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Nonecholocating Fruit Bats Produce Biosonar Clicks with Their Wings
Abstract
Because evolution mostly acts over millions of years, the intermediate steps leading to a functional sensory system remain enigmatic [1-3]. Accordingly, there is an ongoing debate regarding the evolution of bat echolocation [4-10]. In search of the origin of bat echolocation, we studied how Old World fruit bats, which have always been classified as nonecholocating [3, 10-12], orient in complete darkness. We found that two of these nonecholocating species used click-like sounds to detect and discriminate objects in complete darkness. However, we discovered that this click-based echo sensing is rudimentary and does not allow these bats to estimate distance accurately as all other echolocating bats can. Moreover, unlike all other echolocating bats, which generate pulses using the larynx or the tongue, these bats generated clicks with their wings. We provide evidence suggesting that all Old World fruit bats can click with their wings. Although this click-based echo sensing used by Old World fruit bats may not represent the ancestral form of current (laryngeal) bat echolocation, we argue that clicking fruit bats could be considered behavioral fossils, opening a window to study the evolution of echolocation.
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... Гладконосые летучие мыши (Vespertilionidae Gray, 1821) испускают ультразвуковые сигна-лы через ротовую полость, а подковоносые летучие мыши (Rhinolophidae Gray, 1825) -через нос, что находит своё отражение не только в форме носа и наличии характерных околоносовых кожных складок у подковоносых, но и в топологии полости носа, и в микроструктуре слизистых [62,181,205,236]. Представители подотряда крыланов (Megachiroptera Dobson, 1875) в большинстве своём вообще не используют ультразвуковую эхолокацию: исключение составляют летучие собаки Rousettus (Gray, 1821), макроглоссусы (Macroglossus Cuvier F., 1824) и циноптерусы (Cynopterus Cuvier F., 1824), которые производят пощёлкивания либо основанием языка, либо с помощью крыльев (вероятнее всего -костями запястья) [194,228]. Самцы некоторых видов крыланов -например, молотоголовых крыланов (Hypsignathus monstrosus Allen H., 1861) -имеют гипертрофированные щитовидный и перстневидный хрящи (настолько мощные, что серьёзно поджимают другие внутренние органы), а по бокам глотки имеются выходы в носоглотку, которые соединены с усиливающими звук резонаторными камерами (рис. 37) -однако они не используют глотку для извлечения ультразвуковых сигналов, а всего лишь издают громкие «трели» во время брачного «токования» [245]. ...
... , то (193) что тоже вполне логично. Если и летучая мышь, и мотылёк неподвижны (или же принимается приближение ), то получается тривиальное (194) в полном соответствии с формулой (162). О т в е т: выражение (192). ...
... 140). В момент времени передовой волновой фронт сигнала достигнет мишени и начнёт обратное движение, вернувшись к источнику через время в полном соответствие с формулами (162) и (194). Но в этот момент возвращается лишь передовой волновой фронт акустического сигнала, и прежде, чем во внутреннее ухо летучей мыши поступит выделенная намиая волна, туда должны поступить предыдущие волна (на что потребуется дополнительное время, равное Таким образом, в случае (634), испускаемая и принимаемая частота не равны друг другу, а различаются на величину , которая называется доплеровским сдвигом -в честь австрийского физика Кристиана Доплера (1803-1853) (рис. ...
This manual is aimed at a comprehensive study of the phenomenon of bioecholocation. The manual contains theoretical material on the main issues related to the topic of the history of science, zoology, thermodynamics, physics of wave processes, acoustics, equations of mathematical physics. Information beyond the scope of the secondary school curriculum is explained directly in the text in the shortest and most accessible form. To improve the assimilation of the material the manual is accompanied by tables and figures. The manual is intended for undergraduates and postgraduates specialising in biology, biophysics, medicine and applied physics.
... Approximately 85% of the 1200 known species of bats use echolocation to map and navigate their environment [1]. In 2014, a species of bat previously thought to not have the capabilities to echolocate was found to use a crude form of echolocation by emitting bio-sonar clicks with its wings [2]. Inspired by the work in [2], we seek to work towards a MAV platform that can utilize the self-noise generated from the vehicle's normal operation to acoustically sense its surroundings. ...
... In 2014, a species of bat previously thought to not have the capabilities to echolocate was found to use a crude form of echolocation by emitting bio-sonar clicks with its wings [2]. Inspired by the work in [2], we seek to work towards a MAV platform that can utilize the self-noise generated from the vehicle's normal operation to acoustically sense its surroundings. Similar to the way mosquitoes detect changes to their self-induced flow patterns caused by the proximal physical environment [3], we envision creating a region of awareness around MAVs using self-induced acoustic signatures. ...
... The received acoustic signal on the microphones must be spectrally whitened in order to extract the relevant time delays. In the next section, we describe a spectral whitening approach to exploit the model (2) in order to extract the delays τ 0 and τ 1 . ...
In this paper we propose an algorithm to estimate the distance between an aerial vehicle and a large obstacle using the self-induced noise present during the vehicle's normal operation. We demonstrate the feasibility of using the proposed estimation method in real-time as a feedback mechanism to actively control the altitude of a blimp-like vehicle. The method is built upon a physics-based acoustic model of an unknown source emitting sound near an acoustically reflective surface. By placing two microphones beneath a motor-propeller system used to control the altitude of the vehicle, a real-time processing algorithm of the audio signals is presented that can accurately detect the distance from the microphones to the ground. The method is based upon computing the cross-correlation matrix of the signals on the two microphone channels. We develop a novel cross-correlation processor that is capable of filtering out the unknown source term and extracting the relevant time-delay representing the time it takes for an acoustic wave traveling from the microphone to the ground and back. Furthermore, we show that the method is also robust to the more complex noise source generated by a quadrotor in a static, tethered experiment. To the best of our knowledge, this is the first framework and demonstration of obstacle sensing onboard an aerial vehicle using only the self-generated noise.
... Bats with more than almost 1400 known species comprise about a quarter of mammals and widespread throughout world [3] . They are benefit animals in ecosystem and divided to subspecies of Megachiroptera with large eye [4] and Microchiroptera with small eyes and poor eyesight [5] . They have diurnal and nocturnal spices and respond to moonlight intensity [6] . ...
... Rousettus aegyptiacus (Geoffroy 1810) is frugivorous bat that unlike the other megabat use echolocation for orientation. They produce ultrasounds by the tongue banging on the mouth wall [11] or with their wing [4] . They live in dark roosts, but able to detect small differences in brightness and hunt during the day in sunlight. ...
... The consuming materials were prepared as follow 4.28g Sodium cacodylate powder was solvated in 100cc dislated water and solution (0.2M) was obtained. ...
... The Egyptian fruit bat, Rousettus aegyptiacus, is a very interesting animal model to study multisensory integration due to its strong reliance on two sensory systems: vision and echolocation. Rousettus bats have large eyes, providing high spatial acuity (16), high sensitivity (a low visual threshold) (17), and some binocular overlap, suggesting depth perception (18). In addition to their profound use of vision, these bats also use echolocation to navigate and forage (19). ...
... When vision was abolished by conducting the experiment in complete darkness [<10 −7 lux, which is below the visual threshold of these bats (17); "echolocation-only training"], three bats did not succeed in discriminating between the targets (Fig. 1B). We tested them for 10 sessions since, by this point, they all reached 75% success under the bimodal condition. ...
... When presented with a black wall (in the blocked arm) in three different light levels [5 × 10 −2 , 2 × 10 −3 , and 3 × 10 −5 lux, all of which are above their visual threshold (17)], the bats preferred the blocked arm almost exclusively over the open arm. On average, 90% of the ~40 bats in each light level preferred the blocked arm (P < 10 −3 for every light level, binomial test relative to chance; Fig. 3B). ...
How animals integrate information from various senses to navigate and generate perceptions is a fundamental question. Bats are ideal animal models to study multisensory integration due to their reliance on vision and echolocation, two modalities that allow distal sensing with high spatial resolution. Using three behavioral paradigms, we studied different aspects of multisensory integration in Egyptian fruit bats. We show that bats learn the three-dimensional shape of an object using vision only, even when using both vision and echolocation. Nevertheless, we demonstrate that they can classify objects using echolocation and even translate echoic information into a visual representation. Last, we show that in navigation, bats dynamically switch between the modalities: Vision was given more weight when deciding where to fly, while echolocation was more dominant when approaching an obstacle. We conclude that sensory integration is task dependent and that bimodal information is weighed in a more complex manner than previously suggested.
... For example, "megabats" (Pteropodidae) produce wing sounds: Gould (1988) reported that Eonycteris spelaea produce a click-like sound only in flight, and suggested that the mechanism was percussive. Subsequently, Boonman et al. (2014) documented several Pteropodidae species make wing clicks that serve as a form of echolocation, but disputed that percussion was the mechanism, and suggested that further research is needed to determine the mechanism. Waters and Jones (1994) describe broadband, predominantly ultrasonic wing sounds of noctuid moths associated with clap-and-peel wing kinematics. ...
... This suggests a hypothesis: wing-generated sounds might coevolve with display kinematics, such that, initially sonations evolve during aerial displays, but then as the sound becomes a prominent part of the receiver's experience of the display, the display evolves to lose the airborne kinematics but maintains production of the sound. Some of the mechanisms described are widespread in flight, while others are concentrated in a single Boonman et al. 2014Boonman et al. , 2020. Are bats intrinsically quiet, or are they understudied? ...
There are at least eight ways that wings potentially produce sound. Five mechanisms are aerodynamic sounds, created by airflow, and three are structural sound created by interactions of solid surfaces. Animal flight is low Mach (M), meaning all animals move at less than 30% of the speed of sound. Thus in aerodynamic mechanisms the effects of air compressibility can be ignored, except in mechanism #1. Mechanism #1 is trapped air, in which air approaches or exceeds Mach 1 as it escapes a constriction. This mechanism is hypothetical but likely. #2 is Gutin sound, the aerodynamic reaction to lift and drag. This mechanism is ubiquitous in flight, and generates low frequency sound such as the humming of hummingbirds or insect wing tones. #3 is turbulence-generated atonal whooshing sounds, which are also widespread in animal flight. #4 are whistles, tonal sounds generated by geometry-induced flow feedback. This mechanism is hypothetical. #5 is aeroelastic flutter, sound generated by elasticity-induced feedback that is usually but not always tonal. This is widespread in birds (feathers are predisposed to flutter) but apparently not bats or insects. Mechanism #6 is rubbing sound (including stridulation), created when bird feathers or insect wings slide past each other. Atonal rubbing sounds are widespread in bird flight and insects; tonal stridulation is widespread in insects. #7 is percussion, created when two stiff elements collide and vibrate, and is present in some birds and insects. Mechanism #8 are tymbals and other bistable conformations. These are stiff elements that snap back and forth between two conformations, producing impulsive, atonal sound. Tymbals are widespread in insects but not birds or bats; insect cuticle appears predisposed to form tymbals. There are few examples of bat wing sounds: are bats intrinsically quiet, or just under-studied? These mechanisms, especially Gutin sound, whooshes, and rubbing (#2, #3, and #6) are prominent cues in ordinary flight of all flying animals, and are the ‘acoustic substrate’ available to be converted from an adventitious sound (cue) into a communication signal. For instance, wing sounds have many times evolved into signals that are incorporated into courtship displays. Conversely, these are the sounds selected to be suppressed if quiet flight is selected for. The physical mechanisms that underlie animal sounds provides context for understanding the ways in which signals and cues may evolve.
... In fact, phytophagy has rarely evolved in bats, but intensely so within Phyllostomidae and in the ancestor of all pteropodids (Giannini 2019). Pteropodids are also outstanding among bats for lacking the laryngeal echolocation capability present in all other bat families (probably as a result of a secondary loss; see Teeling et al. 2012;Boonman et al. 2014;Wang et al. 2017;Thiagavel et al. 2018), and for their wide interspecific body size variance, including the by far largest bat species (Nowak 1994). Mean body size in species of Old World fruit bats ranges from 14 to ca. 1500 g, while in all other bat families, body size has a median value of~16 g (never exceeding 250 g; see Moyers Arévalo et al. 2020 and citations therein). ...
