COMMUNITY COMPOSITION AFFECTS THE SHAPE OF MATE RESPONSE FUNCTIONS

The evolution of mate preferences can be critical for the evolution of reproductive isolation and speciation. Heterospecific interference may carry substantial fitness costs and result in preferences where females are most responsive to the mean conspecific trait with low response to traits that differ from this value. However, when male traits are unbounded by heterospecifics, there may not be selection against females that respond to extreme trait values in the unbounded direction. To test how heterospecifics affected the shape of female response functions, I presented female Oecanthus tree crickets with synthetic calls representing a range of male calls, then measured female phonotaxis to construct response functions. The species with the fastest pulse rates in the community consistently responded to pulse rates faster than those produced by their males, whereas in the intermediate and slowest pulse rate species there was no significant difference between the male trait and the female response. This work suggests that species with the most extreme signal in the community respond to a greater range of signals, potentially resulting in a higher probability of hybridization during secondary contact, and revealing interactions between mate recognition and other aspects of sexual selection.     

Parallel plasticity of mating songs and preferences in the field cricket Gryllus rubens

In animal communication systems, matching mating signals and preferences enable species identification and successful reproduction. In some species, the environment introduces substantial variation in signals and/or preferences. Only a few studies have tested how the match between signals and preferences is maintained despite phenotypic variation. Signal–preference coupling in the context of phenotypic plasticity is the focus of this study. The bivoltine cricket Gryllus rubens displays seasonal differences in the pulse rate of its mating songs. The seasonal effect on other fine‐temporal characters of the songs besides pulse rate, such as pulse and interval duration, duty cycle, as well as the dominant frequency, is not known and is described in the first part of the study for a Kentucky population. In the second part of the study, we tested preferences of spring and fall females to determine whether they match the seasonal plasticity of male songs using single‐speaker phonotaxis experiments. We found that fall songs had a faster pulse rate, shorter pulse and interval durations, and a higher dominant frequency than spring songs. Female preferences shifted in parallel with male song plasticity, that is, spring females preferred the spring song and fall females the fall song. In addition, female responsiveness to male song was plastic as well, that is, fall females were significantly more responsive than spring females. The parallel plasticity of male songs and female preferences facilitates successful communication despite the environmentally induced variation. The potential origin and function of behavioral plasticity in G. rubens are discussed.     

Temperature coupling of mate attraction signals and female mate preferences in four populations of Enchenopa treehopper (Hemiptera: Membracidae)

Variation in temperature can affect the expression of a variety of important fitness‐related behaviours, including those involved with mate attraction and selection, with consequences for the coordination of mating across variable environments. We examined how temperature influences the expression of male mating signals and female mate preferences—as well as the relationship between how male signals and female mate preferences change across temperatures (signal–preference temperature coupling)—in Enchenopa binotata treehoppers. These small plant‐feeding insects communicate using plantborne vibrations, and our field surveys indicate they experience significant natural variation in temperature during the mating season. We tested for signal–preference temperature coupling in four populations of E. binotata by manipulating temperature in a controlled laboratory environment. We measured the frequency of male signals—the trait for which females show strongest preference—and female peak preference—the signal frequency most preferred by females—across a range of biologically relevant temperatures (18°C–36°C). We found a strong effect of temperature on both male signals and female preferences, which generated signal–preference temperature coupling within each population. Even in a population in which male signals mismatched female preferences, the temperature coupling reinforces predicted directional selection across all temperatures. Additionally, we found similar thermal sensitivity in signals and preferences across populations even though populations varied in the mean frequency of male signals and female peak preference. Together, these results suggest that temperature variation should not affect the action of sexual selection via female choice, but rather should reinforce stabilizing selection in populations with signal–preference matches, and directional selection in those with signal–preference mismatches. Finally, we do not predict that thermal variation will disrupt the coordination of mating in this species by generating signal–preference mismatches at thermal extremes.     

