Abstract  Signalling is a dynamic process that often occurs over brief timescales, particularly in the acoustic modality. Numerous studies of mate choice and acoustic communication have identified signal parameters essential for species recognition and mate preferences, although these studies have rarely considered the dynamic nature of these processes. Here we investigate mate choice behaviour in female túngara frogs, Physalaemus pustulosus, in response to temporally dynamic presentations of male advertisement calls. Our results demonstrate that females are sensitive to the location of preferred call types on a moment-to-moment basis, and that responses are influenced by the continued presence, complexity, sound pressure level and inherent attractiveness of individual male signals. In general, our results support the notion that decision making during mate choice is an open-ended process that is sensitive to interruption and persuasion from competing signallers. We show that for a species in which females actively compare multiple signallers simultaneously, the criterion that predicts the degree of commitment to an initial mate approach is whether there is a state change in the complexity of signals.

Abstract  It is well known that animal decision-making can be influenced by environmental variables, such as the risk of predation. During the breeding season, nocturnal amphibians encounter a range of environmental conditions at breeding aggregations, including variable ambient light conditions. For nocturnal frogs, illumination is expected to minimize conspicuous movement that might increase predator detection. Previous work has shown that female Physalaemus pustulosus (Cope, 1864) (= Engystomops pustulosus (Cope, 1864)) are sensitive to variation in light levels during mate choice. Here we use an acoustic playback design in which stimuli are adjusted for intensity and complexity during female phonotaxis to show that choosiness is influenced by light level. Frogs were more likely to commit to an initial mate choice despite a dynamic reduction in mate attractiveness under dim light conditions compared with darkness. These results suggest that females are trading off the attractiveness of potential mates with the perceived costs of executing mate choice by committing to an initial decision and thereby reducing assessment time and movement. The dynamic playback design used here provides an approach that could be applied in other systems in which context-dependent decision-making is thought to be important.

Abstract  Interest in the question of when and how species recognition and mate preferences emerge in animals with strong species-typical predispositions has faded since the time of the classical ethologists. In its place, the role of plasticity has surfaced as a central emphasis in the study of animal behavior. Here, I step back and examine the origin and execution of sexual behavior in a tropical frog for which auditory predispositions are key. These experiments challenge assumptions about behavioral development, auditory perception, and stereotyped behavior. First, I illustrate when and how a sex- and speciestypical behavior—conspecific phonotaxis—emerges during development. This study demonstrates that phonotaxis, presumably restricted to mature females, is present in both sexes early in postmetamorphic development—potentially long before such behavior might serve an adaptive function. I place this result in the context of hypotheses regarding the development of learned versus non-learned behaviors, and in light of the potential for perception to be altered by physiological changes occurring concomitantly with ontogeny. Next, I describe a set of dynamic mate choice studies that highlight how decision-making in a relatively simple system is more flexible, and less stereotyped, than was previously assumed. Results here show that frogs temporally update their mate choice decisions in a moment-to-moment fashion as advertisement signals change in real time. By decomposing the decision-making process, I determine the stimulus parameters essential for commitment to an initial phonotactic approach. These studies are followed up by experiments that reveal a high level of individual variation in female choosiness during mate choice. Lastly, I describe a mate choice study that revealed categorical perception in frogs, the first “lower” vertebrate now known to exhibit a perceptual mode previously considered a hallmark of “higher” organisms. Collectively, I make the following arguments: (1) constraints on sensory systems play a larger role in shaping behavior than is generally appreciated, irrespective of the involvement of learning; (2) unstudied sources of variation may contribute significantly to the raw material for sexual selection; and (3) phonotaxis in anurans amphibians is not the simple, stereotyped behavior that has been suggested of it in the past.

Abstract  Mate choice studies most often examine female preferences based on population responses, thus potentially overlooking individual differences in behavior. Moreover, such studies typically use invariant stimulus conditions to infer preferences. By using population responses and static stimulus presentations, it is difficult to thoroughly understand the complexity of the mate choice process, including variation present between individuals. Here, we investigated phonotactic mate choice behavior in female tungara frogs (Physalaemus pustulosus) in response to temporally dynamic presentations of male advertisement calls. We tested females on repeated trials to examine individual differences and found considerable variation in the extent to which females update their mate choice decisions. Females in our study were bimodally distributed and thus broadly classified as either committed or uncommitted to an initial mate approach. We compared body condition measures of females differing behaviorally and determined that females with larger residual body masses were more committed to initial mate choices than less massive individuals, despite the fact that all females were in reproductive condition and field collected in amplexus. Our results suggest that anuran phonotaxis, once considered to be a highly stereotyped behavior, is more complex and variable than previously thought.

