Evolution Of Echolocation In Bats Research Articles

How the evolution of air breathing shaped hippocampal function.

To make maps from airborne odours requires dynamic respiratory patterns. I propose that this constraint explains the modulation of memory by nasal respiration in mammals, including murine rodents (e.g. laboratory mouse, laboratory rat) and humans. My prior theories of limbic system evolution offer a framework to understand why this occurs. The answer begins with the evolution of nasal respiration in Devonian lobe-finned fishes. This evolutionary innovation led to adaptive radiations in chemosensory systems, including the emergence of the vomeronasal system and a specialization of the main olfactory system for spatial orientation. As mammals continued to radiate into environments hostile to spatial olfaction (air, water), there was a loss of hippocampal structure and function in lineages that evolved sensory modalities adapted to these new environments. Hence the independent evolution of echolocation in bats and toothed whales was accompanied by a loss of hippocampal structure (whales) and an absence of hippocampal theta oscillations during navigation (bats). In conclusion, models of hippocampal function that are divorced from considerations of ecology and evolution fall short of explaining hippocampal diversity across mammals and even hippocampal function in humans.This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Ontogeny of the hyoid apparatus in Jamaican fruit bats (Chiroptera: Phyllostomidae) in unraveling the evolution of echolocation in bats

AbstractHow echolocation and flight evolved in modern day bats is a compelling and largely unanswered question in biology. As laryngeal echolocation in bats is typified by a bony connection between the larynx and the auditory bulla via the hyoid apparatus, we developed an evolutionary‐developmental model of the hyoid to test hypotheses regarding the evolution of echolocation in bats. Using computed tomography of pre‐ and postnatal Jamaican fruit bats (Artibeus jamaicensis), we showed that much of the hyoid apparatus was ossified prior to parturition. This includes the stereotypical articulation of the stylohyal bone with the auditory bulla found in laryngeal echolocating bats, where the cranial end of the stylohyal is flattened and wraps around the auditory bulla. Postnatally, thyrohyal ossification coincided with the development of increased echolocation call emission rate and the development of flight. We contend that the stepwise development of the hyoid apparatus of A. jamaicensis presented here serves as a proxy for the series of transitional forms that lead to the modern day hyoid apparatus and its cranial articulation with the auditory bulla in modern day laryngeally echolocating bats.

Parallel Amino Acid Deletions of Prestin Protein in Two Dramatically Divergent Bat Lineages Suggest the Complexity of the Evolution of Echolocation in Bats

The membrane motor protein, prestin, encoded by gene Prestin, provides the electromotility to cochlear outer hair cells (OHCs) and is therefore considered responsible for cochlea's high sensitivity to sound waves. Echolocating bats use ultrasound for orientation and hunting. In this study, we obtained the complete Prestin coding sequences of 60 mammal taxa. Alignment results detected the same 3-bp deletion mutation (c.1833_1835del in exon 18) in two bat lineages, Pteropodidae and Emballonuroidea, and caused an amino acid deletion (p.Asp611del). These two bat lineages orient with vision and echolocation, separately, suggesting that the parallel deletion occurred independently after their split. Homology modeling of the protein structures indicated contrasting structural variations after the deletion of this amino acid. Estimation of the distributions of the surface electrostatic potential coincided with the structural variation. Our findings suggest the complexity of the echolocation in bats but functionality analyses are needed to illuminate it.

Prenatal cranial bone development of Thomas's horseshoe bat (Rhinolophus thomasi): with special reference to petrosal morphology.