Interspecific genetics of mate recognition: inheritance of female acoustic preference in Hawaiian crickets

Abstract. Female mating behavior plays a fundamental role in the divergent evolution of mate recognition systems that may lead to speciation. Despite this important role, the phenotypic and genetic bases of female mating behavior remain poorly understood. In this study, I examine the shape of the female acoustic preference function and estimate values for pulse rate preference in two species of Hawaiian crickets, Laupala kohalensis and L. paranigra . In addition, I examine how preference differences are inherited in hybrid crosses between these species. Females expressed unimodal preference functions and were generally more attracted to pulse rates characterizing their own species. Unimodal preference functions also characterized F1 and backcross generations, with hybrid females expressing preferences for intermediate pulse rates. Pulse rate preferences segregated in the backcross generation. Mean pulse rate preference matched mean pulse rate in both parental and hybrid generations. Based on F1 hybrids and segregation patterns in backcross females, I show that changes in both signal and receiver components of the mate recognition system are consistent with a multilocus model of change through incremental steps. The results therefore suggest that ancestors of the current species also expressed unimodal preference functions and that changes in acoustic communication signals occurred through shifts in mean pulse rates and pulse rate preferences among populations.     

Characterization of female preference functions for Drosophila montana courtship song and a test of the temperature coupling hypothesis

Female mate preferences are a major cause of diversity and elaboration in male sexual traits. Here we characterize the shape of female preference functions for pulse length and carrier frequency of the courtship song of Drosophila montana by fitting both parametric and nonparametric functions to the incidence of female receptive gestures to synthetic song. Preference functions for both traits are strongly directional. That for pulse length is linear and favors short pulses, whereas that for carrier frequency is stabilizing in shape, but would exert directional preferences favoring males with high carrier frequency. The preference for carrier frequency has probably evolved under sexual selection, but reasons for the preference for short pulses are less apparent. We also examine the effect of ambient temperature on the carrier frequency of male song and on the preference function for carrier frequency. For many similar acoustic communication systems, temperature coupling, a compensatory effect of temperature on preference functions, is thought to maintain coordination between preferences and signals. However, although the carrier frequency of D. montana song is highly dependent on environmental temperature, there is no temperature coupling of the female preference function. We suggest that temperature coupling may often arise due to a common effect of temperature on song and preference, rather than be an advantageous characteristic whose function is to maintain coordination in temperature-affected communication systems.     

Developmental plasticity of mating calls enables acoustic communication in diverse environments

Male calls of the katydid Neoconocephalus triops exhibit substantial developmental plasticity in two parameters: (i) calls of winter males are continuous and lack the verse structure of summer calls and (ii) at equal temperatures, summer males produce calls with a substantially higher pulse rate than winter males. We raised female N. triops under conditions that reliably induced either summer or winter phenotype and tested their preferences for the call parameters that differ between summer and winter males.Neither generation was selective for the presence of verses, but females had strong preferences for pulse rates: only a narrow range of pulse rates was attractive. The attractive ranges did not differ between summer and winter females. Both male pulse rate and female preference for pulse rate changed with ambient temperature, but female preference changed more than the male calls.As a result, the summer call was attractive only at 25 degrees C, whereas the slower winter call was attractive only at 20 degrees C. Thus, developmental plasticity of male calls compensates for differences in temperature dependency between calls and preferences and enables the communication system to function in heterogeneous environments. The potential role of call plasticity during the invasion of new habitats is discussed.     

Males adjust their signalling behaviour according to experience of male signals and male–female signal duets

