Male Mating Signals Research Articles

Can you hear/see me? Multisensory integration of signals does not always facilitate mate choice

Abstract Females of many species choose mates using multiple sensory modalities. Multimodal noise may arise, however, in dense aggregations of animals communicating via multiple sensory modalities. Some evidence suggests multimodal signals may not always improve receiver decision-making performance. When sensory systems process input from multimodal signal sources, multimodal noise may arise and potentially complicate decision-making due to the demands on cognitive integration tasks. We tested female túngara frog, Physalaemus (=Engystomops) pustulosus, responses to male mating signals in noise from multiple sensory modalities (acoustic and visual). Noise treatments were partitioned into three categories: acoustic, visual, and multimodal. We used natural calls from conspecifics and heterospecifics for acoustic noise. Robotic frogs were employed as either visual signal components (synchronous vocal sac inflation with call) or visual noise (asynchronous vocal sac inflation with call). Females expressed a preference for the typically more attractive call in the presence of unimodal noise. However, during multimodal signal and noise treatments (robofrogs employed with background noise), females failed to express a preference for the typically attractive call in the presence of conspecific chorus noise. We found that social context and temporal synchrony of multimodal signaling components are important for multimodal communication. Our results demonstrate that multimodal signals have the potential to increase the complexity of the sensory scene and reduce the efficacy of female decision making.

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.

Divergence in Potential Contact Pheromones and Genital Morphology Among Sympatric Song Types of the Bush Cricket Mecopoda elongata

A well-established route to speciation in animals is via the evolution of divergent male mating signals and female preferences within a species. However, an open question is how common it is for near complete isolation to be achieved through a single signal-receiver system or whether multiple aspects of the mate-recognition system diverge simultaneously. The five highly divergent song types of the bush cricket Mecopoda elongata, exemplify reproductive isolation in sympatry through long-distance mating signals. Female preference for their own song type has been established as a strong pre-mating reproductive barrier, but the potential existence of additional isolating mechanisms has not been investigated. We quantify divergence in cuticular lipid profiles and external genital structures between song types. These traits show significant divergence among species of Orthoptera and are known to be used in mate recognition following contact. We show that divergence among sympatric Mecopoda song types in both cuticular lipid profiles and two external genital structures is sufficiently extensive that either of them can be used to identify individual song type with 90% accuracy. Our findings suggest that multiple isolating mechanisms are likely to evolve simultaneously to facilitate a more robust reproductive isolation. This indicates a role for sexual selection in the divergence and potential future speciation of these populations and suggests that reproductive isolation may frequently evolve through simultaneous divergence across different aspects of mate recognition systems.

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.

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.

Insect mating signal and mate preference phenotypes covary among host plant genotypes.

Sexual selection acting on small initial differences in mating signals and mate preferences can enhance signal-preference codivergence and reproductive isolation during speciation. However, the origin of initial differences in sexual traits remains unclear. We asked whether biotic environments, a source of variation in sexual traits, may provide a general solution to this problem. Specifically, we asked whether genetic variation in biotic environments provided by host plants can result in signal-preference phenotypic covariance in a host-specific, plant-feeding insect. We used a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess patterns of variation in male mating signals and female mate preferences induced by genetic variation in host plants. We employed a novel implementation of a quantitative genetics method, rearing field-collected treehoppers on a sample of naturally occurring replicated host plant clone lines. We found remarkably high signal-preference covariance among host plant genotypes. Thus, genetic variation in biotic environments influences the sexual phenotypes of organisms living on those environments in a way that promotes assortative mating among environments. This consequence arises from conditions likely to be common in nature (phenotypic plasticity and variation in biotic environments). It therefore offers a general answer to how divergent sexual selection may begin.

The evolutionary consequences of disrupted male mating signals: an agent-based modelling exploration of endocrine disrupting chemicals in the guppy.