... The evolution of very large sizes in pteropodids has been hypothesized to be a consequence of the functional release from physical constraints imposed by echolocation on body size (see Moyers Arévalo et al. 2020 and citations therein). Lack of sophisticated laryngeal echolocation made pteropodids dependent upon olfaction and vision to navigate in search for food, mates, and roost, although echolocation based on tongueclicking (in Rousettus) and wing clicking (in several other genera) evolved secondarily in a few pteropodids allowing these forms to inhabit dark caves (Yovel et al. 2011;Boonman et al. 2014). ...
Pteropodidae constitutes one of the most diverse bat families. These bats have evolved a phytophagous diet, likely lost laryngeal echolocation capability, and attained the largest body sizes among bats. Previous phylogenetic studies suggested that the family might have experienced an explosive diversification at its origin. Here, we readdress this hypothesis using a macroevolutionary approach based on Bayesian statistics (BAMM), a sampling of 139 pteropodid species, and divergence date estimates obtained in a comprehensive phylogenetic study of Chiroptera with multiple fossil calibration points. We evaluated the effect of missing data and of a reduced outgroup by repeating the analyses across simulated complete phylogenies and across a comprehensive Yinpterochiroptera phylogeny, respectively. Additionally, we performed an alternative analysis to detect diversification-rate shifts through time, the birth-death-shift method. In contrast with a previous study, we found strong statistical signals of rapid diversification at the origin of Pteropodidae. BAMM also detected diversification-rate shifts (increases) at the origin of Pteropus, as well as at crown Hipposideridae and Rhinolophidae. The birth-death-shift method detected a shift at approximately 25 million years ago, the estimated crown ages of both Pteropodidae and Hipposideridae. Our results point to a complex dynamics in the evolution of bat families, likely related to key innovations, demographic factors, and environmental opportunity enhanced by global-scale climatic and geographic changes.
... In 2014, a species of bat that previously was not known to possess the biological structures in order to echolocate was shown to exhibit a crude form of echolocation using bio-sonar clicks from their wings [20]. While this primitive form of echolocation cannot be utilized for real-time obstacle avoidance of thin objects such as wires, it has been demonstrated that these fruit bats can identify and avoid collisions with large surfaces. ...
... While this primitive form of echolocation cannot be utilized for real-time obstacle avoidance of thin objects such as wires, it has been demonstrated that these fruit bats can identify and avoid collisions with large surfaces. Inspired by the results in [20], in this work we employ a strategy that leverages the self generated noise already present from motor-propeller systems (MPSs) present on MAVs. The benefits of such an approach is a lightweight, low power sensing system since MAV platforms are subject to size, weight and power constraints and in general, fewer sensors are more desirable. ...
In this paper we propose an algorithm to actively control the distance of a motor-propeller system (MPS) to a large obstacle using data from a single microphone. The method is based upon a broadband constructive/destructive interference pattern across the audible frequency band that is present when the MPS is near an obstacle. By taking the difference between the power spectrum in the obstacle-free case and the spectrum when recording near an obstacle, a broadband oscillation with respect to frequency is revealed. The frequency of this oscillation is linearly-related to the distance from the microphone to the wall. We present both static and dynamic experiments showcasing the ability of the proposed method to estimate the distance to a wall as well as actively control it.
... While LE is unknown in extant pteropodids-as is the case for echolocation of any kind in almost all~200 pteropodid species-the biosonar-based orientation abilities of the tongue-clicking pteropodid, Rousettus aegyptiacus, have recently been recognized as being more sophisticated than previously thought 25 . Furthermore, more rudimentary echo-based orientation has now been experimentally supported in at least two other pteropodid genera, based on wing clicks potentially used in nature for finding suitable roosting places in dark caves 52,53 . Taken together, all of the above suggests that not only was LE lost, rather than never present, in the Pteropodidae, but that the foundations for chiropteran echolocation may not have regressed entirely and instead remain available to be built upon in this lineage. ...
... Taken together, all of the above suggests that not only was LE lost, rather than never present, in the Pteropodidae, but that the foundations for chiropteran echolocation may not have regressed entirely and instead remain available to be built upon in this lineage. Indeed, this has, perhaps, happened several times already (see Fig. 3 in ref. 53 ). ...
Substantial evidence now supports the hypothesis that the common ancestor of bats was nocturnal and capable of both powered flight and laryngeal echolocation. This scenario entails a parallel sensory and biomechanical transition from a nonvolant, vision-reliant mammal to one capable of sonar and flight. Here we consider anatomical constraints and opportunities that led to a sonar rather than vision-based solution. We show that bats' common ancestor had eyes too small to allow for successful aerial hawking of flying insects at night, but an auditory brain design sufficient to afford echolocation. Further, we find that among extant predatory bats (all of which use laryngeal echolocation), those with putatively less sophisticated biosonar have relatively larger eyes than do more sophisticated echolocators. We contend that signs of ancient trade-offs between vision and echolocation persist today, and that non-echolocating, phytophagous pteropodid bats may retain some of the necessary foundations for biosonar.
... If the development of echolocation and social calls are independent they likely have different evolutionary origins (Monroy et al. 2011;. With the exception of tongue clicking (Rousettus) and potentially wing clicking pteropodids (Eonycteris spelea, Cynopterus brachyotis, and Macroglossus sobrinus) (Boonman et al. 2014), echolocation calls are initially formed by the larynx (Griffin 1946). Variable tension on the vocal folds is achieved by the cricothyroid muscles, providing different vibration frequencies required for tonal sound production. ...
... It also may explain why the asymmetrical loads of walking produce a higher rate of echolocation emission than the symmetrical loads of flying in M. tuberculata. This scenario is at odds with the interesting hypothesis proposed by Boonman et al. (2014) where, potentially, wing-clicking fruit bats represent behavioral fossils, suggesting that sophisticated echolocation evolved as a by-product of powered flight. ...
The evolutionary sequence of events that led to flight and echolocation in bats is a compelling question in biology. Fundamentally lacking from this discussion is the ontogeny of how these two systems become functionally integrated producing an evolutionary developmental model. We build such a model by integrating growth and development of the cochlea, larynx, and sound production with the ontogeny of locomotion in newborn bats. In addition, we use available fossil and molecular data along with patterns of high frequency vocalization in extant mammals to model probable evolutionary transitions in bats. We find clear evidence that the ability to hear high frequency echolocation-like sounds preceded the ability to produce it and that a simple echolocation system was likely inherited from a shrew-like ancestor and was not an in situ evolutionary innovation of bats. Refinement of this system coevolved with sustained flight, both ontogenetically and evolutionarily, leading to the sophisticated echolocation observed today.
... Importantly, all bats produced echolocation clicks outdoors, demonstrating that the Egyptian fruit bat relies on echolocation not only in dark caves, as previously speculated [4], but also during orientation and foraging in diverse light environments. As this range of natural outdoor light levels should allow use of vision in this species [6], we next examined if and how Egyptian fruit bats alter their sensory sampling through biosonar at different light levels. ...
... We tested a minimum of nine bats in each condition. The lowest light level we tested (< 10 -7 lux, or 'complete darkness') is equivalent to the light level Correspondence within the cave roosts of these bats and is below their visual detection threshold [6]. The highest tested light level (35 lux, or 'fully lit') is equivalent to the illumination at a typical foraging site in an urban environment. ...
The study of inter-sensory integration has focused largely on how different sensory modalities are weighted and combined in perception [1-3]. However, the extent to which information acquired through one sensory modality is modulated by another is yet unknown. We studied this problem in the Egyptian fruit bat (Rousettus aegyptiacus), an animal equipped with two modalities supporting high resolution distal sensing: biosonar and vision [4,5]. Egyptian fruit bats emit ultra-short, broad-band lingual echolocation clicks that enable accurate spatial orientation and landing [5]. They also rely heavily on vision, exhibiting high absolute sensitivity [4]. Here, we examine how visual information, regulated by altering ambient light level, influences biosonar sampling by Egyptian fruit bats. We tracked bats in the field and demonstrated that they routinely echolocate outdoors under a wide range of light levels. In the laboratory, under biologically relevant light levels, bats increased both echolocation click rate and intensity at lower light levels, where visual information was limited. These findings demonstrate how sensory information from one modality (vision) may influence sensory sampling of another (biosonar). Additionally, the bats adjusted biosonar sampling in a task-dependent manner, increasing click rate prior to landing. They did not cease echolocating under light conditions, which leads us to hypothesize that Egyptian fruit bats use echolocation to complement vision for accurate estimation of distance.
... Nevertheless, our functional analyses of the echolocation-related gene prestin exhibited a higher 1/a value in the LCAP than in the extant fruit bat ( Figure 2C), as is observed between echolocating and nonecholocating mammals (Liu et al., 2014(Liu et al., , 2018, suggesting that the LCAP retained some vestigial ability of relatively high-frequency hearing. Notably, some nonecholocating fruit bats were reported to produce sonar sounds with tongue clicks or wing claps (Boonman et al., 2014), which substantially differ from laryngeal echolocation. ...
The laryngeal echolocation is regarded as one of the conspicuous traits that play major roles in flourishing bats. Whether the laryngeal echolocation in bats originated once, however, is still controversial. We here address this question by performing molecular convergence analyses between ancestral branches of bats and toothed whales. Compared with controls, the molecular convergences were enriched in hearing-related genes for the last common ancestor of bats (LCAB) and extant echolocating bats, but not for the LCA of Old World fruit bats (LCAP). And the convergent hearing gene prestin of the LCAB and the extant echolocating bats functionally converged. More importantly, the high-frequency hearing of the LCAP-prestin knock-in mice decreased with lower cochlear outer hair cell function compared with the LCAB-prestin knock-in mice. Together, our findings provide multiple lines of evidence suggesting a single origin of laryngeal echolocation in the LCAB and the subsequent loss in the LCAP.
... Furthermore, while pteropodids cannot use laryngeal echolocation, they still have other echolocating behaviours which they utilise for obstacle avoidance: tongue-clicking in some Rousettus species, and wing-clicking occurs in at least nineteen other pteropodid species (Griffin et al. 1958, Grinnell & Hagiwara 1972, Herbert 1985, Holland et al. 2004, Boonman et al. 2014. Early authors assumed clickbased echolocation of pteropodids to be crude, yet it has proven a viable alternative to laryngeal echolocation for obstacle avoidance, even exceeding it in Doppler tolerance and target ranging (Waters & Vollrath 2003, Holland et al. 2004, Yovel et al. 2011). ...
Anderson and Ruxton (Mammal Review, 2020) reviewed the evolution of powered flight and laryngeal echolocation in bats. They hypothesised that powered
flight and laryngeal echolocation evolved in separate lineages of handwing gliders.
We note fossil, character evolution, and developmental evidence contradict their
hypothesis, and we test their handwing gliding model, finding it aerodynamically
implausible. We conclude that the traditional view of bat evolution (that flight
and laryngeal echolocation evolved in the common ancestor of all bats, with
the latter being lost in pteropodids) is more plausible than the proposed novel
hypothesis.
... This evidence suggests that the ancestor of all bats used laryngeal echolocation, but that echolocation was lost in the ancestor of the Pteropodidae (Teeling et al. 2005). Fascinatingly, several species in the Pteropodidae can echolocate in a very different way than other bat species, using tongue clicking (lingual echolocation) (Yovel et al. 2010) or wing clapping (Boonman et al. 2014), indicating that echolocation re-evolved in this group in a different form from other bats. ...
We see stunning morphological diversity across the animal world. Less conspicuous but equally fascinating are the sensory and cognitive adaptations that determine animals’ interactions with their environments and each other. We discuss the development of the fields of sensory and cognitive ecology and the importance of integrating these fields to understand the evolution of adaptive behaviors. Bats, with their extraordinarily high ecological diversity, are ideal animals for this purpose. An explosion in recent research allows for better understanding of the molecular, genetic, neural, and behavioral bases for sensory ecology and cognition in bats. We give examples of studies that illuminate connections between sensory and cognitive features of information filtering, evolutionary trade-offs in sensory and cognitive processing, and multimodal sensing and integration. By investigating the selective pressures underlying information acquisition, processing, and use in bats, we aim to illuminate patterns and processes driving sensory and cognitive evolution.
Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 52 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... tenuis). Some Pteropodidae use other mechanisms to produce basic echolocation signals, for example Rousettus leschenaultii echolocate by tongue clicks (Holland et al., 2004;Wordley et al., 2014) and Eonycteris spelaea use wingclapping (Gould, 1988;Boonman et al., 2014). Narrowband calls are optimised to forage in open space, while broadband calls tend to be used by gleaning bats or species that aerially hawk in cluttered habitats (Neuweiler et al., 1984;Neuweiler, 1989Neuweiler, , 1990Jones and Rydell, 2003;Schnitzler et al., 2003). ...
Acoustic monitoring provides an effective and non-invasive means to survey many species such as bats, birds and frogs. However, the acoustic monitoring poses challenges in determining the species identity due to lack of reference recordings or due to similar call structures across species. Here we recorded bats from 30 different locations at varying altitudes (0–1,200 m) and latitudes (7–12°N) using a full spectrum Pettersson M500-384 ultrasound detector. We used 2,070 pulses from 329 individual sequences of 20 bat species to standardise the echobank (catalogue of call characteristics). Discriminant function analyses (DFA) was carried out separately for the bats producing constant frequency (CF) and frequency modulated (FM) calls using frequency of maximum energy and end frequency, and shows an accuracy of 97.48% and 96.09% for CF and FM bats respectively. We also collated published reference calls for bat species in this region to develop a regional echobank for 42 species of echolocating bats from the Western Ghats. For six species, we report their echolocation calls for the first time. The echobank provides a useful tool for further conservation and monitoring studies in the wider region.
... Birds are not the only animals that use sound to locate prey while hunting on the wing, and thus may need to fly in silence: bats also fit this description. Dr Arjan Boonman studies both bat wing sounds (Boonman et al. 2014) and owl wing sounds (Boonman et al. 2018). In the latter paper, he and others presented one of the few measurements of the wing sound of an owl taking off (Neuhaus et al. 1973;Thorpe and Griffin 1962), and showed that rodents were sensitive to these sounds. ...
Synopsis
Animal wings produce an acoustic signature in flight. Many owls are able to suppress this noise to fly quietly relative to other birds. Instead of silent flight, certain birds have conversely evolved to produce extra sound with their wings for communication. The papers in this symposium synthesize ongoing research in “animal aeroacoustics”: the study of how animal flight produces an acoustic signature, its biological context, and possible bio-inspired engineering applications. Three papers present research on flycatchers and doves, highlighting work that continues to uncover new physical mechanisms by which bird wings can make communication sounds. Quiet flight evolves in the context of a predator–prey interaction, either to help predators such as owls hear its prey better, or to prevent the prey from hearing the approaching predator. Two papers present work on hearing in owls and insect prey. Additional papers focus on the sounds produced by wings during flight, and on the fluid mechanics of force production by flapping wings. For instance, there is evidence that birds such as nightbirds, hawks, or falcons may also have quiet flight. Bat flight appears to be quieter than bird flight, for reasons that are not fully explored. Several research avenues remain open, including the role of flapping versus gliding flight or the physical acoustic mechanisms by which flight sounds are reduced. The convergent interest of the biology and engineering communities on quiet owl flight comes at a time of nascent developments in the energy and transportation sectors, where noise and its perception are formidable obstacles.
... The audible wing beats, representing noise pulses generated through friction, are audible at least on close range. Similar non-vocal sound-production through wing movements has been observed in Old World Fruit bats, although not in a social context but in a rudimentary form of echolocation [43]. In C. senex, this behavior might be connected to another morphological peculiarity: Wings of the bat show a distinct pattern of parallel folds between the 5 th and the 4 th digit [23] that might support the observed sound production. ...
Centurio senex is an iconic bat characterized by a facial morphology deviating far from all other New World Leaf Nosed Bats (Phyllostomidae). The species has a bizarrely wrinkled face and lacks the characteristic nose leaf. Throughout its distribution from Mexico to Northern South America the species is most of the time rarely captured and only scarce information on its behavior and natural history is available. Centurio senex is frugivorous and one of the few bats documented to consume also hard seeds. Interestingly, the species shows a distinct sexual dimorphism: Adult males have more pronounced facial wrinkles than females and a fold of skin under the chin that can be raised in style of a face mask. We report the first observations on echolocation and mating behavior of Centurio senex, including synchronized audio and video recordings from an aggregation of males in Costa Rica. Over a period of 6 weeks we located a total of 53 perches, where during the first half of the night males were hanging with raised facial masks at a mean height of 2.35 m. Most of the time, the males moved just their wing tips, and spontaneously vocalized in the ultrasound range. Approaches of other individuals resulted in the perching male beating its wings and emitting a very loud, low frequency whistling call. Following such an encounter we recorded a copula-tion event. The observed aggregation of adult C. senex males is consistent with lek court-ship, a behavior described from only few other bat species.
... As such, in addition to detecting bat echolocation calls (see below), eared insects could potentially detect bats by passive sound cues generated by their flight, or their echolocation calls. There are few examples of sounds produced by bat flight (Gould 1988;Bernal et al. 2007;Boonman et al. 2014). These sounds are low frequency and broadband with dominant frequencies <20 kHz. ...
Insects have a diversity of hearing organs known to function in a variety of contexts, including reproduction, locating food, and defence. While the role of hearing in predator avoidance has been extensively researched over the past several decades, this research has focused on the detection of one type of predator- echolocating bats. Here we reassess the role of hearing in antipredator defence by considering how insects use their ears to detect and avoid the wide range of predators that consume them. To identify the types of sounds that could be relevant to insect prey, we first review the topic of hearing-mediated predator avoidance in vertebrates. Sounds used by vertebrate prey to assess predation risk include incidental sound cues (e.g. flight sounds, rustling vegetation, splashing) produced by an approaching predator or another escaping prey, as well as communication signals produced by a predator (e.g. echolocation calls, songs) or non-predator (e.g. alarm calls). We then review what is known, and what is not known, about such sounds made by the main predators and parasitoids of insects (i.e. birds, bats, terrestrial vertebrates, invertebrates) and how insects respond to them. Three key insights emerged from our review. First, there is a lack of information on how both vertebrate and insect prey use passive sound cues produced by predators to avoid being captured. Second, while there are numerous examples of vertebrate prey eavesdropping on the calls and songs of predators and non-predators to assess risk, there are currently no such examples for eared insect prey. Third, the hearing sensitivity of many insects, including those with ears considered to be dedicated to detecting bats or mates, overlaps with both sound cues and signals generated by non-bat predators. Sounds of particular relevance to insect prey include the flight sounds and calls of insectivorous birds, the flight sounds of insect predators and parasitoids, and rustling vegetation sounds of birds and terrestrial predators. We conclude that research on the role of insect hearing in predator avoidance has been disproportionally focused on bat-detection, and that acoustically-mediated responses to other predators may have been overlooked because the responses of prey may be subtle (e.g. ceasing activity, increasing vigilance). We recommend that researchers expand their testing of hearing-mediated risk assessment in insects by considering the wide range of sounds generated by predators, and the varied responses exhibited by prey to these sounds.
... It has been hypothesized that increasing body size, dietary change, and less frequent roosting in caves are associated with the loss of laryngeal echolocation in megabats (Teeling et al. 2000;Giannini et al. 2012). Although no pteropodids echolocate laryngeally, some do produce sonar clicks via lingual echolocation or wing clapping perhaps as an adaptation for easier navigation in caves where they roost colonially (Gould 1988;Funakoshi et al. 1995;Speakman 2001;Yovel et al. 2011;Schoeman and Goodman 2012;Nesi et al. 2013;Boonman et al. 2014). While primarily frugivorous, some megabats are specialists on certain fruits or nectar, while others are generalists, even occasionally consuming insects (Birt et al. 1997;Kirsch and Lapointe 1997;Banack 1998;Dumont 2003;Barclay et al. 2006). ...
Variation in the dentition yields insight into the evolutionary history of Mammalia. However, to date, there has been limited research on the dental variation in Pteropodidae, a family of bats found throughout sub-Saharan Africa, Southeast Asia, and Oceania. Most species are large, diurnal, non-echolocating, and eat fruit or nectar. Pteropodids are of significant concern in conservation due to rapidly declining populations resulting from habitat loss, climate change, and their impacts on agriculture and disease. We collected dental metrics from the mandibular postcanine teeth of 101 pteropodid specimens spanning six species within the family to test three hypotheses: H1) dental metrics are significantly different across pteropodid species; H2) variation in pteropodid dental metrics is associated with variation in body size; and H3) variation in pteropodid dental proportions is associated with phylogenetic relatedness. We find that dental linear metrics vary significantly across pteropodids and are significantly associated with body size. In contrast, dental proportions of pteropodids reflect phylogenetic relationships. We propose that the combination of approaches for quantifying postcanine dental variation can elucidate and refine our understanding of the various selective forces that shaped the Pteropodidae radiation.
... Megabats are found throughout Africa, the Asian tropics, Australia, and many islands of the Indian and Pacific oceans where they play important ecological roles in seed dispersal and pollination (Nowak, 1994). Although some pteropodids use echolocation (Yovel et al., 2011;Lee et al., 2016;Boonman et al., 2014), most rely on vision and olfaction to navigate and find plant food sources. Pteropodidae is also functionally diverse; for example, it exhibits the widest variation in body size seen in any family of bats, ranging from 14 g to more than 1000 g . ...
... An African dispersal during the MMCO seems therefore a more likely hypothesis for Scotonycterini. Boonman, Bumrungsri, & Yovel (2014) have shown that three species of Asian fruit bats can produce click sounds in the dark by wing clapping: Cynopterus brachyotis, Eonycteris spelaea, and ...
Members of the family Pteropodidae, also known as Old World fruit bats, are represented in Africa by 14 genera and 44 species. Here, we sequenced 67 complete mitochondrial genomes from African and Asian pteropodids to better understand the evolutionary history of the subfamily Rousettinae, which includes most of the African species. An increased frequency of guanine to adenine transitions is detected in the mtDNA genomes of Macroglossus sobrinus and all species of Casinycteris and Scotonycteris. Our phylogenetic and molecular dating analyses based on 126 taxa and 15,448 characters indicate a low signal for deep relationships within the family, suggesting a rapid diversification during the Late Oligocene period of “warming.” Within the subfamily Rousettinae, most nodes are highly supported by our different analyses (all nucleotide sites, SuperTRI analyses of a sliding window, transversions only, coding genes only, and amino acid sequences). The results indicate the existence of four tribes: Rousettini—distributed from Africa through Mediterranean region and South Asia to South‐East Asia; Eonycterini—found in Asia; and Epomophorini and Scotonycterini—restricted to sub‐Saharan Africa. Although most interspecies relationships are highly supported, three parts of the Rousettinae mitochondrial tree are still unresolved, suggesting rapid diversification: (a) among the three subtribes Epomophorina (Epomophorus sensu lato, i.e., including Micropteropus, Epomops, Hypsignathus, Nanonycteris), Plerotina (Plerotes), and Myonycterina (Myonycteris, Megaloglossus) in the Late Miocene; (b) among Epomops, Hypsignathus, and other species of Epomophorina at the Pliocene–Pleistocene boundary; and (c) among Myonycteris species in the Early Pleistocene. Within the Epomophorini, Stenonycteris lanosus emerged first, suggesting that lingual echolocation may have appeared in the common ancestor of Epomophorini and Rousettini. Our analyses suggest that multiple events of mtDNA introgression occurred within the Epomophorus species complex during the Pleistocene.
... Although echolocation is a compelling adaptation to explore nocturnal environments, this sensory innovation is not ubiquitous among bats. Old World fruit bats (Pteropodidae) are incapable of generating laryngeal echolocation calls, though tongue and wingclick-based echolocation have been reported in some pteropodid species (Yovel et al. 2011;Boonman et al. 2014). In contrast, all remaining bat families exhibit laryngeal echolocation ( fig. ...
