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.     

FEMALES ARE CHOOSIER IN THE DARK: ENVIRONMENT‐DEPENDENT RELIANCE ON COURTSHIP COMPONENTS AND ITS IMPACT ON FITNESS

A broad understanding of multimodal courtship function necessitates knowledge of the potential information content of signal components, the efficacy of signal components in eliciting the appropriate receiver response, and the fitness consequences of mating decisions based upon various signal components. We present data addressing each of these requirements for the multimodal‐signaling wolf spider, Schizocosa floridana Bryant. Using diet manipulations, we first demonstrate that both visual and seismic courtship signals are condition‐dependent. Next, using high‐ and low‐quantity diet individuals in mate choice trials across manipulated signaling environments, we demonstrate that the seismic signal is crucial for mating success and further show that female choosiness is environment‐dependent. Females mated more with high diet males only in the absence of visual signals, showing no discrimination in the presence of visual signals. Finally, by quantifying the number of offspring produced by our mated females, we reveal that a female's mating environment, in conjunction with her potential resource availability, influences her fitness—in environments in which females exerted choice, heavier females produced more offspring. Together, this comprehensive set of experiments demonstrates that female choosiness varies across environments, leading to direct fitness consequences.     

Why do ovigerous females approach courting males? Female preferences and sensory biases in a fiddler crab

Perceptual biases explain the origin and evolution of female preference in many species. Some responses that mediate mate choice, however, may have never been used in nonmating contexts. In the fiddler crab, Uca mjoebergi, mate‐searching females prefer faster wave rates and leading wave; however, it remains unclear whether such responses evolved in a mating context (i.e., the preference has effect on the fitness of the female and her offspring that arise from mating with a particular male) or a nonmating contexts (i.e., a female obtains direct benefits through selecting the male with a more detectable trait). Here, we compared the preferences of mate‐searching with those of ovigerous females that are searching for a burrow and do not concern about male “quality.” Results showed that as both mate‐searching and ovigerous females preferentially approached robotic males with faster wave rates. This suggests that wave rate increases detectability/locatability of males, but the mating preference for this trait is unlikely to evolve in the mating context (although it may currently function in mate choice), as it does not provide fitness‐related benefit to females or her offspring. Wave leadership, in contract, was attractive to mate‐searching females, but not ovigerous females, suggesting that female preference for leadership evolves because wave leadership conveys information about male quality. We provide not only an empirical evidence of sensory biases (in terms of the preference for faster wave), but the first experimental evidence that mating context can be the only selection force that mediates the evolution of male sexual traits and female preference (in terms of the preference for leading wave).     

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.     

The Structure of Bonobo Copulation Calls During Reproductive and Non‐Reproductive Sex

Copulation calls in primates are usually identified as sexually selected signals that promote the reproductive success of the caller. In this study, we investigated the acoustic structure of copulation calls in bonobos (Pan paniscus), a great ape known for its heightened socio‐sexuality. Throughout their cycles, females engage in sexual relations with both males and other females and produce copulation calls with both partners. We found that calls produced during sexual interactions with male and female partners could not be reliably distinguished in terms of their acoustic structure, despite major differences in mating behaviour and social context. Call structure was equally unaffected by the size of a female’s sexual swelling and by the rank of her mating partner. Rank of the partner did affect call delivery although only with male, but not female partners. The only strong effect on call structure was because of caller identity, suggesting that these signals primarily function to broadcast individual identity during sexual interactions. This primarily social use of an evolved reproductive signal is consistent with a broader trend seen in this species, namely a transition of sexual behaviour to social functions.     