Sexual signals are conspicuous sources of information about neighbouring competitors, and species in which males and females signal during pair formation provide various sources of public information to which individuals can adjust their behaviour. We performed two experiments with a duetting vibrational insect, Enchenopa binotata treehoppers (Hemiptera: Membracidae), to ask whether males adjust their signalling behaviour according to (1a) their own experience of competitors' signals, (1b) how females adjust their mate preferences on the basis of their experience of male signals (described in prior work), and/or (2) their own experience of female response signals to competitors' signals. We presented males with synthetic male signals of different frequencies and combinations thereof for 2 weeks. We recorded males a day after their last signal exposure, finding that (1a) male signal rate increased in response to experience of attractive competitors, but that (1b) male signal frequency did not shift in a manner consistent with how females adjust their mate preferences in those experience treatments. Second, we presented males with different male–female duets for 2 weeks, finding that (2) male signal length increased from experience of female duets with attractive competitors. Males thus make two types of adjustment according to two sources of public information: one provided by experience of male signals and another by experience of female responses to male signals. Signalling plasticity can generate feedback loops between the adjustments that males and females make, and we discuss the potential consequences of such feedback loops for the evolution of communication systems.     

Within‐Species Mate Preferences Do Not Contribute to the Maintenance of Sexually Monomorphic Mating Signals in Green Lacewings

We know much less about the evolutionary forces and constraints that maintain similar mating displays in females and males than we do about sexually dimorphic mating displays. Both female and male green lacewings have sexually monomorphic vibrational mating signals and are equally choosy against heterospecific mating signals. This similarity in between‐species sex roles may explain a large part of the presence of species‐specific female signals in these species, but does not necessarily predict why female and male signals are similar. We tested for within‐species sex‐specific similarities in mate preferences in Chrysoperla lucasina that may contribute to the maintenance of sexually monomorphic mating signals in this species. We found weak preferences and low levels of discrimination for signals with varying fine‐scale temporal features (volley duration, period, and volley‐duty cycle). The longer signals that both sexes produced in response to playback were sexually monomorphic, but some females and most males also produced shorter signals with significantly reduced volley durations and periods. Notably, all of these signals had indistinguishable volley‐duty cycles, the ratio of volley duration to volley period. We propose that mating signals in C. lucasina are maintained in both sexes because of similar between‐species mate preferences, but the sexually monomorphic mating signals cannot be attributed to significant within‐species mate preferences. What differences are present in within‐species sex roles may be resolved by a male‐biased signal polymorphism, in long and short signals that are hypothesized to have distinct functions during mate calling and courtship.     

Advertisement-call preferences in diploid-tetraploid treefrogs (Hyla chrysoscelis and Hyla versicolor): implications for mate choice and the evolution of communication systems

Signals used for mate choice and receiver preferences are often assumed to coevolve in a lock-step fashion. However, sender-receiver coevolution can also be nonparallel: even if species differences in signals are mainly quantitative, females of some closely related species have qualitatively different preferences and underlying mechanisms. Two-alternative playback experiments using synthetic calls that differed in fine-scale temporal properties identified the receiver criteria in females of the treefrog Hyla chrysoscelis for comparison with female criteria in a cryptic tetraploid species (H. versicolor); detailed preference functions were also generated for both species based on natural patterns of variation in temporal properties. The species were similar in three respects: (1) pulses of constant frequency were as attractive as the frequency-modulated pulses typical of conspecific calls; (2) changes in preferences with temperature paralleled temperature-dependent changes in male calls; and (3) preference functions were unimodal, with weakly defined peaks estimated at values slightly higher than the estimated means in conspecific calls. There were also species differences: (1) preference function slopes were steeper in H. chrysoscelis than in H. versicolor; (2) preferences were more intensity independent in H. chrysoscelis than in H. versicolor; (3) a synergistic effect of differences in pulse rate and shape on preference strength occurred in H. versicolor but not in H. chrysoscelis; and (4) a preference for the pulse shape typical of conspecific calls was expressed at the species-typical pulse duration in H. versicolor but not in H. chrysoscelis. However, females of H. chrysoscelis did express a preference based on pulse shape when tested with longer-than-average pulses, suggesting a hypothesis that could account for some examples of nonparallel coevolution. Namely, preferences can be hidden or revealed depending on the direction of quantitative change in a signal property relative to the threshold for resolving differences in that property. The results of the experiments reported here also predict patterns of mate choice within and between contemporary populations. First, intraspecific mate choice in both species is expected to be strongly influenced by variation in temperature among calling males. Second, simultaneous differences in pulse rate and pulse shape are required for effective species discrimination by females of H. versicolor but not by females of H. chrysoscelis. Third, there is greater potential for sexual selection within populations and for discrimination against calls produced by males in other geographically remote populations in H. chrysoscelis than in H. versicolor.     