Bats are excellent models for studying the molecular basis of sensory adaptation. In Chiroptera, a sensory trade-off has been proposed between the visual and auditory systems, though the extent of this association has yet to be fully examined. To investigate whether variation in visual performance is associated with echolocation, we experimentally assayed the dim-light visual pigment rhodopsin from bat species with differing echolocation abilities. While spectral tuning properties were similar among bats, we found that the rate of decay of their light-activated state was significantly slower in a non-echolocating bat relative to species that use distinct echolocation strategies, consistent with a sensory trade-off hypothesis. We also found that these rates of decay were remarkably slower compared to those of other mammals, likely indicating an adaptation to dim light. To examine whether functional changes in rhodopsin are associated with shifts in selection intensity upon bat Rh1 sequences, we implemented selection analyses using codon-based likelihood clade models. While no shifts in selection were identified in response to diverse echolocation abilities of bats, we detected a significant increase in the intensity of evolutionary constraint accompanying the diversification of Chiroptera. Taken together, this suggests that substitutions that modulate the stability of the light-activated rhodopsin state were likely maintained through intensified constraint after bats diversified, being finely tuned in response to novel sensory specializations. Our study demonstrates the power of combining experimental and computational approaches for investigating functional mechanisms underlying the evolution of complex sensory adaptations.
... Wing communication sounds are produced in flight by birds that include flappet larks (Mirafra spp.) (Norberg, 1991), manakins (Bostwick and Prum, 2003) and guans (Delacour and Amadon, 1973); fruit bats (Boonman et al., 2014); and insects such as butterflies ( Yack et al., 2000), grasshoppers (Otte, 1970) and mosquitoes (Cator et al., 2009). In many of these examples, the wing sounds are produced only during displays, such that the communication sound is not also present in ordinary flight. ...
Wing trills are pulsed sounds produced by modified wing feathers at one or more specific points in time during a wingbeat. Male Allen's Hummingbird (Selasphorus sasin) produce a sexually dimorphic 9 kHz wing trill in flight. Here we investigate the kinematic basis for trill production. The wingtip velocity hypothesis posits that trill production is modulated by the airspeed of the wingtip at some point during the wingbeat, whereas the wing rotation hypothesis posits that trill production is instead modulated by wing rotation kinematics. To test these hypotheses, we flew six male Allen's Hummingbirds in an open jet wind tunnel at flight speeds of 0, 3, 6, 9, 12 and 14 m s-1, and recorded their flight with two 'acoustic cameras' placed below and behind, or below and lateral to the flying bird. The acoustic cameras are phased arrays of 40 microphones that used beamforming to spatially locate sound sources within a camera image. Trill Sound Pressure Level (SPL) exhibited a U-shaped relationship with flight speed in all three camera positions. SPL was greatest perpendicular to the stroke plane. Acoustic camera videos suggest that the trill is produced during supination. The trill was up to 20 dB louder during maneuvers than it was during steady state flight in the wind tunnel, across all airspeeds tested. These data provide partial support for the wing rotation hypothesis. Altered wing rotation kinematics could allow male Allen's Hummingbird to modulate trill production in social contexts such as courtship displays.
... Comparative studies of the hyoid and palate morphology between bats of the genus Rousettus and other genera of the same family may provide insights into the evolution of lingual echolocation. A recent study uncovered evidence that at least three other species of Pteropodidae produce clicks with their wings, which support navigation in the dark [31]. However, sonar-based navigation capability using wing clicks is more limited in comparison to that of Rousettus using tongue clicks, and it is thus likely that wing-clicking bats rely largely on visual input. ...
Animals enhance sensory acquisition from a specific direction by movements of head, ears or eyes. As active sensing animals, echolocating bats also aim their directional sonar beam to selectively “illuminate” a confined volume of space, facilitating efficient information processing by reducing echo interference and clutter. Such sonar beam control is generally achieved by head movements or shape changes of the sound-emitting mouth or nose. However, lingual-echolocating Egyptian fruit bats, Rousettus aegyptiacus, which produce sound by clicking their tongue, can dramatically change beam direction at very short temporal intervals without visible morphological changes. The mechanism supporting this capability has remained a mystery. Here we measured signals from free-flying Egyptian fruit bats and discovered a systematic angular sweep of beam focus across increasing frequency. This unusual signal structure has not been observed in other animals, and cannot be explained by the conventional and widely used “piston model” that describes the emission pattern of other bat species. Through modeling we show that the observed beam features can be captured by an array of tongue-driven sound sources located along the side of the mouth, and that the sonar beam direction can be steered parsimoniously by inducing changes to the pattern of phase differences through moving tongue location. The effects are broadly similar to those found in a phased array–an engineering design widely found in human-made sonar systems that enables beam direction changes without changes in the physical transducer assembly. Our study reveals an intriguing parallel between biology and human engineering in solving problems in fundamentally similar ways.
... De plus, Boonman a récemment démontré que de nombreux ptéropodidés (Eonycteris, Cynopterus et Macroglossus) produisaient des cliquetis avec leurs ailes dont les échos permettent de détecter et discriminer des objets dans l'obscurité. Ce système de repérage n'est pas la forme ancestrale de l'écholocation mais serait plutôt un comportement primitif, propre à ces chiroptères (Boonman et al., 2014). ...
Les zoonoses émergentes constituent un problème de santé publique majeur. A l'image des virus de l'immunodéficience humaine (VIH), influenza, ou encore Ebola, la plupart des pathogènes zoonotiques prennent leur origine chez la faune sauvage. Les chiroptères sont des réservoirs de virus zoonotiques qui peuvent provoquer des pathologies graves chez l'Homme, comme le virus de la rage ou le coronavirus responsable de la pandémie du syndrome respiratoire aigu sévère (SRAS) en 2003-2004. En Asie du Sud-Est, reconnue comme un point chaud d'émergence, les chiroptères sont régulièrement en contact avec l'Homme du fait de l'exploitation des mêmes environnements et des activités de chasse et de consommation de ces animaux sauvages. Le risque de transmission de potentiels virus des chiroptères à l'Homme reste encore très peu étudié, notamment au Cambodge et au Laos. C’est dans ce contexte que s’inscrit ce travail de thèse, qui a pour but de détecter et de caractériser des coronavirus et des astrovirus chez les chiroptères de ces deux pays, et d'explorer les environnements où le risque de transmission à l'Homme serait plus élevé.Un premier axe de travail a porté sur la détection et la caractérisation de ces deux familles virales chez des chiroptères échantillonnés de 2010 à 2013. Une forte diversité de coronavirus et d'astrovirus a été détectée chez de nombreux genres de chiroptères insectivores et frugivores. De nouveaux hôtes réservoirs et de nouvelles souches virales ont été mis en évidence, dont certaines sont relativement proches de souches pathogènes chez l'Homme ou chez d'autres espèces animales. Le deuxième axe d'étude visait une caractérisation plus approfondie des virus. L'étude des protéines impliquées dans l'entrée cellulaire (protéines de capside et de spicule pour les astrovirus et coronaivrus respectivement), permet d'évaluer le potentiel de passage de la barrière d'espèce de ces virus. Plusieurs techniques de séquençage ont été tentées, en particulier au niveau des gènes d'intérêt. Les résultats ont été très limités, et n'ont pas permis une caractérisation approfondie des souches. Néanmoins, ce travail a mis en évidence les points critiques et les approches à envisager dans l'optique d'un futur séquençage de ces virus.Enfin, le troisième axe de recherche a porté sur l'étude des facteurs environnementaux qui pourraient impacter les chiroptères et les potentiels virus zoonotiques qu'ils peuvent porter. Bien que les données aient été limitées, l'approche méthodologique et les pistes d'étude sont à retenir pour des études épidémiologiques futures. De plus les caractéristiques liées à la transformation des paysages naturels par l'Homme est un aspect important à prendre en compte.
... It is listed as a 'Near Threatened' species in the IUCN Red List with a decreasing population trend (Bates et al., 2008c).Payne et al., 1985). However, recent studies managed to show echolocating calls demonstrated by other pteropodids such as E. spelaea, C. brachyotis and M. minimus through wing clapping motion (Boonman et al., 2014). Records fromFukuda et al. (2009)showed the presence of this species in primary and secondary forests at Lambir Hills National Park. ...
A bat survey was conducted at Tumunong Hallu in Silam Coast Conservation Area (SCCA), Lahad Datu, Sabahfollowing the Silam Scientific Expedition 2015 from 7 th July until 5 th August 2015. A total of nine bat species belonging to two families were captured at SCCA. Among the noteworthy species recorded from this survey were Rhinolophus sedulus and Pteropus vampyrus, which are listed as Near Threatened in the IUCN Red List.
... Based on call frequency structures, the echolocation calls of bats are generally categorized into two major types: frequency modulated (FM) sweeps and constant frequency (CF) tones (Schnitzler et al. 2003). Interestingly, FM echolocating bats are not monophyletic in the species tree (Teeling et al. 2005), which provids a valuable system for exploring the molecular basis of improvement in FM echolocation because when echolocation originated, it was too rudimentary to allow bats to estimate distance accurately (Boonman et al. 2014). ...
Molecular basis for mammalian echolocation has been receiving much concerns. Recent findings on the parallel evolution of prestin sequences among echolocating bats and toothed whales suggest that adaptations for high-frequency hearing have occurred during the evolution of echolocation. Here, we report that although the species tree for echolocating bats emitting echolocation calls with frequency modulated (FM) sweeps is paraphyletic, prestin exhibits similar functional changes between FM bats. Site-directed mutagenesis shows that the amino acid 308S in FM bats is responsible for the similar functional changes of prestin We strongly support that the occurrence of serine at position 308 is a case of hemiplasy, caused by incomplete lineage sorting of an ancestral polymorphism. Our study not only reveals sophisticated molecular basis of echolocation in bats, also calls for caution in the inference of molecular convergence in species experiencing rapid radiation.
... The appearance of beacons on an Old World plant raises interesting questions about the behaviour and sensory capacity of Old World nectarfeeding bats (Fenton and Simmons, 2015). The demonstration (Boonman et al., 2014) that some flower-visiting genera of pteropodids have some capacity for fundamental echolocation may indicate the potential importance of ultrasonic beacons for Old World flower-visiting bats. ...
The evolution of cue reception and cue production is well documented. The ability of species to use cues they did not evolve with is important in understanding flexibility in behaviour. We observed Neotropical nectar-feeding bats (Glossophaga soricina) feeding at Old World banana flowers (Musa acuminata) in a Belize garden. The flowers produce a rich source of nectar that is exposed as a bract lifts before dusk. We tested the hypothesis that the bracts serve as beacons to foraging bats and discuss this approach and the use of acoustic information by bats feeding at flowers. We ensonified a bract with cues like those of echolocating G. soricina, which revealed the production of strong echoes from the bract. Additionally, the removal of bracts from the flowers influenced the bats' flower-visiting behaviour. We suggest that the bats use the echoes from the bract opportunistically as a cue to find the nectar source. Our findings provide an example of an interaction between a plant and flower visitor not reflecting a shared evolutionary past.
... The Pteropodidae includes a suite of fruit-and nectar-feeding bats, which range in size from relatively small (~ 10 g) to massive (>1.5 kg). While several species of pteropodid are known to echolocate in darkness with simple clicks produced from the tongue or wings (Roberts 1975;Boonman et al. 2014), they navigate principally by visual cues. This characteristic makes them relatively easy to capture, especially the smaller species, and capture effort is essential for surveying this group. ...
The relatively remote islands of Manus and Mussau, located in the northern portion of the Bismark sea have been long identified as key biodiversity areas in Papua New Guinea and within greater Melanesia. Manus Island has long been known for its endemism and relatively intact forest, while Mussau Island, although relatively unstudied, has been recognised as an Endemic Bird Area. This report documents the findings of a series of rapid biodiversity surveys focusing on terrestrial flora and fauna, funded by the Critical Ecosystems Partnership Fund ,encompassing four sites across the islands of Manus and Mussau; undertaken by a WCS led team of national and international taxonomic specialists in October 2014. The objective of these surveys was to investigate the biodiversity values of these areas. In conjunction with participatory community work conducted prior to, and following the surveys the wider WCS project aims to identify options for natural resource management in the region which addresses both community and biodiversity needs.
