Walter Wilczynski

AUDITORY TUNING AND CALL FREQUENCY PREDICT POPULATION-BASED MATING PREFERENCES IN THE CRICKET FROG, ACRIS CREPITANS

We examined frequency tuning of the females peripheral auditory system, the dominant frequency of the males mating call, and population-based mating preferences in cricket frogs (Acris crepitans) to determine how the relationship between the mean call frequency and mean frequency sensitivity of the females auditory system determines such preferences. Females could exhibit preferences for either local calls or foreign calls. In all instances in which there was a preference, females preferred lower-frequency calls, regardless of whether they were local or foreign. These patterns of female preference are consistent with data showing that females are tuned below the mean call frequency of their population. Tuning also explains differences in preference among females of the same population. Tuning is negatively correlated with body size, and within a population larger females preferred lower frequencies and smaller females preferred higher frequencies. Thus female preference will generate directional selection acting on male call frequency but will also contribute to variation in call frequency.

The role of environmental selection in intraspecific divergence of mate recognition signals in the cricket frog, Acris-crepitans

Divergence of mate recognition signals between closely related taxa is a crucial component in the process of speciation because it can give rise to ethological isolation. The process by which mate recognition signals diverge has been a controversial issue in evolutionary biology. Dobzhanskys (1937) hypothesis of reinforcement suggested that such signals might begin to diverge in allopatry, but to become efficient isolating barriers there must be further selection on the signals during secondary contact between the two taxa. Others (e.g., Mayr, 1942; Lande, 1981; Paterson, 1982; West Eberhard, 1983) have suggestedthat divergence of mate recognition signals is an incidental by-product of speciation; the species isolating effect is not an evolved function but an incidental consequence. Divergence can result from several causes: stochastic factors, such as genetic drift (Lande, 1981); indirect selection, such as a correlated response to selection on other traits (e.g., body size; Nevo and Capranica, 1985); or direct selection on the signal itself, ifsexual selection favored different aspects of the signal in differentpopulations (West Eberhard, 1982) or if the environment favored different call types in different habitats for enhanced transmission efficiency(Morton, 1975). The purpose of this study is to examine the role of environmental selection in the divergence of mate recognition signals between the two subspecies of the cricket frog, Acris crepitans (Hylidae). Cricket frogsare common throughout much ofNorth America east ofthe Rocky Mountains. Males produce groups of short, click-like advertisement calls that attract females and repel males. Acris crepitans consists of two subspecies that differ in morphology (Nevo, 1973), allozymes (Dessauer and Nevo, 1969; Salthe and Nevo, 1969), advertisement calls (Nevo and Capranica, 1985), and habitat (Nevo, 1973). In Texas, which includes the zone of parapatry for the two subspecies, A. c. crepitans is restricted to the pinewoods of the east, while A. c. blanchardi inhabits more open grasslands and plains in the west. Nevo and Capranica (1985; see also Capranica et aI., 1973) examined geographic variation in the advertisement call of A. crepitans across its range in North America, and Ryan and Wilczynski (1988, in press) conducted a more fine-scale analysis of call variation across Texas, concentrating on the area of parapatry ofthe two subspecies. These studies reveal similar patterns. First, there are statistically significant differences in most call characters between subspecies. In general, calls of A. c. crepitans have a shorter duration, fewer pulses, a higher dominant frequency, are repeated at a faster rate within the call group, and contain more calls per call group than calls of A. c. blanchardi. Second, both studies have shown that these differences in the calls can result in local mate preferences. Although both ofthese phenomena (call differenceand local mate preferences) also can exist within a subspecies, they are more pronounced between subspecies. Nevo and Capranica (1985) suggested three hypotheses for the evolution of call differences between A. c. crepitans and A. c. blanchardi: (1) reproductive character displacement between the two subspecies, which they suggest might be incipient ecospecies; (2) a response to indirect selection for body size, which increases from east to west due to selection for the larger A. c. blanchardi to avoid desiccation in drier habitats (Nevo, 1973); (3) a response to direct selection on the call due to environmental selection for increased transmission efficiency.The detailed analysis of geographic variation across the zone of parapatry by Ryan and Wilczynski (in press) rejected the first two hypothesis. In this study we test the hypothesis that environmental selection on the call is responsible for the divergence of mate recognition signals between A. c. crepitans and A. c. blanchardi. Nevo and Capranicas third hypothesis is based on well documented environmental effects on sound transmission, and on the structural differences between the habitats in which these two subspecies occur. Since Mortons (1975) pioneering study, many other studies have shown that acoustic signals exhibit different rates of attenuation (Marten and Marler, 1977; Marten et al., 1977; Waser and Waser, 1977; Bowman, 1983; Wilczynski et aI., 1989) and degradation (Richards and Wiley, 1978, 1982; Gish and Morton, 1981; Ryan and Sullivan, 1989) in different habitats. Several studies examining variation within a species or a group of closely related species also have shown adaptation of bird song structure to local habitat (Hunter and Krebs, 1979; Gish and Morton, 1981; Bowman, 1983).