Acoustic Preference of Frog‐Biting Midges (Corethrella spp) Attacking Túngara Frogs in their Natural Habitat

In many animals, males aggregate to produce mating signals that attract conspecific females. These leks, however, also attract eavesdropping predators and parasites lured by the mating signal. This study investigates the acoustic preferences of eavesdroppers attracted to natural choruses in a Neotropical frog, the túngara frog (Engystomops pustulosus). In particular, we examined the responses of frog‐biting midges to natural variation in call properties and signaling rates of males in the chorus. These midges use the mating calls of the frogs to localize them and obtain a blood meal. Although it is known that the midges prefer complex over simple túngara frog calls, it is unclear how these eavesdroppers respond to natural call variation when confronted with multiple males in a chorus. We investigated the acoustic preference of the midges using calling frogs in their natural environment and thus accounted for natural variation in their call properties. We performed field recordings using a sound imaging system to quantify the temporal call properties of males in small choruses. During these recordings, we also collected frog‐biting midges attacking calling males. Our results revealed that, in a given chorus, male frogs calling at higher rates and with higher call complexity attracted a larger number of frog‐biting midges. Call rate was particularly important at increasing the number of midges attracted when males produced calls of lower complexity. Similarly, call complexity increased attractiveness to the midges especially when males produced calls at a low repetition rate. Given that female túngara frogs prefer calls produced at higher repetition rates and higher complexity, this study highlights the challenge faced by signalers when increasing attractiveness of the signal to their intended receivers.     

Size‐Dependent Male Mate Preference and its Association with Size‐Assortative Mating in a Mangrove Snail,Littoraria ardouiniana

In many animals, body size plays a crucial role in mating success in the context of competition and preference for mates. Increasing evidence has shown that male mate preference can be size‐dependent and, therefore, an important driver of size‐assortative mating. To test this theory, mate choice experiments were performed during the three consecutive stages of mating behaviour, namely trail following, shell mounting and copulation, in the dioecious mangrove snail, Littoraria ardouiniana. These experiments identified two possible forms of size‐dependent male mate preference which could contribute to the formation of size‐assortative mating in these snails. Firstly, whereas small males were unselective, large males were selective and preferred to follow mucus trails laid by large females. Alternatively, the results can also be interpreted as all males were selective and adopted a mating strategy of selecting females similar to, or larger than, their own sizes. Both small and large males also copulated for longer with large than with small females, and this was more pronounced in large males. When two males encountered a female, they engaged in physical aggression, with the larger male excluding the smaller male from copulating with the female. This study, therefore, demonstrated that size‐dependent male mate preference may, along with male–male competition, play an important role in driving size‐assortative mating in these mangrove snails, and this may also be the case in other species that exhibit male mate choice.     

Female House Wrens may Use a Low‐Amplitude Call as an Aggressive Signal

The majority of work on aggressive signaling has focused on male–male contests. Although females in many species compete over important resources, female signals are understudied. In house wrens (Troglodytes aedon), females compete with other females to protect nesting cavities and eggs. We suggest that a high‐pitched, low‐amplitude call, hereafter abbreviated as ‘HI’, may be an aggressive signal used by female house wrens. Using playback of simulated female intruders, we found that females used HI calls significantly more often during playback of female house wrens compared to playback of heterospecifics. Additionally, HI calls were given significantly more often in the minute preceding physical attack. In comparison, song rates did not predict future attacks. Finally, we present pilot data that suggest listening females may respond more aggressively to female playback containing HI calls compared to playback containing only songs. This suggests the reliability of HI calls could be maintained by a receiver retaliation rule. HI calls bear a striking resemblance to the low‐amplitude songs of many male songbirds, in terms of both acoustic structure and social context. This is one of the few reports of a putative low‐amplitude aggressive signal in a female songbird. However, the nature of female competition may make low‐amplitude signaling an underappreciated signaling form in female animals.     

Male–male interactions and male mating success in the leafhopper Aphrodes makarovi

In mating systems based on substrate‐borne vibrations, sexual communication often involves a reciprocal exchange of species‐ and sex‐specific vibrational signals and male is searching for a stationary female. In the leafhopper Aphrodes makarovi, female reply is essential for successful location of the female and its variable duration directly affects male's costs associated with signalling and searching. We studied male and female behaviour in a trio situation (two males and one female), and our results show that male–male competition had important effects on male mating success. Females replied equally to advertisement calls emitted by the winning and losing males and mated with the first male that located them, regardless of his investment in calling effort. Males eavesdropped to male–female duet maintained by the rival, and the winners were better at exploiting female replies to the rival's advertisement calls by silently approaching the female. To interfere with the ongoing male–female duet, males also emitted masking signals overlapping the latter part of the female reply. More overlapped female replies were registered in response to the losers and masking signals most likely delay the rival in reaching the female. Our study shows that a comprehensive understanding of male mating success and female preferences in vibrational duetting systems requires also investigations in more complex settings that more realistically represent the situation in nature.     