Females may select a mate based on signalling traits that are believed to accurately correlate with heritable aspects of male quality. Anthropogenic actions, in particular chemicals released into the environment, are now disrupting the accuracy of mating signals to convey information about male quality. The long-term prediction for disrupted mating signals is most commonly loss of female preference. Yet, this prediction has rarely been tested using quantitative models. We use agent-based models to explore the effects of rapid disruption of mating signals. In our model, a gene determines survival. Males signal their level of genetic quality via a signal trait, which females use to select a mate. We allowed this system of sexual selection to become established, before introducing a disruption between the male signal trait and quality, which was similar in nature to that induced by exogenous chemicals. Finally, we assessed the capacity of the system to recover from this disruption. We found that within a relatively short time frame, disruption of mating signals led to a lasting loss of female preference. Decreases in mean viability at the population-level were also observed, because sexual-selection acting against newly arising deleterious mutations was relaxed. The ability of the population to recover from disrupted mating signals was strongly influenced by the mechanisms that promoted or maintained genetic diversity in traits under sexual selection. Our simple model demonstrates that environmental perturbations to the accuracy of male mating signals can result in a long-term loss of female preference for those signals within a few generations. What is more, the loss of this preference can have knock-on consequences for mean population fitness.

Effects of early auditory experience on the development of local song preference in female swamp sparrows

A growing number of studies show that learning about male mating signals can shape the way females discriminate among males and may influence the evolution of both female preferences and the male traits under selection. Female songbirds commonly prefer local songs over foreign songs from a different population. In some species, however, the extent of variation among songs sung by different males within a population is as great as the variation observed between populations, raising the question of how females are able to discriminate local from foreign songs. Here, we report that laboratory-reared female swamp sparrows (Melospiza georgiana) not only show a preference for the particular song types with which they were tutored as compared with both foreign songs and unfamiliar local songs but also show preference for unfamiliar local songs over unfamiliar foreign songs. An acoustic analysis comparing tutor songs and those presented as unfamiliar local and foreign songs suggests that female swamp sparrows might be attuned to the specifics of local note phonology when assessing the attractiveness of unfamiliar songs. Our results demonstrate that early auditory experience influences response to geographic song variation in female swamp sparrows, and suggest the possibility that female songbirds may generalize what they learn from songs early in life to novel songs heard in adulthood. Additional work is needed to evaluate the contribution of unlearned predispositions for local song.

Trees to treehoppers: genetic variation in host plants contributes to variation in the mating signals of a plant‐feeding insect

Community genetics research has demonstrated 'bottom-up' effects of genetic variation within a plant species in shaping the larger community with which it interacts, such as compositions of arthropod faunas. We demonstrate that such cross-trophic interactions also influence sexually selected traits. We used a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to ask whether male mating signals are influenced by host plant genetic variation. We reared a random sample of the treehoppers on potted replicates of a sample of host plant clone lines. We found that treehopper male signals varied according to the clone line on which they developed, showing that genetic variation in host plants affects male treehoppers' behavioural phenotypes. This is the first demonstration of cross-trophic indirect genetic effects on a sexually selected trait. We discuss how such effects may play an important role in the maintenance of variation and within-population phenotypic differentiation, thereby promoting evolutionary divergence.

Why is birdsong so repetitive? Signal detection and the evolution of avian singing modes

Signal repertoires, such as the song type repertoires of many songbirds, are thought to play a role in male mating success, with females preferring larger male repertoires over smaller ones. Yet, in many songbird species, males sing in a way that does not readily reveal their repertoire sizes by repeating each song type multiple times before switching to the next. Here I describe a potential explanation for such signal redundancy, based on the predictions of signal detection theory as it applies to intersexual communication during mate choice. According to this idea, a female’s response threshold to male mating signals (i.e., her ‘choosiness’) should select for male signal features that elicit favorable female responses (i.e., that are more ‘detectable’). Males can increase the detectability of their signals by producing them with higher redundancy, as well as by increasing their intensity and distinctiveness. Thus, in species with relatively high female response thresholds to males, such as taxa in which the sexes associate only briefly during breeding, males are expected to produce mate attraction signals that are especially stereotyped and repetitive. High signal stereotypy is also expected to be associated with features within signals that are relatively extravagant. Phylogenetic studies of a songbird group with a wide range of mating patterns, the oropendolas and caciques (family Icteridae), provide evidence consistent with these evolutionary predictions. Singing modes in this group have become more repetitive in some lineages along with the evolution of polygynous mating systems, even as various features within songs have become more extravagant.

Environmentally realistic exposure to the herbicide atrazine alters some sexually selected traits in male guppies.

