the forewings of males from six allopatric populations of the black field cricket (Teleogryllus commodus) known to have divergent advertisement calls. We sample from each of these populations using both wild‐caught and common‐garden‐reared cohorts, allowing us to test for multivariate relationships between wing morphology and call structure. We show that the allometry of shape has diverged across populations. However, there was a surprisingly small amount of covariation between wing shape and call structure within populations. Given the importance of male size for sexual selection in crickets, the divergence we observe among populations has the potential to influence the evolution of advertisement calls in this species.     

Multivariate phenotypic selection on a complex sexual signal

Animal signals are complex, comprising multiple components that receivers may use to inform their decisions. Components may carry information of differing value to receivers, and selection on one component could modulate or reverse selection on another, necessitating a multivariate approach to estimating selection gradients. However, surprisingly few empirical studies have estimated the strength of phenotypic selection on complex signals with appropriate design and adequate power to detect nonlinear selection. We used phonotaxis assays to measure sexual selection on the advertisement signal of Cope's gray tree frog, Hyla chrysoscelis. Female preferences were assessed for five signal components using single‐ and two‐stimulus behavioral assays. Linear, quadratic, and correlational selection gradients were estimated from the single‐stimulus data. Significant directional selection is acting on call duration, call rate, pulse rate, and relative amplitude; stabilizing selection is acting on call duration and call rate. Under the two‐stimulus paradigm, conclusions were qualitatively different, revealing nonlinear selection on all components except call duration. For individual subjects, the outcomes of single‐ and two‐stimulus trials were frequently discordant, suggesting that the choice of testing paradigm may affect conclusions drawn from experiments.     

Differential Evolution of Advertisement Call Traits in Dart-Poison Frogs (Anura: Dendrobatidae)

The ability to recognise and discriminate between heterospecific and conspecific individuals plays an essential role in mate choice, reproductive isolation and thus species diversification. Many animals discriminate based on advertisement calls, whose evolution may be driven by a variety of forces such as natural selection, sexual selection or stochastic processes. The relative importance of stochastic processes acting on a given trait is usually correlated with its phylogenetic signal. Mate-recognition signals are complex traits composed of multiple features that could potentially respond independently to evolutionary forces. The advertisement call of anurans is used in species recognition and mate choice. In this study, we estimate the phylogenetic signal for body size and a suite of traits describing the male advertisement call from dart-poison frogs (Anura: Dendrobatidae). We found a surprisingly high phylogenetic signal for all call traits. In addition, call traits varied in their degree of phylogenetic signal, suggesting that evolutionary forces have been acting differently on different traits. Pulse duration showed the strongest phylogenetic signal. Peak frequency and body size were correlated and presented high phylogenetic signal indicating that the evolution of one trait may be driving or constraining the other. Since most variation in call traits can be explained by the phylogenetic history of the species, we cannot reject the hypothesis that stochastic processes account for significant evolutionary divergence in frog calls.     

Intraspecific variation in advertisement call characteristics and acoustic strategies among male forest green tree frogs

Frogs are a representative taxon that use advertisement calls to aid in reproduction. In most frog species, calls vary with body size, and allometric constraints between body size and call frequency have been widely reported among anuran species. Although this variation is an important driver of sexual selection in frogs, male advertisement call strategies may also vary according to body size. In this study, we conducted playback experiments on the male forest green tree frog (Zhangixalus arboreus) to determine whether male advertisement call characteristics and strategies vary according to body size and the amplitude of intraspecific chorus noise. The results indicated that the calls of larger individuals are louder and lower than those of smaller ones, who call more frequently; moreover, the calls become lower, and the number of calls decreases, as noise levels increase. These findings suggest that forest green tree frog emits lower calls or refrains from calling when chorus noise increases, and that intraspecific variation in advertisement call characteristics can induce different strategies in response to chorus noise. Because advertisement call variation with body size is common among frog species, intraspecific variation in male advertisement call strategies may also be a common phenomenon.     

No species barrier by call in an avian hybrid zone between California and Gambel's quail (Callipepla californica and C. gambelii)

Acoustic signals sometimes act as premating isolating barriers between animal species, but we know little about the circumstances that dictate the presence and strength of these barriers. Among insects, barriers to backcrossing are strengthened by acoustic signals that are under genetic control. Hybrid signals tend to be intermediate to parental signals, and signals are recognized only by like‐types, which results in reinforced species boundaries. This is not typically the case in avian taxa. Instead, acoustic signal transmission is controlled by some combination of genes and learning, and perhaps as a consequence of this variation, vocalizations play a diversity of roles in avian hybrid zones. I used California and Gambel's quail (Callipepla californica and C. gambelii), hybridizing birds that do not learn to vocalize, to explore whether genetically determined vocalizations function as a species barrier. Using spectral analysis, I measured temporal features of calls of uniquely colour‐banded quail that were recorded across one area of the California and Gambel's quail hybrid zone. Species discrimination is known to occur under captive conditions, though its basis is unexplored. Here I show that differences in the calls of parental species are likely great enough to permit species discrimination. Hybrid call components were intermediate to those of the parental species and covaried with genetic traits, as assessed with seven highly polymorphic microsatellite loci. Contrary to expectation, males as frequently called in response to unlike‐ as like‐type females who had initiated antiphonal calling, which is a courtship call between a female and a male. Furthermore, paired males and females did not share like‐type assembly calls, nor was there a correlation between the female's genetic or plumage traits and her mate's advertisement call. Based on these results, I conclude that California and Gambel's quail recognize each other and hybrids as potential mates and backcrossing occurs frequently. Thus, compatible mating signals could contribute to increased mixing of gene pools and slow the rate of speciation. I suggest that selection to respond to wide signal variation within species and imprinting on calls of mixed‐species coveys may cause mating signal compatibility between classes within the area of hybridization. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 86 , 253–264.     

The influence of geographic heterogeneity in predation pressure on sexual signal divergence in an Amazonian frog species complex

Sexual selection plays an important role in mating signal divergence, but geographic variation in ecological factors can also contribute to divergent signal evolution. We tested the hypothesis that geographic heterogeneity in predation causes divergent selection on advertisement call complexity within the Engystomops petersi (previously Physalaemus petersi) frog species complex. We conducted predator phonotaxis experiments at two sites where female choice is consistent with call trait divergence. Engystomops at one site produces complex calls, whereas the closely related species at the other site produces simple calls. Bats approached complex calls more than simple calls at both sites, suggesting selection against complex calls. Moreover, bat predation pressure was greater at the site with simple calls, suggesting stronger selection against complex calls and potentially precluding evolution of complex calls at this site. Our results show that geographic variation in predation may play an important role in the evolution and maintenance of mating signal divergence.