SPECIES RECOGNITION AND SEXUAL SELECTION AS A UNITARY PROBLEM IN ANIMAL COMMUNICATION

We investigated patterns of mating call preference and mating call recognition by examining phonotaxis of female túngara frogs, Physalaemus pustulosus, in response to conspecific and heterospecific calls. There are four results: females always prefer conspecific calls; most heterospecific calls do not elicit phonotaxis; some heterospecific calls do elicit phonotaxis and thus are effective mate recognition signals; and females prefer conspecific calls to which a component of a heterospecific call has been added to a normal conspecific call. We use these data to illustrate how concepts of species recognition and sexual selection can be understood in a unitary framework by comparing the distribution of signal traits to female preference functions.     

Mate choice in the predaceous mite Phytoseiulus persimilis: evidence of self‐referent phenotype matching?

Close inbreeding may have negative fitness effects. Consequently, organisms have evolved various mechanisms, which enable them to avoid close inbreeding. In no‐choice and choice experiments we assessed whether the predaceous mite Phytoseiulus persimilis Athias‐Henriot (Acari: Phytoseiidae) avoids close inbreeding by kin recognition. No‐choice experiments demonstrated that virgin females more readily accept unrelated males than they accept related ones, which suggests a female preference for unrelated mates. Because each female had been reared in isolation prior to experiments, females most likely imprinted on themselves, and later used self‐referent phenotype matching to assess potential mating partners. In contrast, neither female nor male choice experiments indicated a preference. Analyses of female and male behavior revealed that in choice experiments, female preference for unrelated males was probably confounded by male competition and/or altered by the different ecological context posed by choice experiments.     

Long‐distance signals influence assessment of close range mating displays in the field cricket,Gryllus integer

Male sexual displays often include components detected across long distances, and those perceived only at close range. Understanding what information females gain from each component of a complex display and how they use these signals to make decisions are questions of major interest in sexual selection research. We evaluated content‐based hypotheses (‘redundant signals’ and ‘multiple messages’) for the courtship displays of field crickets (Gryllus integer) by measuring female responses to males' long‐distance calling song (calls) and close‐range chemical cues. Females' responses to a male's calls and chemical cues were uncorrelated, supporting the ‘multiple messages’ hypothesis. We also tested the ‘inter‐signal interaction’ hypothesis by investigating how long‐distance calls influence evaluation of close‐range courtship. The relationship between long‐ and close‐range signals was complex and conditional: females accepted close‐range courtship more quickly after exposure to attractive calling song than they did after exposure to either unattractive calling song or silence, and unattractive calls were no more or less effective than silence. This inter‐signal interaction could affect our understanding of mate choice in species with multiple mating signals because it implies that females may save time and energy by not assessing the close‐range signals of attractive long‐distance signalers. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 856–865.     

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.     