Cochlear morphology has been regarded as one of the key traits to understand the origin and evolution of echolocation in bats, given its functionality and performance for receiving echolocation sonar. While numerous researchers have compared adult-stage morphology, few have studied the prenatal development of the cochlea. Here, we provide the first detailed three-dimensional description of the prenatal cranial development in bats, using Rhinolophus thomasi as a model, with particular interest to the petrosal which houses the cochlea. Results revealed that among all cranial bones the onset of the ossification of the petrosal is earlier in R. thomasi when compared to other reported mammals. Generally, the cochlea reaches adult size and shape before or around birth in placental mammals including bats, but we found that its shape and size growths continue until maturity in Rhinolophus species. The relationship of cochlear size and skull size is maintained constant throughout the postnatal ontogeny to adulthood in Rhinolophus, a pattern previously reported neither in any other bats nor other mammals. The peculiar developmental pattern in Rhinolophus possibly allows them to form their characteristically large cochlea and facilitate their distinctive echolocation behavior. A recent study reported that non-echolocating Pteropodidae shares a similar prenatal cochlear size to laryngeal echolocating bats. The apparent resemblance of fetal cochlear size was proposed to be a vestigial signal of large cochlear size in the last common ancestor of bats and thus as supporting evidence for the single origin of laryngeal echolocation. However, results from the present observations suggest that limited aspects of the cochlear development were captured in this previous investigation and that the resulting interpretations may be questionable. We point out that diversity and patterns of cochlear development among bats are still not resolved, and the controversy on the origins of laryngeal echolocation is still open to discussion.

Postnatal ontogeny of the cochlea and flight ability in Jamaican fruit bats (Phyllostomidae) with implications for the evolution of echolocation.

Recent evidence has shown that the developmental emergence of echolocation calls in young bats follow an independent developmental pathway from other vocalizations and that adult-like echolocation call structure significantly precedes flight ability. These data in combination with new insights into the echolocation ability of some shrews suggest that the evolution of echolocation in bats may involve inheritance of a primitive sonar system that was modified to its current state, rather than the ad hoc evolution of echolocation in the earliest bats. Because the cochlea is crucial in the sensation of echoes returning from sonar pulses, we tracked changes in cochlear morphology during development that included the basilar membrane (BM) and secondary spiral lamina (SSL) along the length of the cochlea in relation to stages of flight ability in young bats. Our data show that the morphological prerequisite for sonar sensitivity of the cochlea significantly precedes the onset of flight in young bats and, in fact, development of this prerequisite is complete before parturition. In addition, there were no discernible changes in cochlear morphology with stages of flight development, demonstrating temporal asymmetry between the development of morphology associated with echo-pulse return sensitivity and volancy. These data further corroborate and support the hypothesis that adaptations for sonar and echolocation evolved before flight in mammals.

Bats

Bats

Hear, hear: the convergent evolution of echolocation in bats?

The evolutionary history of laryngeal echolocation is controversial, and little is known about the molecular mechanisms that underlie this sense. A recent paper by Li and colleagues is one of the first studies to identify and sequence a gene involved in echolocation in bats -Prestin, the so-called mammalian hearing gene. Phylogenetic analyses show evidence for positive selection acting on this gene in the echolocating lineages and support the convergent evolution of laryngeal echolocation in bats.

Conservation and diversity of Foxp2 expression in muroid rodents: functional implications.

FOXP2, the first gene causally linked to a human language disorder, is implicated in song acquisition, production, and perception in oscine songbirds, the evolution of speech and language in hominids, and the evolution of echolocation in bats. Despite the evident relevance of Foxp2 to vertebrate acoustic communication, a comprehensive description of neural expression patterns is currently lacking in mammals. Here we use immunocytochemistry to systematically describe the neural distribution of Foxp2 protein in four species of muroid rodents: Scotinomys teguina and S. xerampelinus ("singing mice"), the deer mouse, Peromyscus maniculatus, and the lab mouse, Mus musculus. While expression patterns were generally highly conserved across brain regions, we identified subtle but consistent interspecific differences in Foxp2 distribution, most notably in the medial amygdala and nucleus accumbens, and in layer V cortex throughout the brain. Throughout the brain, Foxp2 was highly enriched in areas involved in modulation of fine motor output (striatum, mesolimbic dopamine circuit, olivocerebellar system) and in multimodal sensory processing and sensorimotor integration (thalamus, cortex). We propose a generalized model for Foxp2-modulated pathways in the adult brain including, but not limited to, fine motor production and auditory perception.

Echolocation Performance and Call Structure in the Megachiropteran Fruit-Bat Rousettus aegyptiacus

The structure of the calls made by the echolocating fruit bat Rousettus aegyptiacus while flying within a flight tunnel were investigated. Calls are impulsive clicks lasting around 250 μs, with most energy occurring during the first 100 μs. Such a call duration is much shorter than that previously reported for this species. The ability of R. aegyptiacus to detect and avoid obstacles was tested in both the light and total darkness. Bats were able to detect and avoid 6 mm diameter wires significantly more often than 1.3 mm diameter wires when tested in the light. In the dark, the same relationship held, with no decrease in the ability to detect and avoid the obstacles. Bats used echolocation in both the light and the dark conditions. The simple impulsive clicks used in echolocation by this species are thus able to detect wires of at least 6 mm in diameter and probably smaller. The detection problems associated with very short duration signals is discussed. The possession of both a good visual system, and a good echolocation system in this species has implications for the evolution of echolocation in bats.

