Patterns of mating call preferences in túngara frogs, Physalaemus pustulosus.

We examine acoustic mating preferences of a focal population at four different scales of divergence: within the population, between populations in the same genetic group, between populations in different genetic groups and between different species. At all scales there is substantial genetic divergence, variation in mating signals and preferences are influenced by signal variation. There is, however, no support for the hypothesis that mating preferences accumulate predictably with genetic distance. Females preferred the local conspecific call to the foreign conspecific call in about one-third of the experiments, and preferred the local call to all of the heterospecific calls tested. But there was no significant relationship between the variation in the strength of preference and genetic distance either among conspecific populations, or among heterospecific species. Thus, in this study macroevolutionary patterns are not apparent at the microevolutionary scale.

Animal communication: complex call production in the túngara frog.

Animals' sound-producing organs often act as an integrated whole--particular vocal structure are not directly associated with the creation of discrete syllables. But here we show that the 'chuck' of the 'whine-chuck' mating call of the túngara frog, Physalaemus pustulosus, is caused by a fibrous mass attached to the vocal folds; the chuck is eliminated by removal of this structure, although the frog still tries to produce the sound. Sexual selection affects the acoustic complexity of the frog's call, so evolution may have shaped this unusual vocalization, which is akin to the two-voiced song of songbirds.

Vestigial preference functions in neural networks and túngara frogs.

Although there is a growing interest in understanding how perceptual mechanisms influence behavioral evolution, few studies have addressed how perception itself is shaped by evolutionary forces. We used a combination of artificial neural network models and behavioral experiments to investigate how evolutionary history influenced the perceptual processes used in mate choice by female túngara frogs. We manipulated the evolutionary history of artificial neural network models and observed an emergent bias toward calls resembling known ancestral states. We then probed female túngara frogs for similar preferences, finding strong biases toward stimuli that resemble a call hypothesized for a recent ancestor. The data strongly suggest that female túngara frogs exhibit vestigial preferences for ancestral calls, and provide a general strategy for exploring the role of historical contingency in perceptual biases.

How evolutionary history shapes recognition mechanisms.

Evolutionary psychologists have emphasized the importance of natural selection in shaping cognitive functions, but historical contingency has not received direct study. This is crucial because in response to selection, complex traits tend to be fine-tuned or jury-rigged rather than totally reconstructed. We hypothesize that the neural and cognitive strategies an animal employs in signal recognition are influenced by the strategies used by its ancestors. The responses of female túngara frogs to ancestral calls and to calls of other closely related species are influenced by history. By training artificial neural networks with a series of calls that mimic the species' past history of call evolution or various control histories, we have shown that only networks that evolved through the mimetic history predict the response biases of túngara frogs.

Evolution of calls and auditory tuning in the Physalaemus pustulosus species group.

In species within the Physalaemus pustulosus species group, male frogs produce a whine-like advertisement call consisting of a frequency sweep typically descending from 1,000 to 400 Hz (depending on the species). One species, Physalaemus pustulosus, the túngara frog, has evolved a second call syllable, the chuck, which males place after their whine. Most energy in the chuck is above 1,500 Hz and peaks at 2,400 Hz. We investigated whether the evolution of this new call component in P. pustulosus coincided with evolution of auditory tuning. We used multiunit electrophysiological recordings of auditory-evoked activity in the midbrain to characterize auditory tuning in Physalaemus pustulosus, four other Physalaemus species within the P. pustulosus clade, and three additional, closely related Physalaemus species as outgroups. All eight species had similar sensitivity profiles, with a broad area of enhanced sensitivity from 100 to 1,100 Hz, which we presume represents amphibian papilla (AP) tuning, and a second, narrower area of enhanced sensitivity centered above 2,100 Hz, which we presume represents basilar papilla (BP) tuning. For all species, the whine stimulates the AP. The P. pustulosus chuck stimulates the BP. The frequency with greatest AP sensitivity differed significantly among species. Although in all cases the AP peak lay within the frequency sweep of the whine, phylogenetically corrected correlations revealed no significant relationships between AP tuning and any spectral feature of the whine. BP tuning was similar among all species, with mean BP best excitatory frequencies (BEFs) around 2,100-2,200 Hz, with the exception of P. pustulatus, with a mean BP BEF of 2,549 Hz. Physalaemus pustulosus, the only investigated species that produces a call component stimulating the BP, had a BP BEF that was not significantly different from any of the species within its clade except P. pustulatus, or from any of the outgroup species. A phylogenetic reconstruction of ancestral BP tuning confirms that the only point of evolutionary change in BP tuning is in the line of descent leading to P. pustulatus, not in the line leading to P. pustulosus despite this being the species using the BP for communication. The results indicate that BP tuning around 2,200 Hz is a conserved trait in the Physalaemus pustulosus species group and that no evolution of BP tuning accompanied the subsequent evolution of the call component (the chuck) that stimulates it. This supports the sensory exploitation idea, which posits that signals evolve to match preexisting features of receiver systems.

