Female mate choice can drive the evolution of high frequency echolocation in bats: a case study with Rhinolophus mehelyi.

Animals employ an array of signals (i.e. visual, acoustic, olfactory) for communication. Natural selection favours signals, receptors, and signalling behaviour that optimise the received signal relative to background noise. When the signal is used for more than one function, antagonisms amongst the different signalling functions may constrain the optimisation of the signal for any one function. Sexual selection through mate choice can strongly modify the effects of natural selection on signalling systems ultimately causing maladaptive signals to evolve. Echolocating bats represent a fascinating group in which to study the evolution of signalling systems as unlike bird songs or frog calls, echolocation has a dual role in foraging and communication. The function of bat echolocation is to generate echoes that the calling bat uses for orientation and food detection with call characteristics being directly related to the exploitation of particular ecological niches. Therefore, it is commonly assumed that echolocation has been shaped by ecology via natural selection. Here we demonstrate for the first time using a novel combined behavioural, ecological and genetic approach that in a bat species, Rhinolophus mehelyi: (1) echolocation peak frequency is an honest signal of body size; (2) females preferentially select males with high frequency calls during the mating season; (3) high frequency males sire more off-spring, providing evidence that echolocation calls may play a role in female mate choice. Our data refute the sole role of ecology in the evolution of echolocation and highlight the antagonistic interplay between natural and sexual selection in shaping acoustic signals.

Variability in echolocation call intensity in a community of horseshoe bats: a role for resource partitioning or communication?

BACKGROUND: Only recently data on bat echolocation call intensities is starting to accumulate. Yet, intensity is an ecologically crucial parameter, as it determines the extent of the bats' perceptual space and, specifically, prey detection distance. Interspecifically, we thus asked whether sympatric, congeneric bat species differ in call intensities and whether differences play a role for niche differentiation. Specifically, we investigated whether R. mehelyi that calls at a frequency clearly above what is predicted by allometry, compensates for frequency-dependent loss in detection distance by using elevated call intensity. Maximum echolocation call intensities might depend on body size or condition and thus be used as an honest signal of quality for intraspecific communication. We for the first time investigated whether a size-intensity relation is present in echolocating bats. METHODOLOGY/PRINCIPAL FINDINGS: We measured maximum call intensities and frequencies for all five European horseshoe bat species. Maximum intensity differed among species largely due to R. euryale. Furthermore, we found no compensation for frequency-dependent loss in detection distance in R. mehelyi. Intraspecifically, there is a negative correlation between forearm lengths and intensity in R. euryale and a trend for a negative correlation between body condition index and intensity in R. ferrumequinum. In R. hipposideros, females had 8 dB higher intensities than males. There were no correlations with body size or sex differences and intensity for the other species. CONCLUSIONS/SIGNIFICANCE: Based on call intensity and frequency measurements, we estimated echolocation ranges for our study community. These suggest that intensity differences result in different prey detection distances and thus likely play some role for resource access. It is interesting and at first glance counter-intuitive that, where a correlation was found, smaller bats called louder than large individuals. Such negative relationship between size or condition and vocal amplitude may indicate an as yet unknown physiological or sexual selection pressure.

Behavioral evidence for community-wide species discrimination from echolocation calls in bats.

Recognizing species identity is crucial for many aspects of animal life and is often mediated by acoustic signals. Although most animals are able to distinguish acoustic signals of their own species from other sympatrically occurring species, it is yet unknown whether animals can distinguish among acoustic signals of different closely related sympatric species. In this context, echolocating bats are a particularly interesting model system: their echolocation system evolved primarily for spatial orientation and foraging, but recent studies indicate that echolocation also has an important communicative function. Yet, the role of echolocation calls for species discrimination and thus potentially for interspecific communication has not been investigated. Using a behavioral discrimination assay, we found that two species of wild horseshoe bats could discriminate calls of their own species from those of three sympatric congeneric species. We further show that the bats were able to discriminate between echolocation calls of different congeneric species from the local community. In both cases, discrimination ability was high despite strong overlap of species' call frequency bands. This study provides the first experimental evidence for species discrimination based on echolocation calls. On a more general level, it shows for the first time that animals can distinguish among acoustic signals of different closely related and ecologically similar species from their local community.

Localization dominance and the effect of frequency in the Mongolian Gerbil, Meriones unguiculatus.

Due to its good low-frequency hearing, the Mongolian Gerbil (Meriones unguiculatus) has become a well-established animal model for human hearing. In humans, sound localization in reverberant environments is facilitated by the precedence effect, i.e., the perceptual suppression of spatial information carried by echoes. The current study addresses the question whether gerbils are a valid animal model for such complex spatial processing. Specifically, we quantify localization dominance, i.e., the fact that in the context of precedence, only the directional information of the sound which reaches the ear first dominates the perceived position of a sound source whereas directional information of the delayed echoes is suppressed. As localization dominance is known to be stimulus-dependent, we quantified the extent to which the spectral content of transient sounds affects localization dominance in the gerbil. The results reveal that gerbils show stable localization dominance across echo delays, well comparable to humans. Moreover, localization dominance systematically decreased with increasing center frequency, which has not been demonstrated in an animal before. These findings are consistent with an important contribution of peripheral-auditory processing to perceptual localization dominance. The data show that the gerbil is an excellent model to study the neural basis of complex spatial-auditory processing.

Object-oriented echo perception and cortical representation in echolocating bats.

Echolocating bats can identify three-dimensional objects exclusively through the analysis of acoustic echoes of their ultrasonic emissions. However, objects of the same structure can differ in size, and the auditory system must achieve a size-invariant, normalized object representation for reliable object recognition. This study describes both the behavioral classification and the cortical neural representation of echoes of complex virtual objects that vary in object size. In a phantom-target playback experiment, it is shown that the bat Phyllostomus discolor spontaneously classifies most scaled versions of objects according to trained standards. This psychophysical performance is reflected in the electrophysiological responses of a population of cortical units that showed an object-size invariant response (14/109 units, 13%). These units respond preferentially to echoes from objects in which echo duration (encoding object depth) and echo amplitude (encoding object surface area) co-varies in a meaningful manner. These results indicate that at the level of the bat's auditory cortex, an object-oriented rather than a stimulus-parameter-oriented representation of echoes is achieved.

The absence of spatial echo suppression in the echolocating bats Megaderma lyra and Phyllostomus discolor.

Acoustic orientation most often takes place in echoic environments. The mammalian auditory system shows a variety of specializations to suppress misleading spatial information mediated by echoes. Psychophysically these specializations are summarized as the precedence effect. This study investigates how echolocating bats deal with multiple reflections of their sonar emissions from different spatial positions. In a two-alternative, forced choice paradigm, a study was made of the extent to which the echolocating bats Megaderma lyra and Phyllostomus discolor spontaneously suppress the spatial information of a second reflection of their sonar emission. The delay between the first and the second reflection ranged between 0 and 12.8 ms. In general, M. lyra (five individuals) and P. discolor (two individuals) did not suppress the spatial information of the second reflection of their sonar emission, whatever the delay. Only one M. lyra showed significant suppression for delays between 0.8 and 3.2 ms. However, this suppression could not be confirmed in an exact repetition of the experiment. The current data indicate that although bats may be able to suppress the spatial information of a second reflection, this is not their default mode of auditory processing. The reason for this exceptional absence of spatial echo suppression may lie in the shorter time constants of cochlear processing in the ultrasonic frequency range and the strong influence of cognitive components associated with the ;precedence effect'.