From spatial orientation to food acquisition in echolocating bats

Field research on echolocation behavior in bats has emphasized studies of food acquisition, and the adaptive value of sonar signal design as been considered largely in the context of foraging. However, echolocation tasks related to spatial orientation also differ among bats and are relevant to understanding signal structure. Here, we argue that the evolution of echolocation in bats is characterized by two key innovations: first, the evolution of echolocation for spatial orientation and, second, a later transition for prey acquisition. This conceptual framework calls for a new view on field data from bats orienting and foraging in different types of habitats. According to the ecological constraints in which foraging bats operate, four distinct functional groups or guilds can be defined. Within each group, signal design and echolocation behavior are rather similar.

Signal strength, timing, and self-deafening: the evolution of echolocation in bats

We propose that the ancestors of bats were small, nocturnal, sylvatic gliders that used echolocation for general orientation. Their echolocation calls were short, low intensity, broadband clicks, which translated into a very short operational range. In the lineage that gave rise to bats, a switch to stronger, tonal signals permitted the use of echolocation to detect, track, and assess flying insects in subcanopy settings. We propose that these animals hunted from perches and used echolocation to detect, track, and assess flying insects, which they attacked while gliding. In this way, the perfection of echolocation for hunting preceded the appearance of flapping flight, which marked the emergence of bats. Flapping flight had appeared by the Eocene when at least eight families are known from the fossil record. Stronger signals and adaptations to minimize self-deafening were central to the perfection of echolocation for locating flying prey. Echolocation constituted a key innovation that permitted the evolution and radiation of bats. At the same time, however, its short effective range imposed a major constraint on the size of bats. This constraint is associated with flight speed and the very small time intervals from detection of, and contact with a flying target. Gleaning and high duty cycle echolocation are two derived approaches to hunting prey in cluttered situations, places where echoes from background and other objects arrive before or at the same time as echoes from prey. Both had appeared by the Eocene.

Echolocation and hearing in the mouse-tailed bat,Rhinopoma hardwickei: acoustic evolution of echolocation in bats

1. Mouse-tailed bats (Rhinopoma hardwickei) use short-duration, multiple-harmonic, constant-frequency (CF) or slightly frequency-modulated (FM) signals for echolocation of flying insect prey. The frequency components are 18–20 kHz (first harmonic), 36–40 kHz (second harmonic), 56–60 kHz (third harmonic), and 75–80 kHz (fourth harmonic). The second harmonic is the strongest component, with the third harmonic 2 to 10 dB weaker, and the first and fourth harmonics about 10 to 20 dB weaker than the second. 2. The bat's hearing, as indicated by N4 auditory evoked potentials, is moderately sharply tuned to the second harmonic, broadly sensitive to the first harmonic and to lower frequencies, and moderately sensitive to the third and fourth harmonics. The degree of tuning is sufficient to indicate some specialized function for the second harmonic, perhaps in the task of detecting targets at maximum range, since this is the lowest of the strong harmonics and least affected by atmospheric attenuation. These bats probably do not perform the Doppler compensation response even though their hearing is tuned. 3. The pattern of emission of sonar sounds (repetition rate, duration) during interception of prey is similar to that observed in most other species of bats. The signals are emitted at repetition rates of 10–20/s during the search stage, 20–40/s during the approach stage, and about 100/s during the terminal stage of the pursuit process. The sonar sounds emitted during the search stage are 6–10 ms long, during the approach stage they are 2–4 ms long, and during the terminal stage they are less than 1 ms long. 4. The principal acoustic dimension of echolocation sounds that relates to perception of targets is signal bandwidth, whichRhinopoma hardwickei manipulates throughout the pursuit process by shortening the duration of its sonar sounds and also by slightly broadening the FM sweeps in its terminal-stage sounds. The onset-time of the long, search-stage sounds and the longer, early approach-stage sounds is more abrupt than for the shorter, late approach-stage and the short terminal-stage sounds. This apparently deliberate transient beginning broadens the signal's bandwidth at the onset relative to the narrower bandwidth prevailing for the rest of the CF harmonic structure which follows. In the shorter sounds, which are emitted during the late approach stage and terminal stage, the onset is more gradual, but the duration (the envelope) and the offset-time are now short enough that the bandwidth of the signal as a whole is increased. The bandwidth is manipulated primarily by these changes in signal envelope and secondarily by the increased FM sweep-width in the terminal stage. 5. Except for duration these signals are relatively inflexible and suggestive of a primitive kind of echolocation in which only one dimension is changed to achieve qualities which most other species of bats obtain by changing a variety of signal dimensions simultaneously. The abrupt signal onsets may be an indication that multiple-harmonic CF and FM echolocation sounds evolved from click-like echolocation sounds of the type emitted byRousettus and some terrestrial mammals.

