Simulated Predation Risk Influences Female Choice in Túngara Frogs,Physalaemus pustulosus

While the presence of predators can influence female mate choice, few studies have investigated how females respond to quantitative variation in predation risk. In addition, we know little of how females respond to multiple, independent cues of risk. In this study, we investigated the effects of simulated predation risk on mate choice in túngara frogs, Physalaemus pustulosus, using the advertisement calls of predatory frogs, variation in ambient light, and simulated distance. Females showed aversion to conspecific calls associated with the calls of predators, and females were significantly less likely to travel perceived longer distances while the calls of predatory frogs were broadcast. In both the laboratory and field, females chose among potential mates significantly faster under higher light levels. Female responses to acoustic cues of predation risk were significantly influenced by light level, but decisions about travel distances were not. These results demonstrate that female choice is strongly influenced by perceived predation risk and that females can simultaneously evaluate quantitative variation in different cues of predation risk. The changes in search behavior and mate evaluation we demonstrate indicate that predation plays a strong role in limiting signal evolution and possibly reproductive isolation.     

Localization Error and Search Costs during Mate Choice in Túngara Frogs,Physalaemus pustulosus

Search costs can have profound influences on female choice, causing females to become less choosy or sample less of the diversity of available mates. Predator foraging strategies, however, determine exactly how search time affects predator encounter rates. Ambush predators are more likely to be encountered by females traveling longer distances to evaluate males, but evaluation time is unlikely to influence encounter‐rate with this type of predator. Actively searching predators, however, may be more likely to be encountered by females employing longer travel times and evaluation times. In this study, we examine the effects of perceived search costs on both temporal and spatial aspects of the search behavior of female túngara frogs, Physalaemus pustulosus. Females were collected from natural choruses and presented with conspecific calls at a distance of 50, 115, or 180 cm from their release point. Assays were conducted in either darkness or simulated full moon light levels. Longer starting distances caused longer choice latencies, but choice latency was considerably lowered under higher light conditions. Females spent considerably less time moving under higher light conditions; however, light levels did not affect path length. Females were more likely to leave the release point with more accurate orientation to the sound source under higher light conditions. We demonstrate that females can respond to perceived search costs by altering spatial and temporal aspects of female search behavior. The overall emphasis of females on reducing time spent moving and increasing movement speed indicates that predation by actively searching predators represents a stronger cost to females than ambush predators.     

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

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

Sexual Differences in the Behavioral Response of Túngara Frogs, Physalaemus pustulosus, to Cues Associated with Increased Predation Risk

Engaging in mating behaviors usually increases exposure to predators for both males and females. Anti‐predator strategies during reproduction may have important fitness consequences for prey. Previous studies have shown that individuals of several species adjust their reproductive behavior according to their assessment of predation risk, but few studies have explored potential sexual differences in these strategies. In this study, we investigate whether the acoustic cues associated with predatory attacks or those associated with predators themselves affect the mating behavior of female and male túngara frogs, Physalaemus pustulosus. We compared the responses of females approaching a mate and those of calling males when exposed to mating calls associated with sounds representing increased hazard. When presented with mating calls that differed only in whether or not they were followed by a predation‐related sound, females preferentially approached the call without predation‐related sounds. In contrast to females, calling males showed greater vocal response to calls associated with increased risk than to a call by itself. We found significant differences in the responses of females and males to several sounds associated with increased hazard. Females behaved more cautiously than males, suggesting that the sexes balance the risk of predation and the cost of cautious mating strategies differently.     

The mixed-species chorus as public information: tungara frogs eavesdrop on a heterospecific

Multispecies choruses represent a promising but uninvestigatedforum for public information. Although frogs exposed to a potentialpredator call more readily in the presence of conspecific callsthan in their absence, none are known to make comparable useof heterospecific calls. To test for heterospecific eavesdropping,we isolated calling male túngara frogs (Physalaemus pustulosus),presented them with a potential predator, and recorded theirresponses to playbacks of 1 of 4 stimuli: calls of a conspecific,a sympatric heterospecific (Leptodactylus labialis), an allopatriccongener (Physalaemus enesefae), or silence. We found that malescalled more in response to the L. labialis call than to eitherthe silent stimulus or the P. enesefae call. In contrast, theP. enesefae call did not result in significantly more callingthan the silent stimulus. The conspecific call was the mosteffective at promoting calling. The data indicate that túngarafrogs selectively attend to the call of a heterospecific. Wehypothesize that such heterospecific eavesdropping contributesto the emergent behavior of mixed-species choruses.     