... In the Neotropics, a few bat-pollinated plants found an efficient solution to attract bats by developing floral ultrasound reflectors [7,9], which enabled them to exploit the bats' echolocation system. However, such reflectors have never been described for plants outside the Neotropics, probably because in the Paleotropics, chiropterophilous plants are pollinated by fruit bats (Pteropodidae) that are unlikely to use echolocation for foraging [16,17]. We hypothesized that this phenomenon can also be found in the Paleotropics. ...
Mutualisms between plants and animals shape the world’s ecosystems [1 and 2]. In such interactions, achieving contact with the partner species is imperative. Plants regularly advertise themselves with signals that specifically appeal to the partner’s perceptual preferences [3, 4 and 5]. For example, many plants have acquired traits such as brightly colored, fragrant flowers that attract pollinators with visual, olfactory, or—in the case of a few bat-pollinated flowers—even acoustic stimuli in the form of echo-reflecting structures [6, 7, 8 and 9]. However, acoustic attraction in plants is rare compared to other advertisements and has never been found outside the pollination context and only in the Neotropics. We hypothesized that this phenomenon is more widespread and more diverse as plant-bat interactions also occur in the Paleotropics. In Borneo, mutualistic bats fertilize a carnivorous pitcher plant while roosting in its pitchers [10 and 11]. The pitcher’s orifice features a prolonged concave structure, which we predicted to distinctively reflect the bats’ echolocation calls for a wide range of angles. This structure should facilitate the location and identification of pitchers even within highly cluttered surroundings. Pitchers lacking this structure should be less attractive for the bats. Ensonifications of the pitchers around their orifice revealed that this structure indeed acts as a multidirectional ultrasound reflector. In behavioral experiments where bats were confronted with differently modified pitchers, the reflector’s presence clearly facilitated the finding and identification of pitchers. These results suggest that plants have convergently acquired reflectors in the Paleotropics and the Neotropics to acoustically attract bats, albeit for completely different ecological reasons.
... In the Neotropics, a few bat-pollinated plants found an efficient solution to attract bats by developing floral ultrasound reflectors [7,9], which enabled them to exploit the bats' echolocation system. However, such reflectors have never been described for plants outside the Neotropics, probably because in the Paleotropics, chiropterophilous plants are pollinated by fruit bats (Pteropodidae) that are unlikely to use echolocation for foraging [16,17]. We hypothesized that this phenomenon can also be found in the Paleotropics. ...
Mutualisms between plants and animals shape the world's ecosystems [1, 2]. In such interactions, achieving contact with the partner species is imperative. Plants regularly advertise themselves with signals that specifically appeal to the partner's perceptual preferences [3-5]. For example, many plants have acquired traits such as brightly colored, fragrant flowers that attract pollinators with visual, olfactory, or-in the case of a few bat-pollinated flowers-even acoustic stimuli in the form of echo-reflecting structures [6-9]. However, acoustic attraction in plants is rare compared to other advertisements and has never been found outside the pollination context and only in the Neotropics. We hypothesized that this phenomenon is more widespread and more diverse as plant-bat interactions also occur in the Paleotropics. In Borneo, mutualistic bats fertilize a carnivorous pitcher plant while roosting in its pitchers [10, 11]. The pitcher's orifice features a prolonged concave structure, which we predicted to distinctively reflect the bats' echolocation calls for a wide range of angles. This structure should facilitate the location and identification of pitchers even within highly cluttered surroundings. Pitchers lacking this structure should be less attractive for the bats. Ensonifications of the pitchers around their orifice revealed that this structure indeed acts as a multidirectional ultrasound reflector. In behavioral experiments where bats were confronted with differently modified pitchers, the reflector's presence clearly facilitated the finding and identification of pitchers. These results suggest that plants have convergently acquired reflectors in the Paleotropics and the Neotropics to acoustically attract bats, albeit for completely different ecological reasons.
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This comprehensive species-specific chapter covers all aspects of this mammal’s biology, including paleontology, physiology, genetics, reproduction and development, ecology, habitat, diet, mortality, and behavior. The economic significance and management of mammals and future challenges for research and conservation are addressed as well. The chapter includes a distribution map, a photograph of the animal, and a list of key literature.
Brock Fenton has devoted his career to the study of the ecological adaptations of bat diversity. In this paper we describe his interest and research on the subject of bat evolution and how he has used phylogenetic hypotheses to revise our understanding of divergences and convergences of specific traits within this mammalian order. While he has always been fascinated by the evolution of echolocation, he has also written about the evolution of reproductive, morphological and behavioural traits. Recent methods of documenting diversity incorporate his lifelong love of photography. We describe taxonomic attempts to honour his contributions to bat species diversity. Brock has inspired hundreds of students and colleagues with his endless enthusiasm and generosity and inspired them with ongoing evolutionary research on bats.
Biomechanics is poised at the intersection of organismal form, function, and ecology, and forms a practical lens through which to investigate evolutionary linkages among these factors. We conducted the first evolutionary analysis of bat flight dynamics by examining the phylogenetic patterning of landing mechanics. We discovered that bats perform stereotyped maneuvers that are correlated with landing performance quantified as impact force, and that these are linked with roosting ecology, a critical aspect of bat biology. Our findings suggest that bat ancestors performed simple, four-limbed landings, similar to those performed by gliding mammals, and that more complex landings evolved in association with novel roost types. This explicit connection between ecology and biomechanics presents the opportunity to identify traits that are associated with a locomotor behavior of known ecological relevance, thus laying the foundation for a broader understanding of the evolution of flight and wing architecture in this extraordinarily successful mammalian lineage.
Over 20% of all living mammals are bats (order Chiroptera). Bats possess extraordinary adaptations including powered flight, laryngeal echolocation and a unique immune system that enables them to tolerate a diversity of viral infections without presenting clinical disease symptoms. They occupy multiple trophic niches and environments globally. Significant physiological and ecological diversity occurs across the order. Bats also exhibit extreme longevity given their body size with many species showing few signs of ageing. The molecular basis of this extended longevity has recently attracted attention. Telomere maintenance potentially underpins bats’ extended healthspan, although functional studies are still required to validate the causative mechanisms. In this review, we detail the current knowledge on bat telomeres, telomerase expression, and how these relate to ecology, longevity and life‐history strategies. Patterns of telomere shortening and telomerase expression vary across species, and comparative genomic analyses suggest that alternative telomere maintenance mechanisms evolved in the longest lived bats. We discuss the unique challenges faced when working with populations of wild bats and highlight ways to advance the field including expanding long‐term monitoring across species that display contrasting life‐histories and occupy different environmental niches. We further review how new high quality, chromosome‐level genome assemblies can enable us to uncover the molecular mechanisms governing telomere dynamics and how phylogenomic analyses can reveal the adaptive significance of telomere maintenance and variation in bats.
Aim . The aim of this work was to briefly summarize the current understanding of the phenomenon of echolocation in the order of bats (Chiroptera Blumenbach, 1779). Discussion . The paper discusses: the place of bats among other taxonomic groups of animals that have the ability of echolocation; the history of the discovery of "ear vision" in bats by L. Spallanzani in the 18th century; the first scientifically based assumptions regarding the use of ultrasound by bats and the discovery of this phenomenon in the middle of the last century; methods for emitting and receiving ultrasound by various taxonomic groups of bats; physical patterns underlying the propagation of ultrasonic waves; characteristics of the returned echo and algorithms for echolocation in bats; echolocation interactions between insectivorous bats and nocturnal moths and possibilities for ultrasonic monitoring of bat populations. Conclusion . The inclusion of ultrasound monitoring of bat populations in integrated ecological and virological studies could form a new point of growth in systems to ensure biological security at both national and global levels.
Significance
How do we build a perception from incoming sensory information? To accurately perceive the environment, the brain has to integrate information across different sensory modalities and to analyze multiple sensory dimensions within a sensory modality. We studied this integration in echolocating bats, the masters of active acoustic sensing. By presenting them with targets whose acoustic dimensions were incoherent, we managed to induce misperception, which caused the bats to repeatedly try to fly through a wall even though they detected it with their echolocation. We demonstrate that certain relations between the dimensions must hold to allow accurate perception. Nevertheless, adult bats can learn new relations rapidly. Notably, no misperception was observed in pups, confirming that these relations are not innate.
Knowing their way around
The presence of a cognitive map is essential to our ability to navigate through areas we know because it facilitates the use of spatial knowledge to derive new routes. Whether such maps exist in nonhuman animals has been debated, largely because of the difficulty of demonstrating qualifying components of the map outside of a laboratory. In two studies on Egyptian fruit bats, Harten et al. and Toledo et al. together show that this species's navigational strategies meet the requirements for the use of a cognitive map of their environment, confirming that this skill occurs outside of humans (see the Perspective by Fenton).
Science , this issue p. 194 , p. 188 ; see also p. 142
Synopsis
Animal flight noise can serve as an inspiration to engineering solutions to wind-noise problems in planes or wind turbines. Here we investigate the acoustics of wingbeats in birds and bats by co-registering wing-movement in natural flight with acoustic noise. To understand the relationships between wing movement and acoustics, we conducted additional acoustic measurements of single moving wings and other moving surfaces with accurately tracked motion paths. We found a correlation between wing-surface area and the sound pressure level of wingbeats; with bats tending to produce lower levels than birds. Measuring moving wings in isolation showed that a downstroke toward a microphone causes negative sound pressure that flips back into positive pressure at the reversal to the upstroke. The flip back to positive pressure is unrelated to the action of the upstroke, but occurs when the downward motion is halted. If the microphone is positioned above the downward wingbeat, then sound pressure instead quickly rises during the downward motion of the wing. The phase pattern of the impulse created by the wingbeat varies systematically with recording-angle. The curvature of the wing appears to be a determinant of the average frequency of the acoustic impulse. Our findings can be used to predict the acoustics of smaller flying animals where repetition pitch of similar underlying impulses, repeated at much higher wingbeat-rates become dominant.
Synopsis
We raise and explore possible answers to three questions about the evolution and ecology of silent flight of owls: (1) do owls fly silently for stealth, or is it to reduce self-masking? Current evidence slightly favors the self-masking hypothesis, but this question remains unsettled. (2) Two of the derived wing features that apparently evolved to suppress flight sound are the vane fringes and dorsal velvet of owl wing feathers. Do these two features suppress aerodynamic noise (sounds generated by airflow), or do they instead reduce structural noise, such as frictional sounds of feathers rubbing during flight? The aerodynamic noise hypothesis lacks empirical support. Several lines of evidence instead support the hypothesis that the velvet and fringe reduce frictional sound, including: the anatomical location of the fringe and velvet, which is best developed in wing and tail regions prone to rubbing, rather than in areas exposed to airflow; the acoustic signature of rubbing, which is broadband and includes ultrasound, is present in the flight of other birds but not owls; and the apparent relationship between the velvet and friction barbules found on the remiges of other birds. (3) Have other animals also evolved silent flight? Wing features in nightbirds (nocturnal members of Caprimulgiformes) suggest that they may have independently evolved to fly in relative silence, as have more than one diurnal hawk (Accipitriformes). We hypothesize that bird flight is noisy because wing feathers are intrinsically predisposed to rub and make frictional noise. This hypothesis suggests a new perspective: rather than regarding owls as silent, perhaps it is bird flight that is loud. This implies that bats may be an overlooked model for silent flight. Owl flight may not be the best (and certainly, not the only) model for “bio-inspiration” of silent flight.