Ears adapted for the detection of motion, or how echolocating bats have exploited the capacities of the mammalian auditory system

Bats use the rich food resources of the night by specializing in audition. They emit short echolocation sounds and listen to the echoes returning from potential prey. The bat’s auditory system analyzes spectral and temporal parameters of echoes for detecting, locating, and identifying a target. Different bat species have solved the problem of acoustic target detection and pattern recognition even in clustered situations by focusing on certain acoustical features of a target. The specialized motion detection by horseshoe bats, for instance, analyzes small echofrequency shifts modulated onto a long constant frequency echolocation signal. These frequency modulations are Doppler shifts within echoes returning from wing beating insects. For detecting modulations as small as 10 Hz or 0.01%, horseshoe bats have in the cochlea an extremely narrow filter (Q?500) matched to the carrier frequency (i.e., echolocation sound) of 83 kHz. The filter is realized by structural differentiations of the basilar membrane and the filter frequencies are represented on the basilar membrane in an expanded fashion. We have called this specialized patch of the basilar membrane an ’’acoustical fovea.’’ The ’’foveal frequencies’’ are largely overrepresented in the tonopical arrangement of the ascending auditory pathway. The bats have developed a feedback system which lowers the emitted frequency during flight in such a way that the Doppler shifted echofrequency is kept precisely at a fixed reference frequency of the fovea. This feedback system and other neuronal data disclose an intricate coupling of the auditory and vocalizing system. The evolution of echolocation in bats has driven the analyzing capacities of audition in both frequency and time domain close to theoretical limits. Investigations of such specialized systems give fascinating insights into capacities and possible general principles of auditory information processing.

Ears adapted to detect motion, or how echolocating bats exploit the capacities of the mammalian auditory system

Bats avail themselves of the rich food resources of the night by specializing in audition. They emit short echolocation sounds and listen to the echoes returning from potential prey and the environment. The bat's auditory system analyzes spectral and temporal parameters of echoes for detecting, precisely locating, and identifying a target. Different bat species have solved the problem of acoustic target detection and pattern recognition even in heavily clustered situations by focusing on certain acoustical features of the targets. The specialized motion defection by Horseshoe bats, for instance, analyzes small echofrequency shifts modulated onto a long constant frequency echolocation signal. These frequency modulations are Doppler shifts of echoes returning from wing beating insects. For detecting modulations as small as 10 Hz or 0.01%, Horseshoe bats have in the cochlea an extremely narrow filter (Q = ca. 500) matched to the carrier frequency (i.e., echolocation sound) of 83 kHz. The filter is based on mechanical principles and realized by structural differentiations of the basilar membrane. We have called this specialized patch of the basilar membrane an “acoustical fovea.” In analogy to the visual fovea the “foveal frequencies” are largely over‐represented in the tonopical arrangement of the ascending auditory pathway. The bats have developed a feedback system which lowers the emitted echolocation frequency in such a way that the Doppler shifted echofrequency is kept precisely at a fixed reference frequency close to 83 kHz. This feedback system and additional neuronal data disclose an intricate coupling of the auditory and vocalizing system. The evolution of echolocation in bats has driven the analyzing capacities of audition close to theoretical limits. Investigations in such specialized systems give fascinating insights into possible general principles of auditory information processing.