COSTLY SIGNALS IN A FIELD CRICKET CAN INDICATE HIGH‐ OR LOW‐QUALITY DIRECT BENEFITS DEPENDING UPON THE ENVIRONMENT

The handicap hypothesis proposes that male signals provide reliable information to females because only males of high condition provide high‐quality mating benefits and can afford the costs of producing attractive signals. In the context of direct benefits, the handicap hypothesis predicts that benefit quality and signal attractiveness will positively covary among genotypes, positively covary among environments, or be affected by congruent genotype–environment interactions. The latter should occur if the relative condition of a genotype is environment‐dependent. We tested these predictions in the variable field cricket, Gryllus lineaticeps. An interaction between male family and nutritional environment affected the expression of a costly signal preferred by females, while only male family affected direct benefit quality. These noncongruent effects of family and nutritional environment are inconsistent with the handicap hypothesis, and appear to have resulted from variation among nutritional environments in the relationship between signal attractiveness and benefit quality. Surprisingly, signal attractiveness was positively correlated with benefit quality when males experienced a low nutrition environment but negatively correlated with benefit quality when males experienced a high nutrition environment. As a result, female choice for direct benefits may be difficult, particularly in heterogeneous environments, unless females can assess the environmental histories of males.     

Context‐ and State‐Dependent Male Mate Choice in a Sexually Cannibalistic Spider

High male mating investment may favor selection on male mate choice particularly if females vary in quality. Terminal investment strategies constitute a maximal mating effort and have evolved independently in the absence of paternal investment in several spider taxa including the genus Argiope. To test for male mate preferences in the above context, we used the sexually cannibalistic spider A. bruennichi. We varied male state (mating status and post‐maturation age) as well as the competitive context and quantified male mate choice decisions between females of different states and developmental stages in binary choice tests. We found an overall adaptive preference for the virgin against the mated female regardless of male mating state. Furthermore, we demonstrated that older males paid more attention to female fecundity‐related traits than to mating status. In a second set of experiments, we offered males a choice between a virgin and a subadult female and varied the competitive context which had no effect on male decisions. Curiously, a preference for the virgin adult female was only apparent after exclusion of females that matured <3 d prior to the test. Repeated tests of males supported the hypothesis that males do not distinguish between a freshly matured virgin female and a subadult female. Our results show that male spiders execute mate choice based on information collected from female silk strands and that they integrate their own state into mating decisions.     

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

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

Melodic males and flashy females: Geographic variation in male and female reproductive behavior in red‐eyed treefrogs (Agalychnis callidryas)

Geographic variation in courtship behavior can affect reproductive success of divergent phenotypes via mate choice. Over time, this can lead to reproductive isolation and ultimately to speciation. The Neotropical red‐eyed treefrog (Agalychnis callidryas) exhibits high levels of phenotypic variation among populations in Costa Rica and Panama, including differences in color pattern, body size, and skin peptides. To test the extent of behavioral premating isolation among differentiated populations, we quantified male advertisement calls from six sites and female responses to male stimuli (acoustic and visual signals) from four sites. Our results show that both male advertisement calls and female behavior vary among populations: Discriminant function analyses can predict the population of origin for 99.3% ± 0.7 of males based on male call (dominant frequency and bandwidth) and 76.1% ± 6.6 of females based on female response behavior (frequency and duration of visual displays). Further, female mate choice trials (n = 69) showed that population divergence in male signals is coupled with female preference for local male stimuli. Combined, these results suggest that evolved differences among populations in male call properties and female response signals could have consequences for reproductive isolation. Finally, population variation in male and female behavior was not well explained by geographic or genetic distance, indicating a role for localized selection and/or drift. The interplay between male courtship and female responses may facilitate the evolution of local variants in courtship style, thus accelerating premating isolation via assortative mating.     

Preference for Male Traits Differ in Two Female Morphs of the Tree Lizard,Urosaurus ornatus

Non-random female mating preferences may contribute to the maintenance of phenotypic variation in color polymorphic species. However, the effect of female preference depends on the types of male traits used as signals by receptive females. If preference signals derive from discrete male traits (i.e., morph-specific), female preferences may rapidly fix to a morph. However, female preference signals may also include condition-dependent male traits. In this scenario, female preference may differ depending on the social context (i.e., male morph availability). Male tree lizards (Urosaurus ornatus) exhibit a dewlap color polymorphism that covaries with mating behavior. Blue morph males are aggressive and defend territories, yellow males are less aggressive and defend smaller territories, and orange males are typically nomadic. Female U. ornatus are also polymorphic in dewlap color, but the covariation between dewlap color and female behavior is unknown. We performed an experiment to determine how female mate choice depends on the visual and chemical signals produced by males. We also tested whether female morphs differ in their preferences for these signals. Female preferences involved both male dewlap color and size of the ventral color patch. However, the female morphs responded to these signals differently and depended on the choice between the types of male morphs. Our experiment revealed that females may be capable of distinguishing among the male morphs using chemical signals alone. Yellow females exhibit preferences based on both chemical and visual signals, which may be a strategy to avoid ultra-dominant males. In contrast, orange females may prefer dominant males. We conclude that female U. ornatus morphs differ in mating behavior. Our findings also provide evidence for a chemical polymorphism among male lizards in femoral pore secretions.     

