Mate Attraction Signals Research Articles

Vocal sacs do not function in multimodal mate attraction under nocturnal illumination in Cope's grey treefrog

Multimodal communication signals consist of two or more distinct components produced in different sensory modalities and transduced by receivers using multiple sensory systems. One evolutionary trajectory by which incipient multimodal signals may arise is when receivers are selected to attend both to a well-established signal and a cue in a different sensory modality associated with that signal's production. Previous studies of frogs suggest movement of the male's vocal sac, which is inextricably tied to vocal production in most species, functions as the dynamic visual component of a multimodal mate attraction signal that modulates female responses to sexually advertising males. Most of this work, however, has presented multimodal stimuli using video playbacks or artificially illuminated robots in laboratory settings, which leaves open the question of whether the vocal sac functions in multimodal signalling under more natural nocturnal illumination. In this study of Cope's grey treefrog, Hyla chrysoscelis , a nocturnally breeding species, we tested the hypothesis that vocal sacs are a dynamic visual component of a multimodal mate attraction signal that influences female responses to sexually advertising males. Using robotic frogs as stimuli, we performed multimodal playback experiments outdoors under nocturnal illumination. We found no evidence that vocal sacs were attractive to females or that they influenced the responses of females when acoustic information was rendered less certain due to a degraded signal structure or background noise. While these negative results may reflect genuine species differences, they also corroborate a negative result from one of the only previous studies conducted under natural nocturnal illumination to investigate frog vocal sacs as the visual component of a putative multimodal mate attraction signal (Taylor et al., 2007, Animal Behaviour, 74 , 1753–1763). We consider possible proximate and ultimate explanations for our results and critically review previous research on multimodal mate attraction in nocturnal frogs. • Multimodal signals stimulate multiple receiver sensory organs. • Diverse animals use multimodal signals in many contexts, including mate choice. • Frog vocal sacs previously implicated as components of multimodal sexual signals. • Robotic playbacks under natural, nocturnal illumination suggest otherwise. • Current methods may mismeasure multimodal mate choice in nocturnal animals.

Developmental biology and seasonal phenology of Aacanthocnema dobsoni (Hemiptera: Triozidae) and the influence of climate‐mediated changes in body size on vibrational signals

AbstractThe biology and seasonal phenology of Aacanthocnema dobsoni (Froggatt) were studied at a single site in Victoria over a 2 year period between 2013 and 2015. This species is monophagous on the dioecious host, Allocasuarina verticillata (Lam.) L. Johnson (Casuarinaceae). Laboratory studies found that females attained reproductive maturity 24 h post‐eclosion, lived for 28.6 ± 2.8 (mean ± SE) days and laid 182 ± 23 (mean ± SE) eggs each. Egg development was most rapid at 26 °C, ceased below 7 °C and above 33 °C; hatching required 188 degree‐days. Nymphs could not be reared to adulthood on excised host branchlets maintained under controlled conditions, so no developmental data were obtained for these life stages. Seasonal phenology data revealed pronounced developmental asynchrony, i.e. with overlapping generations and multiple life stages occurring simultaneously. Three generations per year were observed, and there was no evidence of either developmental (egg and nymph) or reproductive diapause. A 4 day heat wave in January 2014 drastically reduced psyllid abundance at the study site and the size of the adults that eclosed from the surviving nymphs. These smaller adults produced substrate‐borne vibrational signals with altered characteristics, i.e. with significantly higher intensities and power. The altered signals might have facilitated communication over longer distances and increased mate finding opportunities when populations were low. The abundance of adults had recovered to preheat wave levels 3 months after the heat wave. High fecundity, multivoltinism and effective mate attraction signalling are life history traits that may mitigate against localised extinction of populations as a consequence of extreme weather events.

Male black widows parasitize mate-searching effort of rivals to find females faster.