Effects of inter-pond distance on the breeding ecology of tungara frogs.

Habitat and resource distributions can influence the movement and aggregation of individuals and thus have important effects on breeding behavior and ecology. Though amphibians have been model systems for the study of breeding behavior and sexual selection, most studies have examined breeding behavior within a single pond. As a result, little is known about how inter-pond distance affects breeding amphibians. We studied the effects of inter-pond distance on the breeding ecology of the tungara frog, Physalaemus pustulosus, in replicated pond arrays in which distance was varied from 0 to 50 m. We predicted that male site fidelity and male aggregation within arrays would increase with inter-pond distance, and that the opportunity for mate choice and oviposition site selectivity by females would decrease with the distance between ponds. Male site fidelity did increase with inter-pond distance. However, male aggregation decreased with distance, such that males tended to be more evenly spaced among ponds when ponds were farther apart. The opportunity for mate choice by females, measured as the number of males within the phonotactic radius of females, also decreased with inter-pond distance. Each of these three responses was consistent with a threshold effect between 5 m and 10 m in inter-pond distance. This threshold corresponded to the maximum distance at which females in laboratory choice experiments exhibited phonotaxis toward the "whine" call of a tungara male, suggesting that phonotactic limits may play an important role in tungara movements and spacing patterns. The distribution of egg masses among ponds, a potential correlate of oviposition site selectivity, did not vary with inter-pond distance. Multiple egg masses deposited on the same night were significantly overdispersed in all distance treatments, implying that females may select oviposition sites to avoid conspecific egg masses over distances of at least 50 m. Collectively, these results demonstrate that inter-pond distance may indeed affect amphibian breeding and movement behavior, and that consideration of multiple habitat patches and their spatial distributions can provide new insights into even the most well-understood mating systems.

Phylogeny of frogs of the Physalaemus pustulosus species group, with an examination of data incongruence.

Characters derived from advertisement calls, morphology, allozymes, and the sequences of the small subunit of the mitochondrial ribosomal gene (12S) and the cytochrome oxidase I (COI) mitochondrial gene were used to estimate the phylogeny of frogs of the Physalaemus pustulosus group (Leptodactylidae). The combinability of these data partitions was assessed in several ways: measures of phylogenetic signal, character support for trees, congruence of tree topologies, compatibility of data partitions with suboptimal trees, and homogeneity of data partitions. Combined parsimony analysis of all data equally weighted yielded the same tree as the 12S partition analyzed under parsimony and maximum likelihood. The COI, allozyme, and morphology partitions were generally congruent and compatible with the tree derived from combined data. The call data were significantly different from all other partitions, whether considered in terms of tree topology alone, partition homogeneity, or compatibility of data with trees derived from other partitions. The lack of effect of the call data on the topology of the combined tree is probably due to the small number of call characters. The general incongruence of the call data with other data partitions is consistent with the idea that the advertisement calls of this group of frogs are under strong sexual selection.

Elastic structures in the vocalization apparatus of the Túngara frog Physalaemus pustulosus (Leptodactylidae).

Histological analysis of the vocal sac and body wall in the leptodactylid frog Physalaemus pustulosus suggests that both muscle and elastic fibers are important in call production. Abdominal musculature as well as abdominal bands of elastin (the lineae masculinae) provide the energy required for exhalation and sound production. Air flowing through the larynx inflates a highly extensible vocal sac lined with muscle and a network of elastic fibers. Inherent elasticity together with muscular activity of the vocal sac likely increase the speed and possibly decrease the energetic costs of lung reinflation following vocalization. The mechanics of call production in P. pustulosus thus involve not only laryngeal activation but also elastic transfer of air between the supralaryngeal vocal sac and abdominal respiratory structures.

Sexual dimorphism and species differences in the neurophysiology and morphology of the acoustic communication system of two neotropical hylids.