The effect of temperature on male mating signals and female choice in the red mason bee,Osmia bicornis (L.)

Climate change and the resulting changes in air temperature are known to have a major influence on most animals, especially poikilothermic insects, because they depend on the high enough temperatures to function. Previous studies have shown that various signals can be affected by changes in temperature. However, research into the effect of temperature on mating signals and subsequently communication between mates and on female choice is still rare. In the red mason bee, Osmia bicornis, which emerges early in spring and is therefore subject to extensive temperature changes, females choose suitable males based on, among other criteria, their thorax vibrations and odor. So far there has been no research into the effect of temperature changes on these signals. We therefore investigated whether the environmental temperature has an influence on the male's mating signals by measuring vibrations using a laser vibrometer and collecting male and female odor at different temperatures. Furthermore, we performed behavioral experiments in order to show whether there is an effect of temperature‐induced changes and female choice. Our results showed that rejected males differed in their vibrations between the two temperature settings but accepted ones did not. Temperature changes therefore seem to have a stronger effect on those males that are rejected by the females, whereas the accepted males are the ones that can produce desirable signals despite temperature fluctuations. Furthermore, we found that the differences in odor profiles were greater between temperature settings than between the sexes and that females change their preference for odor with temperature. We conclude that temperature strongly influences the male mating signals and therefore may have a major impact on sexual selection in this species. This is an important aspect to consider, not only in future studies on mating behavior, but also in view of our ever raising temperatures.     

Divergence in Female Duetting Signals in the Enchenopa binotata Species Complex of Treehoppers (Hemiptera: Membracidae)

Sexual communication often involves signal exchanges between the sexes, or duetting, in which mate choice is expressed through response signals. With both sexes acting as signalers and receivers, variation in the signals of males and females may be important for mate choice, reproductive isolation, and divergence. In the Enchenopa binotata species complex – a case study of sympatric speciation in which vibrational duetting may have an important role – male signals are species‐specific, females choose among males on the basis of signal traits that reflect species and individual differences, and female preferences have exerted divergent selection on male signals. Here, we describe variation in female signals in the E. binotata species complex. We report substantial species differences in the spectral and temporal features of female signals, and in their timing relative to male signals. These differences were similar in range to differences in male signals in the E. binotata complex. We consider processes that might contribute to divergence in female signals, and suggest that signal evolution in the E. binotata complex may be influenced by mate choice in both sexes.     

Evolution of Novel Signal Traits in the Absence of Female Preferences in Neoconocephalus Katydids (Orthoptera,Tettigoniidae)

Background Significance

Communication signals that function to bring together the sexes are important for maintaining reproductive isolation in many taxa. Changes in male calls are often attributed to sexual selection, in which female preferences initiate signal divergence. Natural selection can also influence signal traits if calls attract predators or parasitoids, or if calling is energetically costly. Neutral evolution is often neglected in the context of acoustic communication.

Methodology/Principal Findings

We describe a signal trait that appears to have evolved in the absence of either sexual or natural selection. In the katydid genus Neoconocephalus, calls with a derived pattern in which pulses are grouped into pairs have evolved five times independently. We have previously shown that in three of these species, females require the double pulse pattern for call recognition, and hence the recognition system of the females is also in a derived state. Here we describe the remaining two species and find that although males produce the derived call pattern, females use the ancestral recognition mechanism in which no pulse pattern is required. Females respond equally well to the single and double pulse calls, indicating that the derived trait is selectively neutral in the context of mate recognition.

Conclusions/Significance

These results suggest that 1) neutral changes in signal traits could be important in the diversification of communication systems, and 2) males rather than females may be responsible for initiating signal divergence.     

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.     