Mate-searching success is a critical precursor to mating, but there is a dearth of research on traits and tactics that confer a competitive advantage in finding potential mates. Theory and available empirical evidence suggest that males locate mates using mate-attraction signals produced by receptive females (personal information) and avoid inadvertently produced cues from rival males (social information) that indicate a female has probably already mated. Here, we show that western black widow males use both kinds of information to find females efficiently, parasitizing the searching effort of rivals in a way that guarantees competition over mating after reaching a female's web. This tactic may be adaptive because female receptivity is transient, and we show that (i) mate searching is risky (88% mortality) and (ii) a strongly male-biased operational sex ratio (from 1.2 : 1 to more than 10 : 1) makes competition inevitable. Males with access to rivals' silk trails moved at higher speeds than those with only personal information, and located females even when personal information was unreliable or absent. We show that following rivals can increase the potential for sexual selection on females as well as males and argue it may be more widespread in nature than is currently realized.

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.

The paradox of hearing at the lek: auditory sensitivity increases after breeding in female gray treefrogs (Hyla chrysoscelis).

Both behavioral receptivity and neural sensitivity to acoustic mate attraction signals vary across the reproductive cycle, particularly in seasonally breeding animals. Across a variety of taxa receptivity to signals increases, as does peripheral auditory sensitivity, as females transition from a non-breeding to breeding condition. We recently documented decreases in receptivity to acoustic mate attraction signals and circulating hormone levels, but an increase in peripheral auditory sensitivity to call-like stimuli following oviposition in Cope's gray treefrogs (Hyla chrysoscelis). However, it is not known if changes in auditory sensitivity are confined to the frequency range of calls, or if they result from more generalized changes in the auditory periphery. Here, we used auditory brainstem responses (ABRs) to evaluate peripheral frequency sensitivity in female Cope's gray treefrogs before and after oviposition. We found lower ABR thresholds, greater ABR amplitudes, and shorter ABR latencies following oviposition. Changes were most pronounced and consistent at lower frequencies associated with the amphibian papilla, but were also detectable at higher frequencies corresponding to the tuning of the basilar papilla. Furthermore, only ABR latencies were correlated with circulating steroid hormones (testosterone). Changes in peripheral processing may result from changes in metabolic function or sensorineural adaptation to chorus noise.

Synchronous waving in fiddler crabs: a review.

Many animals that use acoustic communication synchronize their mate attraction signals: individuals precisely time their calls to overlap those of their neighbors. In contrast, synchrony in the mate attraction displays of species with visual/motion-based signals is rare. It has only been documented in five species of fiddler crabs. In all of them, small groups of males wave their single large claw in close synchrony. Here, I review what we know about synchrony in fiddler crabs, comparing the five species with each other to determine whether similar mechanisms and functions are common to all. I also propose future research questions that, if answered, would shed light on synchronous behavior in both visual and acoustic signallers.

How dietary protein and carbohydrate influence field cricket development, size and mate attraction signalling

Researchers examining how nutrition impacts fitness traits usually examine one nutrient at a time, ignoring potential interactions. When researchers simultaneously examine multiple nutrients, their studies often focus on adults, ignoring potential changes in nutritional needs that occur during the transition between juvenile and adult stages. To address these issues, we quantified how dietary nutrient balance (relative amounts of protein and carbohydrate) during development and into adulthood influenced life history and sexually selected traits using male Jamaican field crickets, Gryllus assimilis. Our findings revealed that male crickets developed significantly faster and grew larger when they were reared on a protein-rich diet, but their average daily time spent signalling for mates was significantly higher when they were reared on a carbohydrate-rich diet. Furthermore, while the probability of signalling and daily time spent signalling increased with age, time spent signalling for mates tended to increase at a higher rate with age when males consumed a carbohydrate-rich diet in adulthood. Together our findings suggest that traits may differ in their nutrient requirements, resulting in diet influencing a possible trade-off between traits across different life stages. The ability to locate and consume foods rich in protein during development should impact adult male fitness, as protein availability results in larger males, and larger males typically produce more attractive signals and are preferred by females. Conversely, the ability to locate and consume foods rich in carbohydrate should also impact a male's fitness, as males signal with higher effort when fed carbohydrate-rich diets, and higher signalling effort can directly impact a male's ability to attract a female.