Spatial and reversal learning in congeneric lizards with different foraging strategies

Environmental demands that require intensive search for mates, food and nest sites are correlated with efficient spatial memory in many mammalian and avian species. This convergence of evidence has led to the view that spatial memory, and the neurological structures associated with it, have been selected in niches that require memory for the location of goal objects. Whether such evolutionary demands are also correlated with nonspatial abilities that require flexible use of associations similar to those required for spatial memory has not been well studied. In addition, correlations between niche types and the use of spatial or nonspatial memory have not been investigated in nonmammalian, nonavian taxa. In this study, we investigated the relationship between foraging strategies and performance on two tasks, one spatial and the other nonspatial, in congeneric lizard species: Acanthodactylus boskianus, an active forager that collects clumped sedentary prey, Acanthodactylus scutellatus, a sit-and-wait predator that collects distributed mobile prey. The two species did not differ in their performance of a spatial memory task, but A. boskianus, the active forager, performed better on the reversal of a visual discrimination, a nonspatial task. These findings question the generality of the spatial adaptation model for vertebrates. We present the pliancy hypothesis, which we developed to account for these results. Copyright 1999 The Association for the Study of Animal Behaviour.

Current research in amphibians: studies integrating endocrinology, behavior, and neurobiology.

Amphibian behavioral endocrinology has focused on reproductive social behavior and communication in frogs and newts. Androgens and estrogens are critical for the expression of male and female behavior, respectively, and their effects are relatively clear. Corticosteroids have significant modulatory effects on the behavior of both sexes, as does the peptide neuromodulator arginine vasotocin in males, but their effects and interactions with gonadal steroids are often complex and difficult to understand. Recent work has shown that the gonadal hormones and social behavior are mutually reinforcing: engaging in social interactions increases hormone levels just as increasing hormone levels change behavior. The reciprocal interactions of hormones and behavior, as well as the complex interactions among gonadal steroids, adrenal steroids, and peptide hormones have implications for the maintenance and evolution of natural social behavior, and suggest that a deeper understanding of both endocrine mechanisms and social behavior would arise from field studies or other approaches that combine behavioral endocrinology with behavioral ecology.

Acoustic communication in spring peepers - Call characteristics and neurophysiological aspects

SummarySpectral and amplitude features of the advertisement call of male spring peeper tree frogs (Hyla crucifer) were analyzed and compared to the physiological characteristics of the peripheral auditory system in both males and females determined by single unit electrophysiological recording in the VIIIth cranial nerve. The call is a very simple, nearly tonal signal with a single spectral peak (mean for the population = 2,895 Hz) and little or no harmonic or internal temporal structure. The electrophysiological results show two populations of auditory fibers in the VIIIth nerve with characteristics similar to those in other anurans. One population, presumably from the amphibian papilla, contains units tuned below 1,200 Hz. A second, high frequency population is also present, and presumably arises from the basilar papilla (BP). A sexual dimorphism is apparent in the tuning of BP units. Female BPs are tuned between 2,100 and 3,700 Hz (X= 2,939 Hz) while male BPs are tuned between 3,350 and 4,000 Hz (X= 3,580). Thus in this species the advertisement call is detected only by the basilar papilla. The BP of females is tuned to the call while the male BP is mismatched. Males can still detect the call with the lower flanks of their BP tuning curves, however, but the detection threshold will be much higher than in the females. Therefore the male advertisement call will be far more audible to females than to males.