Male courtship signals and female signal assessment in Photinus greeni fireflies

The evolutionary dynamic of courtship signaling systems is drivenby the interaction between male trait distributions and femalepreferences. This interaction is complex because females maychoose mates based on multiple components of male signals, andfemale preference functions may vary depending on mate availability,female reproductive state, and environmental conditions. InPhotinus fireflies (Coleoptera: Lampyridae), flying males emitbioluminescent flash signals to locate sedentary females, whichreply selectively to attractive male flash signals with theirown response flash. In this study, we first examined temporalvariation in the paired-pulse flash patterns produced by Photinusgreeni males in the field and found significant among-male variation(70% of total variation) in interpulse intervals (IPIs). Therewas no significant relationship between male IPI and spermatophoresize, suggesting that P. greeni male courtship signals do notprovide females with reliable indicators of male material resources.In laboratory playback experiments, we presented P. greeni femaleswith simulated flash signals to assess how IPI and pulse durationindependently affected the likelihood of female flash response.We also examined the effects of female body mass and time duringthe mating season on female preference functions, hypothesizingthat females would be less discriminating when they were heavier(more fecund) and when mate availability declined. We foundthat P. greeni females discriminated among signals within theirspecies' range based primarily on flash pattern IPI. Neitherthe time during the mating season nor female weight alteredfemale preference functions for IPI, although season did influencefemale response to pulse duration. These results reveal thatP. greeni females discriminate among conspecific males basedprimarily on male IPIs, the same signal character previouslyshown to be important for firefly species recognition. Fieldplayback experiments indicated that female responsiveness peakednear the average IPI given by males at different ambient temperatures,suggesting that fireflies exhibit temperature coupling similarto that seen in many acoustically signaling animals.     

MULTIPLE GENETIC LINKAGES BETWEEN FEMALE PREFERENCE AND MALE SIGNAL IN RAPIDLY SPECIATING HAWAIIAN CRICKETS

Diverging sexual communication systems can lead to the evolution of new species that no longer recognize each other as potential mates. The coevolution of male and female components of sexual communication is facilitated by physical linkage between genes underlying signals and preferences. By crossing two closely related Hawaiian crickets (Laupala kohalensis and Laupala paranigra) with vastly different song pulse rates and female preferences, and assessing segregation of songs and preferences among second generation backcrosses, we show a strong genetic correlation between song and preference variation. Furthermore, multiple, but not all, quantitative trait loci underlying song variation also predict female preferences. This physical linkage or pleiotropy may have facilitated the striking diversification of pulse rates observed among Laupala species in conjunction with one of the most rapid species radiations so far recorded.     

Elevated stress hormone diminishes the strength of female preferences for acoustic signals in the green treefrog

Mate selection can be stressful; time spent searching for mates can increase predation risk and/or decrease food consumption, resulting in elevated stress hormone levels. Both high predation risk and low food availability are often associated with increased variation in mate choice by females, but it is not clear whether stress hormone levels contribute to such variation in female behavior. We examined how the stress hormone corticosterone (CORT) affects female preferences for acoustic signals in the green treefrog, Hyla cinerea. Specifically, we assessed whether CORT administration affects female preferences for call rate — an acoustic feature that is typically under directional selection via mate choice by females in most anurans and other species that communicate using acoustic signals. Using a dual speaker playback paradigm, we show that females that were administered higher doses of CORT were less likely to choose male advertisement calls broadcast at high rates. Neither CORT dose nor level was related to the latency of female phonotactic responses, suggesting that elevated CORT does not influence the motivation to mate. Results were also not related to circulating sex steroids (i.e., progesterone, androgens or estradiol) that have traditionally been the focus of studies examining the hormonal basis for variation in female mate choice. Our results thus indicate that elevated CORT levels decrease the strength of female preferences for acoustic signals.     