Male mating signals, including ornaments and courtship displays, and other sexually selected traits, like male-male aggression, are largely controlled by sex hormones. Environmental pollutants, notably endocrine disrupting compounds, can interfere with the proper functioning of hormones, thereby impacting the expression of hormonally regulated traits. Atrazine, one of the most widely used herbicides, can alter sex hormone levels in exposed animals. I tested the effects of environmentally relevant atrazine exposures on mating signals and behaviors in male guppies, a sexually dimorphic freshwater fish. Prolonged atrazine exposure reduced the expression of two honest signals: the area of orange spots (ornaments) and the number of courtship displays performed. Atrazine exposure also reduced aggression towards competing males in the context of mate competition. In the wild, exposure levels vary among individuals because of differential distribution of the pollutants across habitats; hence, differently impacted males often compete for the same mates. Disrupted mating signals can reduce reproductive success as females avoid mating with perceptibly suboptimal males. Less aggressive males are at a competitive disadvantage and lose access to females. This study highlights the effects of atrazine on ecologically relevant mating signals and behaviors in exposed wildlife. Altered reproductive traits have important implications for population dynamics, evolutionary patterns, and conservation of wildlife species.

Male red ornamentation is associated with female red sensitivity in sticklebacks.

Sexual selection theory proposes correlated evolutionary changes in mating preferences and secondary sexual characters based on a positive genetic correlation between preference and the preferred trait. Empirical work has provided support for a genetic covariation between female preference and male attractiveness in several taxa. Here, we study parent and offspring visual traits in threespine sticklebacks, Gasterosteus aculeatus. While focusing on the proximate basis of mating preferences, we compare the red breeding coloration of males, which strongly contributes to female choice, with their daughters' red sensitivity measured by optomotor response thresholds. We show that the red color expression of fathers correlates well with their daughters' red sensitivity. Given that a within-population genetic correlation between signal and preference was experimentally confirmed for the red coloration in sticklebacks, our results indicate a proximate mechanism in terms of perceptual sensitivity being involved in the co-evolution of female preferences and male mating signals.

Endocrine disruption of male mating signals: ecological and evolutionary implications

Summary 1. Endocrine disrupting chemicals (EDCs) are chemicals that interfere with proper hormonal functioning in exposed animals. They enter the natural environment through multiple sources, and many non-target wildlife species are exposed to them via several modes. Exposure causes altered hormone levels, importantly gonadal hormones, resulting in changed reproductive characteristics. 2. Vertebrate male mating signals convey important mate quality information to females. These signals are dependent on androgens for their production and maintenance. Female responses to signals depend on oestrogens. Disrupting these pathways jeopardizes signal production and reception, which has implications for mating system ecology. 3. Besides affecting various aspects of the vertebrate physiology, EDCs can impair hormonal functioning by binding to or blocking hormone receptors, or by altering production and function of hormones or hormone receptors. 4. We consider the ecological implications of multi-generational signal disruption by EDCs. Altered signals can influence population dynamics and sex ratios; local extinctions are possible. Community-level dynamics may be affected via interspecific dependence on signals or population fluctuations. 5. We then address the evolutionary effects of EDC-altered male mating signals in vertebrates and discuss how females may respond to altered signals over evolutionary time. Trans-generational reduction in signal reliability can lead to reduced preference and eventual loss of the signal trait and to the evolution of new traits as signals of mate quality. Genetic divergence between endocrine disrupted and undisrupted populations may result, perhaps giving rise to speciation. 6. Finally, we recommend areas of research to further explore some of the issues addressed in this review. We suggest field surveys to document existing alterations in mating systems and genetic divergence in endocrine disrupted populations. Long-term mesocosm studies and mathematical models would be useful to predict the fate of mating signals and female responses as a result of prolonged endocrine disruption. EDCs have been the focus of ecotoxicology for some time now, and we feel that this analysis should now enter the realm of evolutionary biology to determine the subtle, yet far-reaching effects on exposed non-target wildlife.