Tree crickets optimize the acoustics of baffles to exaggerate their mate-attraction signal.

Object manufacture in insects is typically inherited, and believed to be highly stereotyped. Optimization, the ability to select the functionally best material and modify it appropriately for a specific function, implies flexibility and is usually thought to be incompatible with inherited behaviour. Here, we show that tree-crickets optimize acoustic baffles, objects that are used to increase the effective loudness of mate-attraction calls. We quantified the acoustic efficiency of all baffles within the naturally feasible design space using finite-element modelling and found that design affects efficiency significantly. We tested the baffle-making behaviour of tree crickets in a series of experimental contexts. We found that given the opportunity, tree crickets optimised baffle acoustics; they selected the best sized object and modified it appropriately to make a near optimal baffle. Surprisingly, optimization could be achieved in a single attempt, and is likely to be achieved through an inherited yet highly accurate behavioural heuristic.

Influence of dietary nutrient balance on aggression and signalling in male field crickets

Indicator models of sexual selection predict that sexually selected trait elaboration should covary positively with condition. However, nutrition might influence the expression of multiple traits, where high-quality diets may result in positive trait correlations and low-quality diets in trade-offs. Although previous studies have examined how diet quantity or single nutrients, such as protein, carbohydrate and phosphorus, influence sexual traits, few have examined how dietary nutrient balance affects sexual trait expression. We therefore investigated how dietary protein:carbohydrate ratio and percentage of phosphorus influence the relationship between investment in mate attraction signalling and aggression. We fought groups of six adult male Gryllus veletis crickets, each consuming a unique diet, while recording their prefight and postfight signalling parameters. We found no evidence that diet influenced aggression or prefight signalling, with the exception that high-phosphorus diets had a negative influence on several signalling effort parameters. Body size was an important predictor of aggressive behaviour and most signalling parameters, suggesting that developmental diet may have a greater influence on these sexual traits. Several prefight signalling parameters were weakly related to aggression, suggesting that signalling may advertise competitive abilities. Males consuming high-carbohydrate and equal protein:carbohydrate diets experienced changes in signalling parameters that represented an overall increase in signalling effort following aggressive contests compared to males consuming high-protein diets, suggesting that dietary effects on signalling may only become apparent following periods of highly energetic activity. Changes in signalling following aggressive contests were also related to aggression levels modulated by dietary phosphorus content, such that only males consuming low-phosphorus diets were able to invest heavily in signalling after investing heavily in aggression. Our findings highlight the importance of research on the interplay between multiple sexually selected traits, and how dietary nutrient balance influences these relationships.

A Higher-Than-Average Female Voice Can Cause Young Adult Female Listeners to Think About Aggression More

Previous research found that speakers with more attractive voices receive more favorable evaluations (aka the vocal attractiveness stereotype). But sexual selection theory predicts that, to the extent that men perceive women with higher pitched voices as more attractive, women will be more hostile toward those women because they make more threatening mate rivals. Supporting this hypothesis, Study 1 ( N = 102) showed that female participants higher in trait dominance displayed heightened aggressive cognition after being primed with a romantic (but not a control) feeling and listening to a higher- but not lower-than-average female voice. Study 2 ( N = 111) showed that this heightened aggressive cognition was activated by a long-term but not a short-term mating motive. These findings supported sexual selection theory, challenged the vocal attractiveness stereotype, and suggested a mechanism that helps maintain the honesty of female voice pitch as a mate attraction signal.