Hormonal state influences aspects of female mate choice in the Túngara Frog (Physalaemus pustulosus)

Females alter their mate choices as they transition through different reproductive stages; however, the proximal mechanisms for such behavioral fluctuation are unclear. In many taxa, as females transition through different reproductive stages, there is an associated change in hormone levels; therefore, we examined whether fluctuation in hormone levels serves as a proximal mechanism for within-individual variation in mate choice in female túngara frogs (Physalaemus pustulosus). We manipulated hormone levels of females by administering 0, 10, 100, 500 or 1,000 IU of human chorionic gonadotropin (HCG), which is a ligand for luteinizing hormone (LH) receptors and will therefore cause increased gonadal hormone production. Phonotaxis assays were conducted to measure three aspects of mate choice behavior before and after HCG administration; receptivity (response to a conspecific mate signal), permissiveness (response to a signal that is less attractive than conspecific signals) and discrimination (ability to discern signal differences). The probability of response to a conspecific and an artificial hybrid signal significantly increased at the highest HCG doses. The difference in mean response time between pre- and post-HCG tests was significantly different for both the receptivity and permissiveness tests among the five doses. Increased permissiveness, however, was not due to decreased discrimination because females could discriminate between calls even at the highest HCG doses. These hormonal manipulations caused the same behavioral pattern we reported in females as they transitioned through different reproductive stages (Lynch, K.S., Rand, A.S., Ryan, M.J., Wilczynski, W., 2005. Plasticity in female mate choice associated with changing reproductive states. Anim. Behav. 69, 689-699), suggesting that changes in hormone levels can influence the females mate choice behavior.

Arginine Vasotocin Injection Increases Probability of Calling in Cricket Frogs, but Causes Call Changes Characteristic of Less Aggressive Males

Male cricket frogs, Acris crepitans communicate to males and females using advertisement calls, which are arranged into call groups. Calls at the middle and end, but not beginning of the call group, are modified in response to male-male aggressive interactions. We found in this field study of male cricket frogs in natural breeding choruses that the peptide hormone arginine vasotocin (AVT) not only increased the probability that males called after injections, but also caused modifications in middle and end calls to produce calls characteristic of less aggressive males. Moreover, AVT-injected males showed significantly greater increases in call dominant frequency than saline-injected males, again, a characteristic of less aggressive males. Cricket frog calls are used to both repel males and attract females, thus call changes may relate to male-male and/or male-female interactions. Saline-injected males also demonstrated significant changes in several call traits, including changes that occurred in the beginning and middle calls of the call groups, but not the end calls. AVT appeared to block some call changes produced through handling. These data suggest that AVT can influence acoustic communication in frogs in several ways, including effects on call characteristics and dominant frequency, as well as potentially blocking some handling effects.

Functional Mapping of the Auditory Midbrain during Mate Call Reception

We examined patterns of neural activity as assayed by changes in gene expression to localize representation of acoustic mating signals in the auditory midbrain of frogs. We exposed wild-caught male Physalaemus pustulosus to conspecific mating calls that vary in their behavioral salience, nonsalient mating calls, or no sound. We measured expression of the immediate early gene egr-1 (also called ZENK, zif268, NGFI-A, and krox-24) throughout the torus semicircularis, the auditory midbrain homolog of the inferior colliculus. Differential egr-1 induction in response to the acoustic stimuli occurred in the laminar, midline, and principal nuclei of the torus semicircularis, whereas the ventral region did not show significant effects of stimulus. The laminar nucleus differentially responded to conspecific mating calls compared with nonsalient mating calls, whereas the midline and principal nuclei responded preferentially to one of two conspecific calls. These responses were not explained by simple acoustic properties of the stimuli, and they demonstrate a functional heterogeneity of auditory processing of complex biological signals within the frog midbrain. Moreover, using analyses that assess the ability of the torus semicircularis as a whole to discriminate among acoustic stimuli, we found that activity patterns in the four regions together provide more information about biologically relevant acoustic stimuli than activity in any single region.

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.

The effects of arginine vasotocin on the calling behavior of male cricket frogs in changing social contexts.

We investigated the effects of the neurohypophysial peptide, arginine vasotocin (AVT), on the calling behavior of male Acris crepitans during and immediately following a simulated acoustic agonistic encounter. AVT did not block the aggressive response to agonistic calls, as the changes in temporal call characteristics in response to the encounter were similar to those of saline-treated males. However, AVT caused males to begin calling sooner during the agonistic encounter and to call significantly more than saline males during and after the agonistic encounter. In addition, AVT-treated males maintained a higher dominant frequency compared to saline animals during and following the agonistic encounter. Changes in temporal characteristics in the period following the agonistic encounter indicated that control males were more likely to exhibit a rebound effect which resulted in larger changes in calling parameters compared to AVT-treated animals. The results indicate that AVT causes changes in calling behavior in male A. crepitans during and following an agonistic encounter that are consistent with animals highly motivated to maintain vigorous active calling throughout changing social conditions.