We examined auditory tuning and the morphology of the anatomical structures underlying acoustic communication in female Hyla microcephala and H. ebraccata and compared our findings to data from a previous study (Wilczynski et al. 1993) in which we showed species differences in the traits that in males relate to differences in the species-typical calls. Female species differences in the best excitatory frequency (BEF) of the basilar papilla (BP) were similar to the differences seen in males, and females had a significantly lower BEF in H. ebraccata, but not H. microcephala. In both species, females had lower BP thresholds. Snout-vent length, head width, and tympanic membrane diameters were sexually dimorphic in both species and larger in females, whereas laryngeal components were sexually dimorphic and larger in males. Middle and inner ear volumes were not sexually dimorphic. Despite the significant species differences in laryngeal morphology seen in males, female larynges are not significantly different. Furthermore, the interaction of species and sex differences resulted in significantly different degrees of sex dimorphism in the species, particularly for the larynx, which is more sexually dimorphic in H. microcephala, and measures of body size, which are more dimorphic in H. ebraccata.

Female responses to ancestral advertisement calls in tungara frogs.

Phylogenetic techniques were used to estimate and reconstruct advertisement calls at ancestral nodes. These calls were used to investigate the degree of preference of female túngara frogs (Physalaemus pustulosus) for both extant and ancestral calls. Females did not discriminate between calls of males of their own species and calls at their most recent ancestral node. They also recognized calls of three extant species and at four ancestral nodes as the signals of appropriate mates. Both shared ancestral history, and call convergence might differentially influence call preferences.

Acoustic, auditory, and morphological divergence in three species of neotropical frog.

Advertisement calls, auditory tuning, and larynx and ear morphology were examined in 3 neotropical frogs, Hyla microcephala, H. phlebodes and H. ebraccata, H. microcephala has the highest call dominant frequency (6.068 kHz) and basilar papilla tuning (5.36 kHz). H. phlebodes and H. ebraccata calls have lower dominant frequencies (3.832 and 3.197 kHz respectively) and basilar papilla tuning (2.79 and 2.56 kHz). The primary call notes of H. ebraccata are longer (181.6 ms) than those of H. microcephala (95.5 ms) or H. phlebodes (87.3 ms). Morphometric analysis suggests that temporal call features differ as laryngeal musculature changes, in the process changing the overall size of the larynx. The spectral aspects of the call differ as head size, and hence the size of its resonating and radiating structures, changes, modifying the dominant frequency of calls by accentuating their higher harmonics when head size decreases. Decreasing head size decreases the size of the middle and inner ear chambers, changing the mechanical tuning of the ear in the same direction as the change in dominant frequency. These changes result in divergent spectral-temporal characteristics of both the sending and receiving portions of the acoustic communication system underlying social behavior in these frogs.

Sexual selection for sensory exploitation in the frog Physalaemus pustulosus.

The sensory bases of species and population mate preferences are well known; in frogs properties of the female auditory system influence such preferences. By contrast, there is little understanding of how sensory characteristics could result in sexual selection within a population. One possible mechanism is that females are more sensitive to male courtship signals that deviate from the population mean. We document this mechanism in the frog Physalaemus pustulosus. Female basilar papilla tuning is biased toward lower-than-average frequencies in the 'chuck' portion of the male's call, explaining female preference for the lower-frequency chucks produced by larger males. The tuning does not differ between P. pustulosus and its close relative P. coloradorum, a species in which males never evolved the ability to produce chucks; thus the female tuning evolved before the chuck and therefore the chuck played no role in the evolution of the preference. This allows us to reject two popular hypotheses for the evolution of this female preference (runaway sexual selection and natural selection) in favour of a third: sexual selection for sensory exploitation.

Crocodiles don't focus underwater.

Crocodilians are amphibious reptiles which hunt prey both on land and in water. Previous refractive and anatomical studies have suggested that their eyes can focus objects in air and that their ability to refocus the eye underwater may be limited. Examination of the plane of focus of six species of crocodilians both in air and underwater has revealed that they are generally well focused in air for distant targets and severely defocused underwater. These results suggest that sensory systems other than vision must play an important role in prey capture underwater.

Social behavior in hatchling green iguanas: life at a reptile rookery.

Hatchling green iguanas (Iguana iguana) emerge from the ground in small groups in a communal nesting area on a small Panamanian islet and engage in complex social interactions. Iguanas from different clutches often join together before and during departure from the nest site. They also usually move around the islet and migrate from it to the larger adjacent landmass in social groups. These and other observations indicate that the sophistication of saurian social organization and neonate behavior has been underestimated.