Linking mating preferences to sexually selected traits and offspring viability: good versus complementary genes hypotheses

Indirect fitness benefits hypotheses suggest that offspring of preferred mates should exhibit greater survival or reproductive success. For example, good genes hypotheses propose that female mating preferences are mediated by secondary sexual traits because they honestly reflect the ability to pass on genes that will enhance offspring survival or reproduction. Conversely, complementary genes hypotheses propose that mating preferences are mediated by complementary genes because they enhance offspring viability. While these two research traditions are not strict alternatives and both may operate simultaneously, they have never been tested together. Here we explore the multiple potential underlying factors influencing mating preference evolution in Jamaican field crickets, Gryllus assimilis. After evaluating female preferences for randomly selected males, we tested whether preferred males differed from nonpreferred males in their body size, relative mass or mate attraction signals. We then mated females to their preferred or nonpreferred partners and tested offspring viability. Results revealed: (1) females preferred larger males, (2) larger females oviposited more eggs, (3) neither morphology nor mate attraction signalling explained variation in offspring viability, and (4) mating with a preferred partner did not enhance offspring viability. Overall, in our current study population, cricket mate preferences were inconsistent with complementary genes and good genes hypotheses for indirect fitness benefits. Our current research explores whether male secondary sexual traits honestly reflect the ability to pass on genes that enhance offspring reproduction.

The worm has turned: Behavioural drivers of reproductive isolation between cryptic lineages

Behavioural processes such as species recognition and mate attraction signals enforce and reinforce the reproductive isolation required for speciation. The earthworm Lumbricus rubellus in the UK is deeply differentiated into two major genetic lineages, ‘A’ and ‘B’. These are often sympatric at certain sites, but it is not known whether they are to some extent reproductively isolated. Behavioural tests were performed, in which individually genotyped worms were able to choose between soils previously worked either by genetically similar or dissimilar individuals (N = 45). We found that individuals (75%) were significantly (P < 0.05) more likely to orientate towards the soil conditioned by worms of their own lineage. Further testing involved a choice design based on filter papers wetted with water extracts of soils worked by a different genotype on each side (N = 18) or extracts from worked soil vs. un-worked control soil (N = 10). Again, earthworms orientated towards the extract from their kindred genotype (P < 0.05). These findings indicate that genotype-specific water-soluble chemicals are released by L. rubellus; furthermore, they are behaviour-modifying, and play a role in reproductive isolation between sympatric earthworm lineages of cryptic sibling species, through pre-copulatory assortative mate choice.

Same-sex sexual behaviour in crickets: understanding the paradox

Same-sex sexual behaviour (SSSB) occurs in animals ranging from insects to mammals, yet its evolutionary origins remain enigmatic. Is it adaptive, or has it evolved as a by-product of selection for other traits? Using data from two experiments on male spring field crickets, Gryllus veletis, we tested whether SSSB is socially adaptive, sexually adaptive, correlated with other sexual behaviours and/or a result of sex misidentification. By identifying how sexual experience, audience composition, mate attraction signalling time, body size/mass, food composition and aggression levels correlated with levels of SSSB, we found support for the misidentification and phenotypic correlation hypotheses. More aggressive males were more likely to court other males, and males who spent the most time signalling to attract mates tended to spend the most time courting other males, suggesting that aggression, mate signalling effort and same-sex courtship may all be phenotypically correlated. However, the positive relationship between mate attraction signalling effort and probability of expressing same-sex courtship only occurred in males on a high-carbohydrate, low-protein food, suggesting that the expression of such a phenotypic correlation may be constrained by dietary carbohydrate availability. Finally, males were more likely to be courted if they were less aggressive and spent little time signalling for mates, but, for the latter, only if they were on high-carbohydrate foods, suggesting that together, diet, which may alter chemical cues involved in sex identification, and behavioural cues may lead to sex misidentification. Thus, SSSB in male G. veletis does not appear to be adaptive, probably evolving instead as a by-product of selection for other sexually selected traits. By investigating both proximate and ultimate factors contributing to the evolutionary enigma of SSSB, we may gain important insights into the selective forces shaping aggression, social interactions and reproductive strategies in social animals.

Sensory-based niche partitioning in a multiple predator - multiple prey community.