Echolocation allows toothed whales to adapt to underwater habitats where vision is ineffective. Because echolocation requires the ability to detect exceptional high-frequency sounds, fossils related to the auditory system can help to pinpoint the origin of echolocation in whales. However, because of conflicting interpretations of archaeocete fossils, when and how whales evolved the high-frequency hearing correlated with echolocation remain unclear. We address these questions at the molecular level by systematically investigating the convergent evolution of 7206 orthologs across 16 mammals and find that convergent genes between the last common ancestor of all whales (LCAW) and echolocating bats are not significantly enriched in functional categories related to hearing, and that convergence in hearing-related proteins between them is not stronger than that between nonecholocating mammalian lineages and echolocating bats. However, these results contrast with those of parallel analyses between the LCA of toothed whales (LCATW) and echolocating bats. Furthermore, we reconstruct the ancestral genes for the hearing protein prestin for the LCAW and LCATW; we show that the LCAW prestin exhibits the same function as that of nonecholocating mammals, but the LCATW prestin shows functional convergence with that of extant echolocating mammals. Mutagenesis shows that functional convergence of prestin is driven by convergent changes in the prestins S392A and L497M in the LCATW and echolocating bats. Our results provide genomic and functional evidence supporting the origin of high-frequency hearing in the LCAW, not the LCATW, and reveal molecular insights into the origin and evolutionary trajectories of echolocation in whales.
Bats have evolved a plethora of adaptations
in response to the challenges of their diverse habitats
and the physics of sound propagation
. Such adaptations
can confound investigations of adaptations that arise in response to prey. Here, we review the adaptations in the echolocation and foraging behaviour of bats. Bats use a variety of foraging modes including aerial hawking
and gleaning
. The main challenge to bats echolocating in clutter
is increased resolution to detect small objects, be they insects or twigs, and overcoming the masking
effects that result from the overlap
of echoes from prey and the background. Low-duty-cycle
echolocating bats that aerial hawk in clutter have evolved short, frequency-modulated calls with high bandwidth
that increase resolution and minimizes masking effects
. Bats that glean prey from the vegetation have similar adaptations but in addition use passive listening
and/or 3-D flight
to ensonify substrate-bound prey from different directions. High-duty-cycle
echolocating bats have evolved Doppler-shift
compensation which allows the detection
of acoustic glints
from the flapping wings of insects. Bats that aerial hawk in the open have to search large volumes of space efficiently and use narrowband
, low-frequency (for decrease atmospheric attenuation
) echolocation
calls that maximize detection distance
. The wings and echolocation of bats form an adaptive complex. Bats that forage in clutter where distances are short have short broad wings for slow, manoeuvrable
flight. Bats that hunt in the open where detection distances are long have long narrow wings for fast, agile flight.
This chapter is intended to identify some of the major challenges that only now emerge as technically feasible when studying hearing in bats. These technical advances include all aspects of biological research, from novel genetic tools to novel recording techniques of ultrasonic audio, high-speed video, and global positioning data. Most recently, on-board and telemetric recording techniques for both ultrasound and electrode signals allow for unprecedented insight into the neuroethology of bat hearing and echolocation from awake and behaving animals engaged in a clearly defined perceptual task. Only with these new techniques will we be able to address specializations in the bat vocalization and auditory systems, from its genetic foundations to its behavioral dynamics. We hope that the current chapter is received as an ‘appetizer’ for young biologists across disciplines to focus their scientific efforts onto the fascinating topic of how it is to be a bat that has made the nocturnal air space its home.
An increasingly asked question is ‘can we confidently link bats with emerging viruses?’. No, or not yet, is the qualified answer based on the evidence available. Although more than 200 viruses – some of them deadly zoonotic viruses – have been isolated from or otherwise detected in bats, the supposed connections between bats, bat viruses and human diseases have been raised more on speculation than on evidence supporting their direct or indirect roles in the epidemiology of diseases (except for rabies). However, we are convinced that the evidence points in that direction and that at some point it will be proved that bats are competent hosts for at least a few zoonotic viruses. In this review, we cover aspects of bat biology, ecology and evolution that might be relevant in medical investigations and we provide a historical synthesis of some disease outbreaks causally linked to bats. We provide evolutionary-based hypotheses to tentatively explain the viral transmission route through mammalian intermediate hosts and to explain the geographic concentration of most outbreaks, but both are no more than speculations that still require formal assessment.
There is currently considerable interest in the consequences of loss in one sensory modality on the remaining senses. Much of this work has focused on the development of enhanced auditory abilities among blind individuals, who are often able to use sound to navigate through space. It has now been established that many blind individuals produce sound emissions and use the returning echoes to provide them with information about objects in their surroundings, in a similar manner to bats navigating in the dark. In this review, we summarize current knowledge regarding human echolocation. Some blind individuals develop remarkable echolocation abilities, and are able to assess the position, size, distance, shape, and material of objects using reflected sound waves. After training, normally sighted people are also able to use echolocation to perceive objects, and can develop abilities comparable to, but typically somewhat poorer than, those of blind people. The underlying cues and mechanisms, operable range, spatial acuity and neurological underpinnings of echolocation are described. Echolocation can result in functional real life benefits. It is possible that these benefits can be optimized via suitable training, especially among those with recently acquired blindness, but this requires further study. Areas for further research are identified.
Evolution is typically thought to proceed through divergence of genes, proteins and ultimately phenotypes. However, similar traits might also evolve convergently in unrelated taxa owing to similar selection pressures. Adaptive phenotypic convergence is widespread in nature, and recent results from several genes have suggested that this phenomenon is powerful enough to also drive recurrent evolution at the sequence level. Where homoplasious substitutions do occur these have long been considered the result of neutral processes. However, recent studies have demonstrated that adaptive convergent sequence evolution can be detected in vertebrates using statistical methods that model parallel evolution, although the extent to which sequence convergence between genera occurs across genomes is unknown. Here we analyse genomic sequence data in mammals that have independently evolved echolocation and show that convergence is not a rare process restricted to several loci but is instead widespread, continuously distributed and commonly driven by natural selection acting on a small number of sites per locus. Systematic analyses of convergent sequence evolution in 805,053 amino acids within 2,326 orthologous coding gene sequences compared across 22 mammals (including four newly sequenced bat genomes) revealed signatures consistent with convergence in nearly 200 loci. Strong and significant support for convergence among bats and the bottlenose dolphin was seen in numerous genes linked to hearing or deafness, consistent with an involvement in echolocation. Unexpectedly, we also found convergence in many genes linked to vision: the convergent signal of many sensory genes was robustly correlated with the strength of natural selection. This first attempt to detect genome-wide convergent sequence evolution across divergent taxa reveals the phenomenon to be much more pervasive than previously recognized.
The Neotropical frog-eating bat, Trachops cirrhosus, primarily hunts stationary prey, either by gleaning on the wing, or in a sit-and-wait mode hanging from a perch. It listens passively for prey-generated sounds, but uses echolocation in all stages of the hunt. Like other bats in the family Phyllostomidae, T. cirrhosus has a conspicuous nose leaf, hypothesized to direct and focus echolocation calls emitted from the nostrils. T. cirrhosus is highly flexible in its cognitive abilities and its use of sensory strategies for prey detection. Additionally, T. cirrhosus has been observed to echolocate both with closed and open mouth. We hypothesize that its flexibility extends to echolocation call design. We investigated the effect of hunting mode, perching or flying, as well as the effect of mouth opening, on the acoustic parameters and directionality of the echolocation call. We used a multi-microphone array, a high-speed video camera, and a microphone-diode-video system to directly visualize the echolocation sound beam synchronized with the bat's behavior. We found that T. cirrhosus emits a highly directional sound beam with half amplitude angle (HAM) of 12-18° and DI (directionality index) of ~17 dB, among the most directional bat sonar beams measured to date. The directionality was high both when flying and when perching. The emitted intensity was low, around 88 dB SPL at 10 cm from the mouth, when hanging, but higher, around 100 dB SPL at 10 cm, when flying or just before take-off. Our data suggests that the limited search volume of T. cirrhosus sonar beam defined by the high directionality and the rather low intensity of its echolocation calls is adapted to the highly cluttered hunting habitat and to the perch hunting mode.
The discovery of ultrasonic bat echolocation prompted a wide search for other animal biosonar systems, which yielded, among few others, two avian groups. One, the South American Oilbird (Steatornis caripensis: Caprimulgiformes), is nocturnal and eats fruit. The other is a selection of diurnal, insect-eating swiftlets (species in the genera Aerodramus and Collocalia: Apodidae) from across the Indo-Pacific. Bird echolocation is restricted to lower frequencies audible to humans, implying a system of poorer resolution than the ultrasonic (>20 kHz) biosonar of most bats and toothed whales. As such, bird echolocation has been labeled crude or rudimentary. Yet, echolocation is found in at least 16 extant bird species and has evolved several times in avian lineages. Birds use their syringes to produce broadband click-type biosonar signals that allow them to nest in dark caves and tunnels, probably with less predation pressure. There are ongoing discrepancies about several details of bird echolocation, from signal design to the question about whether echolocation is used during foraging. It remains to be seen if bird echolocation is as sophisticated as that of tongue-clicking rousette bats. Bird echolocation performance appears to be superior to that of blind humans using signals of notable similarity. However, no apparent specializations have been found so far in the birds' auditory system (from middle ear to higher processing centers). The advent of light-weight recording equipment and custom software for examining signals and reconstructing flight paths now provides the potential to study the echolocation behavior of birds in more detail and resolve such issues.
Great advances have been made recently in understanding the genetic basis of the sensory biology of bats. Research has focused on the molecular evolution of candidate sensory genes, genes with known functions [e.g., olfactory receptor (OR) genes] and genes identified from mutations associated with sensory deficits (e.g., blindness and deafness). For example, the FoxP2 gene, underpinning vocal behavior and sensorimotor coordination, has undergone diversification in bats, while several genes associated with audition show parallel amino acid substitutions in unrelated lineages of echolocating bats and, in some cases, in echolocating dolphins, representing a classic case of convergent molecular evolution. Vision genes encoding the photopigments rhodopsin and the long-wave sensitive opsin are functional in bats, while that encoding the short-wave sensitive opsin has lost functionality in rhinolophoid bats using high-duty cycle laryngeal echolocation, suggesting a sensory trade-off between investment in vision and echolocation. In terms of olfaction, bats appear to have a distinctive OR repertoire compared with other mammals, and a gene involved in signal transduction in the vomeronasal system has become non-functional in most bat species. Bitter taste receptors appear to have undergone a "birth-and death" evolution involving extensive gene duplication and loss, unlike genes coding for sweet and umami tastes that show conservation across most lineages but loss in vampire bats. Common vampire bats have also undergone adaptations for thermoperception, via alternative splicing resulting in the evolution of a novel heat-sensitive channel. The future for understanding the molecular basis of sensory biology is promising, with great potential for comparative genomic analyses, studies on gene regulation and expression, exploration of the role of alternative splicing in the generation of proteomic diversity, and linking genetic mechanisms to behavioral consequences.
Molecular and morphological data have important roles in
illuminating evolutionary history. DNA data often yield well resolved
phylogenies for living taxa, but are generally unattainable for
fossils. A distinct advantage of morphology is that some types of
morphological data may be collected for extinct and extant taxa.
Fossils provide a unique window on evolutionary history and may
preserve combinations of primitive and derived characters that are not
found in extant taxa. Given their unique character complexes, fossils
are critical in documenting sequences of character transformation over
geologic time and may elucidate otherwise ambiguous patterns of
evolution that are not revealed by molecular data alone. Here, we
employ a methodological approach that allows for the integration of
molecular and paleontological data in deciphering one of the most
innovative features in the evolutionary history of mammals—laryngeal
echolocation in bats. Molecular data alone, including an expanded data
set that includes new sequences for the A2AB gene, suggest that
microbats are paraphyletic but do not resolve whether laryngeal
echolocation evolved independently in different microbat lineages or
evolved in the common ancestor of bats and was subsequently lost in
megabats. When scaffolds from molecular phylogenies are incorporated
into parsimony analyses of morphological characters, including
morphological characters for the Eocene taxa
Icaronycteris, Archaeonycteris,
Hassianycteris, and Palaeochiropteryx,
the resulting trees suggest that laryngeal echolocation evolved in the
common ancestor of fossil and extant bats and was subsequently lost in
megabats. Molecular dating suggests that crown-group bats last shared a
common ancestor 52 to 54 million years ago.