Choosing a Mate in a Cocktail Party‐Like Situation: The Effect of Call Complexity and Call Timing between Two Rival Males on Female Mating Preferences in the Túngara Frog Physalaemus pustulosus

Signal detection, recognition, and localization are hampered when multiple signalers coincide in time and space, a problem known as ‘cocktail party effect’. In many taxa, senders utter complex calls consisting of two or more elements which often vary in the ease with which they can be assessed in different signaling environments. Receivers’ selective attention to different cues may increase the probability of correctly assigning a signal to its source (localization) in face of conspecific interference. Túngara frogs, Physalaemus pustulosus, produce complex calls consisting of an initial whine, followed by zero up to seven broad‐banded, amplitude‐modulated chucks. Under ideal conditions (without interference or noise), females prefer whines followed by chucks over whines alone, but the preference is not linear; females do not discriminate between whines with one or two chucks. When whines lack chucks, call overlap elicits random responses in females, with no preference for leading calls. In this study, I explored the combined effect of call timing and call complexity on female preferences in a two‐choice paradigm—a simplification of the cocktail party scenario. I tested the hypothesis that the effect of call overlap can be reduced when the calls of one of the two rivals have chucks, specifically more chucks than those of the rival. I gave females a choice between whines alone and with chucks (one or two) presented at three time relations (alternated, abutted, and partially overlapped) and two emission orders (whine with less chucks leading and whine with more chucks leading). I found that the preference for one chuck over no chuck was preserved in all the experimental treatments, but when a w + 2chk preceded a w + chk, either overlapped or abutted, a preference existed for the whine with more chucks. Therefore, an interaction between call order and the number of chucks was obtained. The results only partially supported the hypothesis, and call order emerges as an opportunistic component of signaling in P. pustulosus.     

Trade-off in short- and long-distance communication in tungara (Physalaemus pustulosus) and cricket (Acris crepitans) frogs

Female phonotaxis in túngara (Physalaemus pustulosus)and cricket (Acris crepitans) frogs is biased toward male advertisementcalls or call components of lower frequency. This behavioralbias might result in part from a mismatch between the spectralcharacteristics of the advertisement call and the most sensitive frequencyof the peripheral end organ implicated in reception of thesesounds. In both species, females are tuned to frequencies lowerthan average for the calls in their population. This mismatch,however, represents the situation during short-distance communication.Female frogs can also use the call to detect choruses at longdistances, and the spectral distribution of call energy canvary with transmission distance. We used computer simulationsto test the hypothesis that there is a better match betweentuning and call spectral energy at long distances from the callingmale than at short distances by comparing the performance (soundenergy received) of the natural tuning curve relative to anoptimal tuning curve (i.e., one centered at the call's dominantfrequency). The relative performance of the natural tuning curveincreased with distance in túngara frogs. For the twosubspecies of cricket frogs, however, the relative performancedecreased at longer distances. The performance did not equalthe optimal tuning curve at the distances tested. The resultsindicate that the relationship between calls and auditory tuningcannot be optimal for both long and short distance reception.The relationship between female tuning and call dominant frequencymay represent a compromise between short and long distance communication,and the bias toward short or long distances may vary among species.     

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.     

Carotenoid‐based bill coloration functions as a social,not sexual,signal in songbirds (Aves: Passeriformes)

Many animals use coloration to communicate with other individuals. Although the signalling role of avian plumage colour is relatively well studied, there has been much less research on coloration in avian bare parts. However, bare parts could be highly informative signals as they can show rapid changes in coloration. We measured bill colour (a ubiquitous bare part) in over 1600 passerine species and tested whether interspecific variation in carotenoid‐based coloration is consistent with signalling to potential mates or signalling to potential rivals in a competitive context. Our results suggest that carotenoid bill coloration primarily evolved as a signal of dominance, as this type of coloration is more common in species that live in social groups in the nonbreeding season, and species that nest in colonies; two socio‐ecological conditions that promote frequent agonistic interactions with numerous and/or unfamiliar individuals. Additionally, our study suggests that carotenoid bill coloration is independent of the intensity of past sexual selection, as it is not related to either sexual dichromatism or sexual size dimorphism. These results pose a significant challenge to the conventional view that carotenoid‐based avian coloration has evolved as a developmentally costly, condition‐dependent sexual signal. We also suggest that bare part ornamentation may often signal different information than plumage ornaments.     