Many predators and parasites eavesdrop on the communication signals of their prey. Eavesdropping is typically studied as dyadic predator-prey species interactions; yet in nature, most predators target multiple prey species and most prey must evade multiple predator species. The impact of predator communities on prey signal evolution is not well understood. Predators could converge in their preferences for conspicuous signal properties, generating competition among predators and natural selection on particular prey signal features. Alternatively, predator species could vary in their preferences for prey signal properties, resulting in sensory-based niche partitioning of prey resources. In the Neotropics, many substrate-gleaning bats use the mate-attraction songs of male katydids to locate them as prey. We studied mechanisms of niche partitioning in four substrate-gleaning bat species and found they are similar in morphology, echolocation signal design and prey-handling ability, but each species preferred different acoustic features of male song in 12 sympatric katydid species. This divergence in predator preference probably contributes to the coexistence of many substrate-gleaning bat species in the Neotropics, and the substantial diversity in the mate-attraction signals of katydids. Our results provide insight into how multiple eavesdropping predator species might influence prey signal evolution through sensory-based niche partitioning.

Silent katydid females are at higher risk of bat predation than acoustically signalling katydid males.

Males that produce conspicuous mate attraction signals are often at high risk of predation from eavesdropping predators. Females of such species typically search for signalling males and their higher motility may also place them at risk. The relative predation risk faced by males and females in the context of mate-finding using long-distance signals has rarely been investigated. In this study, we show, using a combination of diet analysis and behavioural experiments, that katydid females, who do not produce acoustic signals, are at higher risk of predation from a major bat predator, Megaderma spasma, than calling males. Female katydids were represented in much higher numbers than males in the culled remains beneath roosts of M. spasma. Playback experiments using katydid calls revealed that male calls were approached in only about one-third of the trials overall, whereas tethered, flying katydids were always approached and attacked. Our results question the idea that necessary costs of mate-finding, including risk of predation, are higher in signalling males than in searching females.

How male sound pressure level influences phonotaxis in virgin female Jamaican field crickets (Gryllus assimilis).

Understanding female mate preference is important for determining the strength and direction of sexual trait evolution. The sound pressure level (SPL) acoustic signalers use is often an important predictor of mating success because higher sound pressure levels are detectable at greater distances. If females are more attracted to signals produced at higher sound pressure levels, then the potential fitness impacts of signalling at higher sound pressure levels should be elevated beyond what would be expected from detection distance alone. Here we manipulated the sound pressure level of cricket mate attraction signals to determine how female phonotaxis was influenced. We examined female phonotaxis using two common experimental methods: spherical treadmills and open arenas. Both methods showed similar results, with females exhibiting greatest phonotaxis towards loud sound pressure levels relative to the standard signal (69 vs. 60 dB SPL) but showing reduced phonotaxis towards very loud sound pressure level signals relative to the standard (77 vs. 60 dB SPL). Reduced female phonotaxis towards supernormal stimuli may signify an acoustic startle response, an absence of other required sensory cues, or perceived increases in predation risk.

Behavioral and phylogenetic differentiation in a potential cryptic species complex, the canyon treefrog

Detection of genetic and behavioral diversity within morphologically similar species has led to the discovery of cryptic species complexes. We tested the hypothesis that the canyon treefrog (Hyla arenicolor) may consist of cryptic species by examining mate-attraction signals among highly divergent lineages defined by mitochondrial DNA (mtDNA). Unexpectedly, calls exhibited little variation among the three U.S. lineages despite large mtDNA sequence divergences. We re-analyzed intraspecific and interspecific phylogenetic relationships by sequencing both mitochondrial and nuclear genetic markers among populations and a closely related, but morphologically and behaviorally different species, the Arizona treefrog (H. wrightorum). Discordance between mitochondrial and nuclear datasets suggests multiple instances of introgression of H. wrightorum's mitochondrial genome into populations of H. arenicolor. Furthermore, intraspecific population structure based on nuclear markers shows better congruence with patterns of call variation than population structure based on the mitochondrial dataset. Although the U.S. lineages do not appear to represent cryptic species, Mexican lineages do show biologically relevant call differences as assessed through female preference tests. Our results suggest that call variation can indicate genetic structure of populations; however, a multilocus approach should be used in defining genetic structure, as using only mtDNA may lead to erroneous conclusions.