Abstract  We investigated the natural dynamics in a sexual signal that combines different call components and explored the role of call complexity in sexual selection using a neotropical frog. Male túngara frogs, Physalaemus pustulosus, facultatively add up to seven short, multiharmonic components (chucks) to the simple form of their calls (whines). Female túngara frogs are preferentially attracted to whines with chucks over whines without chucks, and males also call more in response to calls containing chucks. Because acoustic predators prefer complex calls, in the context of simple (no chucks) versus complex (any number of chucks) calls, the variably complex call appears to have evolved in response to the opposing selective forces of natural and sexual selection. There is no evidence, however, for the function of increasing the number of chucks within complex calls. We tested two aspects of increasing call complexity: natural patterns of use of call types in males and how both sexes respond to variation in multi-chuck calls. Males incrementally change call complexity by the addition or subtraction of a single chuck and usually do not produce more than two chucks. Variation in call complexity, for calls with at least one chuck, does not influence response calling in males or phonotaxis in females. Our results suggest that one reason for not increasing call complexity beyond a single chuck is the diminishing effectiveness on the responses of both sexes.

Abstract  Categorical perception is common in humans, but it is not known whether animals perceive continuous variation in their own multidimensional social signals categorically. There are two components to categorical perception: labeling and discrimination. In the first, continuously variable stimuli on each side of a category boundary are labeled. In the second, there is strong discrimination between stimuli from opposite sides of the boundary, whereas stimuli on the same side of the boundary are not discriminated. Here, we show that female tu´ ngara frogs respond categorically to complex mating calls that vary simultaneously along multiple dimensions and are within the natural range of signal variation. In response to a transect of synthetic stimuli that varied continuously and systematically in seven dimensions, female tu´ ngara frogs label mating calls as either conspecific or not conspecific. For pairs of stimuli that differed by the same magnitude, females discriminate those in different categories but not those in the same category. In addition, latency to respond was significantly shorter when stimuli were in the same versus different categories. Because responses to mating calls are critical in generating species recognition and sexual selection, this finding has implications for both animal perception and the influences of mate choice on the tempo and mode of evolution.

Abstract  Stable carbon isotope analyses have shown that South African australopiths did not have exclusively frugivorous diets, but also consumed significant quantities of C4 foods such as grasses, sedges, or animals that ate these foods. Yet, these studies have had significant limitations. For example, hominin sample sizes were relatively small, leading some to question the veracity of the claim for australopith C4 consumption. In addition, it has been difficult to determine which C4 resources were actually utilized, which is at least partially due to a lack of stable isotope data on some purported australopith foods. Here we begin to address these lacunae by presenting carbon isotope data for 14 new hominin specimens, as well as for two potential C4 foods (termites and sedges). The new data confirm that non-C3 foods were heavily utilized by australopiths, making up about 40% and 35% of Australopithecus and Paranthropus diets respectively. Most termites in the savanna-woodland biome of the Kruger National Park, South Africa, have intermediate carbon isotope compositions indicating mixed C3/C4 diets. Only 28% of the sedges in Kruger were C4, and few if any had well-developed rhizomes and tubers that make some sedges attractive foods. We conclude that although termites and sedges might have contributed to the C4 signal in South African australopiths, other C4 foods were also important. Lastly, we suggest that the consumption of C4 foods is a fundamental hominin trait that, along with bipedalism, allowed australopiths to pioneer increasingly open and seasonal environments.

Abstract  Modern theories of learned vocal behaviours, such as human speech and singing in songbirds1 , posit that acoustic communication signals are reproduced from memory, using auditory feedback2 . The nature of these memories, however, is unclear. Here we propose and test a model for how complex song structure can emerge from sparse sequence information acquired during tutoring. In this conceptual model, a population of combination-sensitive (phrase-pair) detectors is shaped by early exposure to song and serves as the minimal representation of the template necessary for generating complete song. As predicted by the model, birds that were tutored with only pairs of normally adjacent song phrases were able to assemble full songs in which phrases were placed in the correct order; birds that were tutored with reverse-ordered phrase pairs sang songs with reversed phrase order. Birds that were tutored with all song phrases, but presented singly, failed to produce normal, full songs. These findings provide the first evidence for a minimal requirement of sequence information in the acoustic model that can give rise to correct song structure.

Also see the News & Views article for this study by Daniel Margoliash.