Mate choice and sexual conflict in <Emphasis Type="Italic">Brachionus plicatilis</Emphasis> (Rotifera)

Male mate choice in Brachionus plicatilis is based on information from coronal receptors and contact chemoreception of a glycoprotein signal on the body surface of females. Male mating behavior is modulated by mating signal quality and strength, which determines male mating persistence and circling intensity. We probe the sensory abilities of males by better resolving their discrimination of female age. Males preferentially initiate mating with young females, but not too young. Males circle 0.2 h old females just hatched from resting eggs only about 1/2 as frequently as 12 h old females. Males are even more discriminating of females with whom they copulate, preferring 3 h old females significantly more than 0.2 h or 6 h old females. In contrast, males cannot distinguish between virgin females and those who have already copulated. Similarly, males circled and copulated with females hatching from resting eggs with equal frequency as those hatching from amictic eggs. The counterpoint to male mate choice is female resistance to mating. When males contact females, the females respond with one of four behaviors: no response, acceleration, foot flipping, or coronal retraction. In 65% of male–female encounters, there was no initial response by females. However, when males began circling females, females accelerated 11.1 times more often than when males were absent. The second type of evasive female behavior was foot-flipping, which tends to knock off males attempting to circle the female. In the presence of circling males, females performed foot-flipping behavior three times more often than in the absence of males. Coronal retraction, where they stop swimming and withdraw their corona, was observed less frequently than acceleration or foot-flipping, and there was no difference in the presence or absence of males. These data are interpreted in the context of sexual conflict, where the behaviors that optimize male and female fitness differ. Guest editors: S. S. S. Sarma, R. D. Gulati, R. L. Wallace, S. Nandini, H. J. Dumont & R. Rico-Martínez Advances in Rotifer Research     

Male vocalization and female choice in the hybridogenetic Rana lessonae/Rana esculenta complex

In many species, females can improve their fitness by preferring particular males over others. In Palaearctic water frogs of the Rana lessonae/R. esculenta complex the consequences of such mate choice are particularly pronounced. To produce viable offspring, the hybrid R. esculenta (genotype RL) must mate with the parental species R. lessonae (LL); but R. lessonae should avoid mating with R. esculenta, because the resulting hybrid offspring will eliminate the L genome from the germline (hybridogenesis). Hence, there exists a conflict between the sexual parasite (RL) and its sexual host (LL) over the best mating partner. Previous studies have shown a preference for LL males in LL and RL females; but they have also shown that females cannot usually realize their choice when in close proximity to males, because the males forcefully and indiscriminately amplex them. We tested whether females use male vocalizations as a long-distance signal to increase their chances of mating with the preferred LL males. We exposed female R. lessonae and R. esculenta to playbacks of single LL and RL mating calls (experiment 1) and to choruses with a 3:1 excess of LL and RL calls, respectively (experiment 2). In experiment 1, both female types were attracted more by the LL than by the RL calls. In experiment 2, no discrimination between LL- and RL-dominated choruses was observed. The results suggest that females do not use distant male vocalization to approach preferentially ponds or arenas within a pond that hold an excess of LL males. But once they have arrived in a chorus, mating calls from nearby males can direct them to the preferred LL mates. We discuss possible reasons for the failure to discriminate between choruses and the chances for successful choice between individuals within choruses. Copyright 2000 The Association for the Study of Animal Behaviour.