Male Enchenopa treehoppers (Hemiptera: Membracidae) vary mate-searching behavior but not signaling behavior in response to spider silk

Finding and attracting mates can impose costs on males in terms of increased encounters with, and attraction of, predators. To decrease the likelihood of predation, males may modify mate-acquisition efforts in two main ways: they may reduce mate-searching efforts or they may reduce mate-attraction efforts. The specific behavior that males change in the presence of predator cues should depend upon the nature of risk imposed by the type of predator present in the environment. For example, sit-and-wait predators impose greater costs to males moving in search of mates. Here, we test whether cues of the presence of a sit-and-wait predator lead to a reduction in mate-searching but not mate-acquisition behavior. We used a member of the Enchenopa binotata complex of treehoppers-a clade of vibrationally communicating insects in which males fly in search of mates and produce mate-attraction signals when they land on plant stems. We tested for changes in mate-searching and signaling behaviors when silk from a web-building spider was present or absent. We found that males delayed flight when spider silk was present but only if they were actively searching for mates. These results suggest that males have been selected to reduce predation risk by adjusting how they move about their environment according to the cues of sit-and-wait predators.

How age influences phonotaxis in virgin female Jamaican field crickets (Gryllus assimilis)

Female mating preference can be a dominant force shaping the evolution of sexual signals. However, females rarely have consistent mating preferences throughout their lives. Preference flexibility results from complex interactions of predation risk, social and sexual experience, and age. Because residual reproductive value should theoretically decline with age, older females should not be as choosy as younger females. We explored how age influences phonotaxis towards a standard mate attraction signal using a spherical treadmill (trackball) and a no-choice experimental protocol. Female Jamaican field crickets, Gryllus assimilis, were highly variable in their phonotaxis; age explained up to 64% of this variation. Females 10 days post imaginal eclosion and older oriented toward the mate attraction signal, with 10- and 13-day females exhibiting the greatest movement in the direction of the signal. Our study suggests 10- and 13-day old females would be most responsive when quantifying the preference landscape for G. assimilis sexual signals.

Adaptive plasticity in wild field cricket's acoustic signaling.

Phenotypic plasticity can be adaptive when phenotypes are closely matched to changes in the environment. In crickets, rhythmic fluctuations in the biotic and abiotic environment regularly result in diel rhythms in density of sexually active individuals. Given that density strongly influences the intensity of sexual selection, we asked whether crickets exhibit plasticity in signaling behavior that aligns with these rhythmic fluctuations in the socio-sexual environment. We quantified the acoustic mate signaling behavior of wild-caught males of two cricket species, Gryllus veletis and G. pennsylvanicus. Crickets exhibited phenotypically plastic mate signaling behavior, with most males signaling more often and more attractively during the times of day when mating activity is highest in the wild. Most male G. pennsylvanicus chirped more often and louder, with shorter interpulse durations, pulse periods, chirp durations, and interchirp durations, and at slightly higher carrier frequencies during the time of the day that mating activity is highest in the wild. Similarly, most male G. veletis chirped more often, with more pulses per chirp, longer interpulse durations, pulse periods, and chirp durations, shorter interchirp durations, and at lower carrier frequencies during the time of peak mating activity in the wild. Among-male variation in signaling plasticity was high, with some males signaling in an apparently maladaptive manner. Body size explained some of the among-male variation in G. pennsylvanicus plasticity but not G. veletis plasticity. Overall, our findings suggest that crickets exhibit phenotypically plastic mate attraction signals that closely match the fluctuating socio-sexual context they experience.