Bumpus in the snake den: effects of sex, size, and body condition on mortality of red-sided garter snakes

Huge breeding aggregations of red-sided garter snakes (Thamnophis sirtalis parietalis) at overwintering dens in Manitoba provide a unique opportunity to identify sources of mortality and to clarify factors that influence a snake's vulnerability to these factors. Comparisons of sexes, body sizes, and body condition of more than 1000 dead snakes versus live animals sampled at the same time reveal significant biases. Three primary sources of mortality were identified. Predation by crows, Corvus brachyrhynchos (590 snakes killed), was focussed mostly on small snakes of both sexes. Crows generally removed the snake's liver and left the carcass, but very small snakes were sometimes brought back to the nest. Suffocation beneath massive piles of other snakes within the den (301 dead animals) involved mostly small males and (to a lesser extent) large females; snakes in poor body condition were particularly vulnerable. Many emaciated snakes (n = 142, mostly females) also died without overt injuries, probably due to depleted energy reserves. These biases in vulnerability are readily interpretable from information on behavioral ecology of the snakes. For example, sex biases in mortality reflect differences in postemergence behavior and locomotor capacity, the greater attractiveness of larger females to males, and the high energy costs of reproduction for females.     

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

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

No evidence of sexual dimorphism in the tails of the swallowtail butterflies Papilio machaon gorganus and P. m. britannicus

The European swallowtail butterfly (Papilio machaon) is so named, because of the long and narrow prominences extending from the trailing edge of their hindwings and, although not a true tail, they are referred to as such. Despite being a defining feature, an unequivocal function for the tails is yet to be determined, with predator avoidance (diverting an attack from the rest of the body), and enhancement of aerodynamic performance suggested. The swallowtail, however, is sexually size dimorphic with females larger than males, but whether the tail is also sexually dimorphic is unknown. Here, museum specimens were used to determine whether sexual selection has played a role in the evolution of the swallowtail butterfly tails in a similar way to that seen in the tail streamers of the barn swallow (Hirundo rustica), where the males have longer streamers than those of the females. Previously identified sexual dimorphism in swallowtail butterfly size was replicated, but no evidence for dimorphism in tail length was found. If evolved to mimic antennae and a head to divert a predatory attack, and if an absolute tail size was the most effective for this, then the tail would probably be invariant with butterfly hindwing size. The slope of the relationship between tail length and size, however, although close to zero, was nonetheless statistically significantly above (tail length ∝ hindwing area ^{0.107 ± 0.011}). The slope also did not equate to that expected for geometric similarity (tail length ∝ hindwing area^1/2) suggesting that tail morphology is not solely driven by aerodynamics. It seems likely then, that tail morphology is primarily determined by, and perhaps a compromise of several, factors associated with predator avoidance (e.g. false head mimicry and a startling function). Of course, experimental data are required to confirm this.     

Variation of the advertisement call of Physalaemus centralis Bokermann, 1962 (Anura: Leptodactylidae) in the Cerrado of central Brazil

Acoustic signals are employed to support the correct designation of species and enables the discrimination between individuals. We analyzed both intra and interindividual variability of the advertisement call of Physalaemus centralis on the basis of specimens recorded in eight localities of the Cerrado in central Brazil. Within-individual variation, most of the call parameters were static properties. Both spectral and temporal call properties were dynamic between individuals. All call proprieties varied more between individuals than within an individual. Our study adds important data for future studies on the taxonomy and phylogeny of the P. cuvieri clade.     

Sex‐specific responses to territorial intrusions in a communication network: Evidence from radio‐tagged great tits

Signals play a key role in the ecology and evolution of animal populations, influencing processes such as sexual selection and conflict resolution. In many species, sexually selected signals have a dual function: attracting mates and repelling rivals. Yet, to what extent males and females under natural conditions differentially respond to such signals remains poorly understood, due to a lack of field studies that simultaneously track both sexes. Using a novel spatial tracking system, we tested whether or not the spatial behavior of male and female great tits (Parus major) changes in relation to the vocal response of a territorial male neighbor to an intruder. We tracked the spatial behavior of male and female great tits (N = 44), 1 hr before and 1 hr after simulating territory intrusions, employing automatized Encounternet radio‐tracking technology. We recorded the spatial and vocal response of the challenged males and quantified attraction and repulsion of neighboring males and females to the intrusion site. We additionally quantified the direct proximity network of the challenged male. The strength of a male's vocal response to an intruder induced sex‐dependent movements in the neighborhood, via female attraction and male repulsion. Stronger vocal responders were older and in better body condition. The proximity networks of the male vocal responders, including the number of sex‐dependent connections and average time spent with connections, however, did not change directly following the intrusion. The effects on neighbor movements suggest that the strength of a male's vocal response can provide relevant social information to both the males and the females in the neighborhood, resulting in both sexes adjusting their spatial behavior in contrasting ways, while the social proximity network remained stable. This study underlines the importance of “silent” eavesdroppers within communication networks for studying the dual functioning and evolution of sexually selected signals.     