The effect of vibratory disturbance on sexual behaviour of the southern green stink bug Nezara viridula (Heteroptera, Pentatomidae)

The effect of vibratory disturbance on sexual behaviour and substrate-borne sound communication of the southern green stink bug, Nezara viridula L. was studied. Disturbance signals do not change the time N. viridula males need to locate the source of vibratory signals, but decrease the number of males responding with the calling and courtship song to calling females. Female N. viridula proceed calling during stimulation with disturbance signals but some of them change the song rhythm by skipping one or more signal intervals or emitting the repelling signals. The number of females which change the dominant frequency of the calling song decreases proportionally with increasing differences between the dominant frequency of the disturbance signals and the emitted female calling song. Variation of the song dominant frequency probably serves females to avoid interference by increasing the signal to noise ratio. Signal duration and repetition rate do not change significantly when the female is stimulated with the disturbance signals. This indicates that frequency shift by calling females is the main strategy for reducing interference by competitive signalers in N. viridula vibrational communication.     

Adjustment of vibratory signals to ambient temperature in a host-searching parasitoid

Abstract.  Certain ichneumonid parasitoids (Hymenoptera) use self-produced vibrations transmitted on plant substrate, so-called vibrational sounding, to locate their immobile concealed pupal hosts. An ambient temperature dependency with higher frequencies and intensities at higher temperatures is postulated because signals are of myogenic origin. Here, temperature influence on vibratory signals is analysed in the temperate parasitoid Pimpla turionellae under different thermal conditions using plant-stem models to elicit host-searching behaviour. Signals are measured with laser Doppler vibrometry and analysed for time parameters and frequency components applying fast-Fourier transformations. The results reveal an unexpected effect of ambient temperature on signals produced by the female wasps. Although average values of time parameters (pulse trains, pulse train periods, inter pulse duration) are unchanged by ambient temperature, the frequency parameters show an inverse thermal effect. Within the temperature range tested (8–26 °C), decreasing temperature leads to significantly higher frequency and intensity of the self-produced vibrations in the temperate species. This inverse thermal effect may be explained by a temperature-coupled signal production in the frequency domain to compensate negative low-temperature effects on the mechanoreceptors by increased muscle activity. The option of heterothermy to produce signals reliably during vibrational sounding under low temperature is also discussed.     

Proximity‐dependent Response to Variably Complex Mating Signals in Túngara Frogs (Physalaemus pustulosus)

The plasticity of animal behavior allows individuals to maximize fitness in a wide range of contexts. Both production of and preference for mating signals are context‐dependent according to internal factors such as hormonal state, and external factors such as predation risk. In many species, male‐to‐female proximity also defines an important context for mating communication. Males often possess short‐distance courtship signals, and females often exhibit distance‐related variation in signal response. Such variation in response may occur when a signal’s relevance changes with male‐to‐female distance, but it may also result from perceptual constraints that are unrelated to fitness. Túngara frogs produce variably complex advertisement calls, and sexual selection theory predicts that females should prefer calls of greater complexity. Preference tests, however, have not demonstrated consistent trends for preference between calls of variable complexity. We tested whether proximity to males influences female response to variable signal complexity and found that both preference and memory for signal complexity are proximity‐dependent.     

Mating signal partitioning in multi-species assemblages: a null model test using frogs

Abstract Competitive partitioning of ‘community’ signal space has long been suggested to underlie diversification of mating signals. Selection or competitive exclusion is expected to reduce overlap of signals, minimizing destructive interference or reducing mismating. We used null models backed by simulation of type I and II error rates to test for evidence of structuring within 11 frog advertisement call assemblages. Within three assemblages, we found significant over‐dispersion and regularity‐of‐spacing in dominant frequency and in pulse rate, consistent with a signal interference hypothesis and signal confusion hypothesis, respectively. Observed partitioning could represent signal evolution or could result from selection on assemblage composition. Most assemblages showed no acoustic partitioning possibly because: (i) partitioning is more readily apparent in female preference, calling times or sites, rather than call attributes; (ii) assemblages have not yet accommodated recently arrived species, or are compositionally unstable so that acoustic accommodation cannot occur; and (iii) evidence of partitioning is only likely where the acoustic space is densely packed.