Introduction
Many mammals have evolved highly adapted hearing associated with ecological specialisation. Of these, bats possess the widest frequency range of vocalisations and associated hearing sensitivities, with frequencies of above 200 kHz in some lineages that use laryngeal echolocation. High frequency hearing in bats appears to have evolved via structural modifications of the inner ear, however, studying these minute features presents considerable challenges and hitherto few such attempts have been made. To understand these adaptations more fully, as well as gain insights into the evolutionary origins of ultrasonic hearing and echolocation in bats, we undertook micro-computed tomography (μCT) scans of the cochleae of representative bat species from 16 families, encompassing their broad range of ecological diversity. To characterise cochlear gross morphology, we measured the relative basilar membrane length and number of turns, and compared these values between echolocating and non-echolocating bats, as well as other mammals.
Results
We found that hearing and echolocation call frequencies in bats correlated with both measures of cochlear morphology. In particular, relative basilar membrane length was typically longer in echolocating species, and also correlated positively with the number of cochlear turns. Ancestral reconstructions of these parameters suggested that the common ancestor of all extant bats was probably capable of ultrasonic hearing; however, we also found evidence of a significant decrease in the rate of morphological evolution of the basilar membrane in multiple ancestral branches within the Yangochiroptera suborder. Within the echolocating Yinpterochiroptera, there was some evidence of an increase in the rate of basilar membrane evolution in some tips of the tree, possibly associated with reported shifts in call frequency associated with recent speciation events.
Conclusions
The two main groups of echolocating bat were found to display highly variable inner ear morphologies. Ancestral reconstructions and rate shift analyses of ear morphology point to a complex evolutionary history, with the former supporting ultrasonic hearing in the common bat ancestor but the latter suggesting that morphological changes associated with echolocation might have occurred later. These findings are consistent with theories that sophisticated laryngeal echolocation, as seen in modern lineages, evolved following the divergence of the two main suborders.
Bats (order Chiroptera) are one of the few orders of mammals that echolocate and the only group with the capacity for powered flight. The order is subdivided into Microchiroptera and Megachiroptera, with an array of characteristics defining each group, including complex laryngeal echolocation systems in microbats and enhanced visual acuity in megabats. The respective monophylies of the two suborders have been tacitly assumed, although microbat monophyly is uncorroborated by molecular data. Here we present a phylogenetic analysis of bat relationships using DNA sequence data from four nuclear genes and three mitochondrial genes (total of 8,230 base pairs), indicating that microbat families in the superfamily Rhinolophoidea are more closely related to megabats than they are to other microbats. This implies that echolocation systems either evolved independently in rhinolophoids and other microbats or were lost in the evolution of megabats. Our data also reject flying lemur (order Dermoptera) as the bat sister group, indicating that presumed shared derived characters for flying lemurs and bats are convergent features that evolved in association with gliding and flight, respectively.
Cases of convergent evolution - where different lineages have evolved similar traits independently - are common and have proven central to our understanding of selection. Yet convincing examples of adaptive convergence at the sequence level are exceptionally rare [1]. The motor protein Prestin is expressed in mammalian outer hair cells (OHCs) and is thought to confer high frequency sensitivity and selectivity in the mammalian auditory system [2]. We previously reported that the Prestin gene has undergone sequence convergence among unrelated lineages of echolocating bat [3]. Here we report that this gene has also undergone convergent amino acid substitutions in echolocating dolphins, which group with echolocating bats in a phylogenetic tree of Prestin. Furthermore, we find evidence that these changes were driven by natural selection.
The family Pteropodidae comprises bats commonly known as megabats or Old World fruit bats. Molecular phylogenetic studies of pteropodids have provided considerable insight into intrafamilial relationships, but these studies have included only a fraction of the extant diversity (a maximum of 26 out of the 46 currently recognized genera) and have failed to resolve deep relationships among internal clades. Here we readdress the systematics of pteropodids by applying a strategy to try to resolve ancient relationships within Pteropodidae, while providing further insight into subgroup membership, by 1) increasing the taxonomic sample to 42 genera; 2) increasing the number of characters (to >8,000 bp) and nuclear genomic representation; 3) minimizing missing data; 4) controlling for sequence bias; and 5) using appropriate data partitioning and models of sequence evolution.
Our analyses recovered six principal clades and one additional independent lineage (consisting of a single genus) within Pteropodidae. Reciprocal monophyly of these groups was highly supported and generally congruent among the different methods and datasets used. Likewise, most relationships within these principal clades were well resolved and statistically supported. Relationships among the 7 principal groups, however, were poorly supported in all analyses. This result could not be explained by any detectable systematic bias in the data or incongruence among loci. The SOWH test confirmed that basal branches' lengths were not different from zero, which points to closely-spaced cladogenesis as the most likely explanation for the poor resolution of the deep pteropodid relationships. Simulations suggest that an increase in the amount of sequence data is likely to solve this problem.
The phylogenetic hypothesis generated here provides a robust framework for a revised cladistic classification of Pteropodidae into subfamilies and tribes and will greatly contribute to the understanding of character evolution and biogeography of pteropodids. The inability of our data to resolve the deepest relationships of the major pteropodid lineages suggests an explosive diversification soon after origin of the crown pteropodids. Several characteristics of pteropodids are consistent with this conclusion, including high species diversity, great morphological diversity, and presence of key innovations in relation to their sister group.
Echolocating bats of the genus Rousettus produce click sonar signals, using their tongue (lingual echolocation). These signals are often considered rudimentary and are believed to enable only crude performance. However, the main argument supporting this belief, namely the click's reported long duration, was recently shown to be an artifact. In fact, the sonar clicks of Rousettus bats are extremely short, ~50-100 μs, similar to dolphin vocalizations. Here, we present a comparison between the sonar systems of the 'model species' of laryngeal echolocation, the big brown bat (Eptesicus fuscus), and that of lingual echolocation, the Egyptian fruit bat (Rousettus aegyptiacus). We show experimentally that in tasks, such as accurate landing or detection of medium-sized objects, click-based echolocation enables performance similar to laryngeal echolocators. Further, we describe a sophisticated behavioral strategy for biosonar beam steering in clicking bats. Finally, theoretical analyses of the signal design--focusing on their autocorrelations and wideband ambiguity functions--predict that in some aspects, such as target ranging and Doppler-tolerance, click-based echolocation might outperform laryngeal echolocation. Therefore, we suggest that click-based echolocation in bats should be regarded as a viable echolocation strategy, which is in fact similar to the biosonar used by most echolocating animals, including whales and dolphins.
Is centering a stimulus in the field of view an optimal strategy to localize and track it? We demonstrated, through experimental
and computational studies, that the answer is no. We trained echolocating Egyptian fruit bats to localize a target in complete
darkness, and we measured the directional aim of their sonar clicks. The bats did not center the sonar beam on the target,
but instead pointed it off axis, accurately directing the maximum slope (“edge”) of the beam onto the target. Information-theoretic
calculations showed that using the maximum slope is optimal for localizing the target, at the cost of detection. We propose
that the tradeoff between detection (optimized at stimulus peak) and localization (optimized at maximum slope) is fundamental
to spatial localization and tracking accomplished through hearing, olfaction, and vision.
Echolocation is an active form of orientation in which animals emit sounds and then listen to reflected echoes of those sounds to form images of their surroundings in their brains. Although echolocation is usually associated with bats, it is not characteristic of all bats. Most echolocating bats produce signals in the larynx, but within one family of mainly non-echolocating species (Pteropodidae), a few species use echolocation sounds produced by tongue clicks. Here we demonstrate, using data obtained from micro-computed tomography scans of 26 species (n = 35 fluid-preserved bats), that proximal articulation of the stylohyal bone (part of the mammalian hyoid apparatus) with the tympanic bone always distinguishes laryngeally echolocating bats from all other bats (that is, non-echolocating pteropodids and those that echolocate with tongue clicks). In laryngeally echolocating bats, the proximal end of the stylohyal bone directly articulates with the tympanic bone and is often fused with it. Previous research on the morphology of the stylohyal bone in the oldest known fossil bat (Onychonycteris finneyi) suggested that it did not echolocate, but our findings suggest that O. finneyi may have used laryngeal echolocation because its stylohyal bones may have articulated with its tympanic bones. The present findings reopen basic questions about the timing and the origin of flight and echolocation in the early evolution of bats. Our data also provide an independent anatomical character by which to distinguish laryngeally echolocating bats from other bats.
The remarkable high-frequency sensitivity and selectivity of the mammalian auditory system has been attributed to the evolution of mechanical amplification, in which sound waves are amplified by outer hair cells in the cochlea. This process is driven by the recently discovered protein prestin, encoded by the gene Prestin. Echolocating bats use ultrasound for orientation and hunting and possess the highest frequency hearing of all mammals. To test for the involvement of Prestin in the evolution of bat echolocation, we sequenced the coding region in echolocating and nonecholocating species. The resulting putative gene tree showed strong support for a monophyletic assemblage of echolocating species, conflicting with the species phylogeny in which echolocators are paraphyletic. We reject the possibilities that this conflict arises from either gene duplication and loss or relaxed selection in nonecholocating fruit bats. Instead, we hypothesize that the putative gene tree reflects convergence at stretches of functional importance. Convergence is supported by the recovery of the species tree from alignments of hydrophobic transmembrane domains, and the putative gene tree from the intra- and extracellular domains. We also found evidence that Prestin has undergone Darwinian selection associated with the evolution of specialized constant-frequency echolocation, which is characterized by sharp auditory tuning. Our study of a hearing gene in bats strongly implicates Prestin in the evolution of echolocation, and suggests independent evolution of high-frequency hearing in bats. These results highlight the potential problems of extracting phylogenetic signals from functional genes that may be prone to convergence.
• evolution
• phylogenetics
• convergence
• cochlea
• mammals
Echolocation has evolved in relatively few animal species. One constraint may be the high cost of producing pulses, the echoes of which can be detected over useful distances. The energy cost of echolocation in a small (6 g) insectivorous bat, when hanging at rest, was recently measured at 0.067 Joules per pulse, implying a mean cost for echolocation in flight of 9.5 x basal metabolic rate (range 7 to 12x). Because flight is very costly, whether the costs of echolocation and flying are additive is an important question. We measured the energy costs of flight in two species of small echolocating Microchiroptera using a novel combination of respirometry and doubly-labelled water. Flight energy expenditure (adjusted for body mass) was not significantly different between echolocating bats and non-echolocating bats and birds. The low cost of echolocation for flying vertebrates may have been a significant factor favouring its evolution in these groups.
Echolocation call intensity was measured in the laboratory for five species of British insectivorous bats in free flight and in the hand. All species showed similar call intensities of between 80 and 90 dB peSPL (peak equivalent SPL) at 1 m during flight except Plecotus auritus, whose call intensity was between 68 and 77 dB peSPL at 1 m. Calls from stationary bats were about 13 dB less intense than calls during flight. A method is proposed to measure the root mean square (rms) amplitude of echolocation calls and, hence, to calculate the energy flux density of the call.
The constant−frequency calls of Rhinolophus hipposideros have energy flux densities approximately ten times higher than those of bats using frequency−modulated calls as a result of their longer durations and lower crest factors. It is argued that the low−intensity calls of P. auritus allow it to approach tympanate moths more closely before triggering their escape response.
Theoretical considerations of eye design allow us to find routes along which the optical structures of eyes may have evolved. If selection constantly favours an increase in the amount of detectable spatial information, a light-sensitive patch will gradually turn into a focused lens eye through continuous small improvements of design. An upper limit for the number of generations required for the complete transformation can be calculated with a minimum of assumptions. Even with a consistently pessimistic approach the time required becomes amazingly short: only a few hundred thousand years.