INTRASPECIFIC REPRODUCTIVE CHARACTER DISPLACEMENT IN A POLYMORPHIC POISON DART FROG, DENDROBATES PUMILIO

Divergence in male mating signals and associated female preferences is often an important step in the process of speciation. Reproductive character displacement, the pattern of greater divergence of male signals and/or female preference in sympatry than in allopatry, has been observed in a variety of taxa with different degrees of postzygotic isolation. A number of selective processes, including reinforcement, have been proposed to cause such a pattern. Cases in which reproductive character displacement occurs among intraspecific variants are especially informative for understanding how selection acting within a species can lead to the evolution of reproductive barriers and speciation. This study tested the hypothesis that female strawberry poison dart frogs (Dendrobates pumilio) in polymorphic populations of the Bocas del Toro archipelago of Panama show stronger mating discrimination than do females from monomorphic populations, exhibiting an intraspecific pattern of reproductive character displacement. Our results contribute important insights into understanding selection's role in generating the striking diversity of Bocas del Toro's D. pumilio and provide a snapshot of what could be the early stages of reproductive isolation and speciation.

Neural Activity Patterns in Response to Interspecific and Intraspecific Variation in Mating Calls in the Túngara Frog

BackgroundDuring mate choice, individuals must classify potential mates according to species identity and relative attractiveness. In many species, females do so by evaluating variation in the signals produced by males. Male túngara frogs (Physalaemus pustulosus) can produce single note calls (whines) and multi-note calls (whine-chucks). While the whine alone is sufficient for species recognition, females greatly prefer the whine-chuck when given a choice.Methodology/Principal FindingsTo better understand how the brain responds to variation in male mating signals, we mapped neural activity patterns evoked by interspecific and intraspecific variation in mating calls in túngara frogs by measuring expression of egr-1. We predicted that egr-1 responses to conspecific calls would identify brain regions that are potentially important for species recognition and that at least some of those brain regions would vary in their egr-1 responses to mating calls that vary in attractiveness. We measured egr-1 in the auditory brainstem and its forebrain targets and found that conspecific whine-chucks elicited greater egr-1 expression than heterospecific whines in all but three regions. We found no evidence that preferred whine-chuck calls elicited greater egr-1 expression than conspecific whines in any of eleven brain regions examined, in contrast to predictions that mating preferences in túngara frogs emerge from greater responses in the auditory system.ConclusionsAlthough selectivity for species-specific signals is apparent throughout the túngara frog brain, further studies are necessary to elucidate how neural activity patterns vary with the attractiveness of conspecific mating calls.

Experimental manipulation of the rearing environment influences adult female zebra finch song preferences

In songbirds, sensory and social learning processes in juveniles contribute to variation in male song and female preferences. The developmental stress hypothesis proposes that suboptimal early development affects the costly brain structures involved in male song learning and, as a consequence, song quality. As an extension of this hypothesis we tested in this study whether developmental conditions also modulate female song preference acquisition. We tested song preferences in adult female zebra finches, Taeniopygia guttata, originating from a brood size manipulation experiment that had induced differences in mass, condition, immune response and levels of plasma testosterone at the early nestling stage. During the song-learning phase, juvenile birds were housed in small mixed-treatment groups with unrelated adult male song tutors. Adult females' song preferences were tested in an operant set-up where females could trigger different song playbacks by pecking different response keys. When females could choose between their own and an unfamiliar tutor's song they preferred their tutors' songs independent of experimental brood size. However, when females chose between two unfamiliar songs there was a significant effect of experimental brood size on preference strength: females from small broods showed significantly stronger preferences than those from medium and large broods. Hence, both females' rearing environment and sensory learning processes appear to contribute to variation in the direction and strength of female preference for male mating signals.

Age-related changes in an insect mating signal have no effect on female choice

The structure of male mating signals is often influenced by age. The causes and consequences of age-based signal variation have been much studied in visual, acoustic, and chemical signaling modalities, but are less explored in species that use vibrational signals for mate attraction. However, the complex structure of many vibrational signals makes them ideal for investigating the relationships between age, signal variation, and patterns of female choice. In the thornbug treehopper, Umbonia crassicornis, females mate more often with older males, but the mechanism underlying older male mating success is unknown. Our goals in this study were to determine whether male vibrational mate advertisement signals vary with age, and, if so, whether females prefer the signals of older males. We recorded male signals over four consecutive weeks beginning at the onset of signaling (a period spanning most of the male reproductive lifespan), and measured ten temporal, spectral, and energy-related parameters from each signal. Several features of male signals changed markedly with age. However, females responded similarly to signals representing males of different ages, indicating that they do not favor older males on the basis of long distance mate advertisement signals. Nonetheless, the results reveal that even in short-lived, determinate growth species age can have surprisingly large effects on mating signals, and we discuss some factors that may contribute to age-related signal variability in U. crassicornis.