Predation‐associated divergence of male genital morphology in a livebearing fish

Male genital morphology is remarkably diverse across internally fertilizing animals, a phenomenon largely attributed to sexual selection. Ecological differences across environments can alter the context of sexual selection, yet little research has addressed how this may influence the rapid, divergent evolution of male genitalia. Using the model system of Bahamas mosquitofish (Gambusia hubbsi) undergoing ecological speciation across blue holes, we used geometric morphometric methods to test (i) whether male genital shape (the small, approximately 1 mm long, distal tip of the sperm‐transfer organ, the gonopodium) has diverged between populations with and without predatory fish and (ii) whether any observed divergence has a genetic basis. We additionally examined the effects of genetic relatedness and employed model selection to investigate other environmental factors (i.e. interspecific competition, adult sex ratio and resource availability) that could potentially influence genital shape via changes in sexual selection. Predation regime comprised the most important factor associated with male genital divergence in this system, although sex ratio and some aspects of resource availability had suggestive effects. We found consistent, heritable differences in male genital morphology between predation regimes: Bahamas mosquitofish coexisting with predatory fish possessed more elongate genital tips with reduced soft tissue compared with counterparts inhabiting blue holes without predatory fish. We suggest this may reflect selection for greater efficiency of sperm transfer and fertilization during rapid and often forced copulations in high‐predation populations or differences in sexual conflict between predation regimes. Our study highlights the potential importance of ecological variation, particularly predation risk, in indirectly generating genital diversity.     

Effects of an invasive species on refuge‐site selection by native fauna: The impact of cane toads on native frogs in the Australian tropics

Invasive species can induce shifts in habitat use by native taxa: either by modifying habitat availability, or by repelling or attracting native species to the vicinity of the invader. The ongoing invasion of cane toads (Rhinella marina) through tropical Australia might affect native frogs by affecting refuge‐site availability, because both frogs and toads frequently shelter by day in burrows. Our laboratory and field studies in the wet‐dry tropics show that native frogs of at least three species (Litoria tornieri, Litoria nasuta and Litoria dahlii) preferentially aggregate with conspecifics, and with (some) other species of native frogs. However, the frogs rarely aggregated with cane toads either in outdoor arenas or in standardized experimental burrows that we monitored in the field. The native frogs that we tested either avoided burrows containing cane toads (or cane toad scent) or else ignored the stimulus (i.e. treated such a burrow in the same way as they did an empty burrow). Native frogs selected a highly non‐random suite of burrows as diurnal retreat sites, whereas cane toads were less selective. Hence, even in the absence of toads, frogs do not use many of the burrows that are suitable for toads. The invasion of cane toads through tropical Australia is unlikely to have had a major impact on retreat‐site availability for native frogs.     

The evolution of partial reproductive isolation as an adaptive optimum

Decades of theoretical work on the evolution of adaptive prezygotic isolation have led to an interesting finding—namely that stable partial reproductive isolation is a relatively common outcome. This conclusion is generally lost, however, in the desire to pinpoint when exactly speciation occurs. Here, we argue that the evolution of partial reproductive isolation is of great interest in its own right and matches empirical findings that ongoing hybridization is taxonomically widespread. We present the mechanisms by which partial reproductive isolation can be a stable evolutionary endpoint, concentrating on insights from theoretical studies. We focus not on cases in which hybridization results from constraints imposed by ongoing migration or mutation, but on the intriguing idea that partial reproductive isolation may instead be an adaptive optimum. We identify three general categories of selective mechanisms that can lead to partial reproductive isolation: context-dependent hybrid advantage, indirect selection due to the varying actions of sexual selection in different geographic contexts, and a balance of costs of choosiness with indirect selection for stronger mating preferences. By any of these mechanisms, stable partial reproductive isolation can potentially provide a robust evolutionary alternative to either complete speciation or population fusion.