Preferred songs predict preferred males: consistency and repeatability of zebra finch females across three test contexts

Male mating signals are often multidimensional, potentially providing multiple messages to females. However, the relative importance of different signal dimensions and their context dependency are poorly understood. Even in a well-studied species such as the zebra finch, Taeniopygia guttata , an important avian model for the study of mate choice, there is little consensus on the relative weighting of visual versus acoustic signals in mate choice. We therefore tested the consistency and repeatability of female mating preferences across different test contexts, presenting male song only or full courtship displays. We concurrently conducted a detailed analysis of male song characteristics and morphological traits. Females' individual preferences were consistent across three commonly used binary test paradigms (operant and phonotaxis tests with songs and association tests with live males). Preference direction was thus independent of test contexts. Preference strength was repeatable only between the operant and live male tests, possibly because these two tests allowed active interaction with songs or males whereas exposure to songs in the phonotaxis test was passive. The song structure parameters that predicted female preferences best were context independent and also predicted male morphology. We conclude from the combined results that song structure (in addition to song rate or absolute output as previously suggested) does contain sufficient information on the singer for female mate choice. We suggest that the earlier focus on song rate rather than song content might partly account for the differences between studies in the importance attributed to acoustic versus visual signals.

Assortative preferences and discrimination by females against hybrid male song in the grasshoppers Chorthippus brunneus and Chorthippus jacobsi (Orthoptera: Acrididae)

The grasshoppers Chorthippus brunneus and Chorthippus jacobsi are highly differentiated for male mating signals, and form a mosaic hybrid zone in northern Spain. At some sites within this zone, many hybrids are observed. At others, few hybrids are observed. Such bimodal sites may reflect recent contacts between parental genotypes, or local variation in levels of assortative mating or selection against hybrids. Playback of 12 parental and F1 male songs to 296 parental and hybrid females revealed positive assortative preferences in C. brunneus and C. jacobsi females, supporting a direct role of male mating signals in female choice. However, all female genotypic classes showed reduced responsiveness to F1 male songs. Such sexual selection against hybrids is consistent with the narrow cline width observed in the field for song characters relative to morphology. These results have implications for the genetic structure of the hybrid zone and for models of speciation by reinforcement.

SEXUAL SELECTION IN FEMALE PERCEPTUAL SPACE: HOW FEMALE TÚNGARA FROGS PERCEIVE AND RESPOND TO COMPLEX POPULATION VARIATION IN ACOUSTIC MATING SIGNALS

Female preferences for male mating signals are often evaluated on single parameters in isolation or small suites of characters. Most signals, however, are composites of many individual parameters. In this study we quantified multivariate traits in the advertisement call of the túngara frog, Physalaemus pustulosus. We represented the calls in multidimensional scaling space and chose nine test calls to represent the range of population variation. We then tested females for phonotactic preference between calls in each pair of the nine test calls. We used statistics developed for paired comparisons in such “round robin” competitions to evaluate the null hypothesis of equal attractiveness, and to examine the degree to which females responded to calls as being different from or similar to one another in attractiveness. We then examined the attractiveness of each test call relative to all other test calls as a function of their location in multivariate acoustic space (the acoustic landscape) to visualize sexual selection on calls. Finally, we used methods from cognitive psychology to illustrate the females' perception of call attractiveness in multivariate space, and compared this perceptual landscape to the acoustic landscape of quantitative call variation.We show that correlations between individual call characters are not strong and thus there are few biomechanical constraints on their independent evolution. Most call variables differed among males, and there was high repeatability of call characters within males. Females often discriminated between pairs of calls from the population, and there were significant differences among calls in their attractiveness. Female preferences for calls were not stabilizing. The region of the acoustic landscape that was most attractive to females included the mean call but was not centered around it. The females' perceptual or preference landscape did not correlate with the call's acoustic landscape, and female perception of calls decreased rather than enhanced call differences.