Molecular phylogenies challenge the view that bats belong to the superordinal group Archonta, which also includes primates, tree shrews, and flying lemurs. Some molecular studies also challenge microbat monophyly and instead support an alliance between megabats and representative rhinolophoid microbats from the families Rhinolophidae (horseshoe bats, Old World leaf-nosed bats) and Megadermatidae (false vampire bats). Another molecular study ostensibly contradicts these results and supports traditional microbat monophyly, inclusive of representative rhinolophoids from the family Nycteridae (slit-faced bats). Resolution of the microbat paraphyly/monophyly issue is essential for reconstructing the temporal sequence and deployment of morphological character state changes associated with flight and echolocation in bats. If microbats are paraphyletic, then laryngeal echolocation either evolved more than once in different microbats or was lost in megabats after evolving in the ancestor of all living bats. To examine these issues, we used a 7.1-kb nuclear data set for nine outgroups and twenty bats, including representatives of all rhinolophoid families. Phylogenetic analyses and statistical tests rejected both Archonta and microbat monophyly. Instead, bats are in the superorder Laurasiatheria and microbats are paraphyletic. Further, the superfamily Rhinolophoidea is polyphyletic. The rhinolophoid families Rhinolophidae and Megadermatidae belong to the suborder Yinpterochiroptera along with rhinopomatids and megabats. The rhinolophoid family Nycteridae belongs to the suborder Yangochiroptera along with vespertilionoids, noctilionoids, and emballonuroids. These results resolve the apparent conflict between previous molecular studies that sampled different rhinolophoid families. An important implication of rhinolophoid polyphyly is independent evolution of key anatomical innovations associated with the nasal-emission of echolocation pulses.
Rousettus aegyptiacus Geoffroy 1810 is a member of the only genus of Megachiropteran bats to use vocal echolocation, but the structure of its brief, click-like signal is poorly described. Although thought to have a simple echolocation system compared to that of Microchiroptera, R. aegyptiacus is capable of good obstacle avoidance using its impulse sonar. The energy content of the signal was at least an order of magnitude smaller than in Microchiropteran bats and dolphins (approximately 4 x 10(-8) J m(-2)). Measurement of the duration, amplitude and peak frequency demonstrate that the signals of this animal are broadly similar in structure and duration to those of dolphins. Gabor functions were used to model signals and to estimate signal parameters, and the quality of the Gabor function fit to the early part of the signal demonstrates that the echolocation signals of R. aegyptiacus match the minimum spectral spread for their duration and amplitude and are thus well matched to its best hearing sensitivity. However, the low energy content of the signals and short duration should make returning echoes difficult to detect. The performance of R. aegyptiacus in obstacle avoidance experiments using echolocation therefore remains something of a conundrum.
Bats make up more than 20% of extant mammals, yet their evolutionary history is largely unknown because of a limited fossil record and conflicting or incomplete phylogenies. Here, we present a highly resolved molecular phylogeny for all extant bat families. Our results support the hypothesis that megabats are nested among four major microbat lineages, which originated in the early Eocene [52 to 50 million years ago (Mya)], coincident with a significant global rise in temperature, increase in plant diversity and abundance, and the zenith of Tertiary insect diversity. Our data suggest that bats originated in Laurasia, possibly in North America, and that three of the major microbat lineages are Laurasian in origin, whereas the fourth is Gondwanan. Combining principles of ghost lineage analysis with molecular divergence dates, we estimate that the bat fossil record underestimates (unrepresented basal branch length, UBBL) first occurrences by, on average, 73% and that the sum of missing fossil history is 61%.
Bats (Order Chiroptera), the only mammals capable of powered flight and sophisticated laryngeal echolocation, represent one of the most species-rich and ubiquitous orders of mammals. However, phylogenetic relationships within this group are poorly resolved. A robust evolutionary tree of Chiroptera is essential for evaluating the phylogeny of echolocation within Chiroptera, as well as for understanding their biogeographical history. We generated 4 kb of sequence data from portions of four novel nuclear intron markers for multiple representatives of 17 of the 18 recognized extant bat families, as well as the putative bat family Miniopteridae. Three echolocation-call characters were examined by mapping them onto the combined topology: (1) high-duty cycle versus low-duty cycle, (2) high-intensity versus low-intensity call emission, and (3) oral versus nasal emission. Echolocation seems to be highly convergent, and the mapping of echolocation-call design onto our phylogeny does not appear to resolve the question of whether echolocation had a single or two origins. Fossil taxa may also provide insight into the evolution of bats; we therefore evaluate 195 morphological characters in light of our nuclear DNA phylogeny. All but 24 of the morphological characters were found to be homoplasious when mapped onto the supermatrix topology, while the remaining characters provided insufficient information to reconstruct the placement of the fossil bat taxa with respect to extant families. However, a morphological synapomorphy characterizing the Rhinolophoidea was identified and is suggestive of a separate origin of echolocation in this clade. Dispersal-Vicariance analysis together with a relaxed Bayesian clock were used to evaluate possible biogeographic scenarios that could account for the current distribution pattern of extant bat families. Africa was reconstructed as the center of origin of modern-day bat families.
Comparing the hearing abilities of echolocating and non-echolocating bats can provide insight into the effect of echolocation on more basic hearing abilities. Toward this end, we determined the audiograms of two species of non-echolocating bats, the straw-colored fruit bat (Eidolon helvum), a large (230-350 g) African fruit bat, and the dog-faced fruit bat (Cynopterus brachyotis), a small (30-45 g) bat native to India and Southeast Asia. A conditioned suppression/avoidance procedure with a fruit juice reward was used for testing. At 60 dB SPL, the hearing range of E. helvum extends from 1.38 to 41 kHz with best sensitivity at 8k Hz; the hearing range of C. brachyotis extends from 2.63 to 70 kHz with best sensitivity at 10 kHz. As with all other bats tested so far, neither species was able to hear below 500 Hz, suggesting that they may not use a time code for perceiving pitch. Comparison of the high-frequency hearing abilities of echolocating and non-echolocating bats suggests that the use of laryngeal echolocation has resulted in additional selective pressure to hear high frequencies. However, the typical high-frequency sensitivity of small non-echolocating mammals would have been sufficient to support initial echolocation in the early evolution of bats, a finding that supports the possibility of multiple origins of echolocation.
Insights into the onset of evolutionary novelties are key to the understanding of amniote origins and diversification. The possession of an impedance-matching tympanic middle ear is characteristic of all terrestrial vertebrates with a sophisticated hearing sense and an adaptively important feature of many modern terrestrial vertebrates. Whereas tympanic ears seem to have evolved multiple times within tetrapods, especially among crown-group members such as frogs, mammals, squamates, turtles, crocodiles, and birds, the presence of true tympanic ears has never been recorded in a Paleozoic amniote, suggesting they evolved fairly recently in amniote history.
In the present study, we performed a morphological examination and a phylogenetic analysis of poorly known parareptiles from the Middle Permian of the Mezen River Basin in Russia. We recovered a well-supported clade that is characterized by a unique cheek morphology indicative of a tympanum stretching across large parts of the temporal region to an extent not seen in other amniotes, fossil or extant, and a braincase specialized in showing modifications clearly related to an increase in auditory function, unlike the braincase of any other Paleozoic tetrapod. In addition, we estimated the ratio of the tympanum area relative to the stapedial footplate for the basalmost taxon of the clade, which, at 23:1, is in close correspondence to that of modern amniotes capable of efficient impedance-matching hearing.
Using modern amniotes as analogues, the possession of an impedance-matching middle ear in these parareptiles suggests unique ecological adaptations potentially related to living in dim-light environments. More importantly, our results demonstrate that already at an early stage of amniote diversification, and prior to the Permo-Triassic extinction event, the complexity of terrestrial vertebrate ecosystems had reached a level that proved advanced sensory perception to be of notable adaptive significance.
Bats (Chiroptera) represent one of the largest and most diverse radiations of mammals, accounting for one-fifth of extant species. Although recent studies unambiguously support bat monophyly and consensus is rapidly emerging about evolutionary relationships among extant lineages, the fossil record of bats extends over 50 million years, and early evolution of the group remains poorly understood. Here we describe a new bat from the Early Eocene Green River Formation of Wyoming, USA, with features that are more primitive than seen in any previously known bat. The evolutionary pathways that led to flapping flight and echolocation in bats have been in dispute, and until now fossils have been of limited use in documenting transitions involved in this marked change in lifestyle. Phylogenetically informed comparisons of the new taxon with other bats and non-flying mammals reveal that critical morphological and functional changes evolved incrementally. Forelimb anatomy indicates that the new bat was capable of powered flight like other Eocene bats, but ear morphology suggests that it lacked their echolocation abilities, supporting a 'flight first' hypothesis for chiropteran evolution. The shape of the wings suggests that an undulating gliding-fluttering flight style may be primitive for bats, and the presence of a long calcar indicates that a broad tail membrane evolved early in Chiroptera, probably functioning as an additional airfoil rather than as a prey-capture device. Limb proportions and retention of claws on all digits indicate that the new bat may have been an agile climber that employed quadrupedal locomotion and under-branch hanging behaviour.
Basic kinematic and detailed physical mechanisms of avian, non-vocal sound production are both unknown. Here, for the first time, field-generated high-speed video recordings and acoustic analyses are used to test numerous competing hypotheses of the kinematics underlying sonations, or non-vocal communicative sounds, produced by two genera of Pipridae, Manacus and Pipra (Aves). Eleven behaviorally and acoustically distinct sonations are characterized, five of which fall into a specific acoustic class of relatively loud, brief, broad-frequency sound pulses, or snaps. The hypothesis that one kinematic mechanism of snap production is used within and between birds in general, and manakins specifically, is rejected. Instead, it is verified that three of four competing hypotheses of the kinematic mechanisms used for producing snaps, namely: (1). above-the-back wing-against-wing claps, (2). wing-against-body claps and (3). wing-into-air flicks, are employed between these two clades, and a fourth mechanism, (4). wing-against-tail feather interactions, is discovered. The kinematic mechanisms used to produce snaps are invariable within each identified sonation, despite the fact that a diversity of kinematic mechanisms are used among sonations. The other six sonations described are produced by kinematic mechanisms distinct from those used to create snaps, but are difficult to distinguish from each other and from the kinematics of flight. These results provide the first detailed kinematic information on mechanisms of sonation in birds in general, and the Pipridae specifically. Further, these results provide the first evidence that acoustically similar avian sonations, such as brief, broad frequency snaps, can be produced by diverse kinematic means, both among and within species. The use of high-speed video recordings in the field in a comparative manner documents the diversity of kinematic mechanisms used to sonate, and uncovers a hidden, sexually selected radiation of behavioral and communicative diversity in the Pipridae.
The Eocene fossil record of bats (Chiroptera) includes four genera known from relatively complete skeletons: lcaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx. Phylogenetic relationships of these taxa to each other and to extant lineages of bats were investigated in a parsimony analysis of 195 morphological characters, 12 rDNA restriction site characters, and one character based on the number of R-1 tandem repeats in the mtDNA d-loop region. Results indicate that lcaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx represent a series of consecutive sister-taxa to extant microchiropteran bats. This conclusion stands in contrast to previous suggestions that these fossil forms represent either a primitive grade ancestral to both Megachiroptera and Microchiroptera (e.g., Eochiroptera) or a separate clade within Microchiroptera (e.g., Palaeochiropterygoidea). A new higher-level classification is proposed to better reflect hypothesized relationships among Eocene fossil bats and extant taxa. Critical features of this classification include restriction of Microchiroptera to the smallest clade that includes all extant bats that use sophisticated echolocation (Emballonuridae + Yinochiroptera + Yangochiroptera), and formal recognition of two more inclusive clades that encompass Microchiroptera plus the four fossil genera. Comparisons of results of separate phylogenetic analyses including and subsequently excluding the fossil taxa indicate that inclusion of the fossils changes the results in two ways: (1) altering perceived relationships among extant forms at a few poorly supported nodes; and (2) reducing perceived support for some nodes near the base of the tree. Inclusion of the fossils affects some character polarities (hence slightly changing tree topology), and also changes the levels at which transformations appear to apply (hence altering perceived support for some clades). Results of an additional phylogenetic analysis in which soft-tissue and molecular characters were excluded from consideration indicate that these characters are critical for determination of relationships among extant lineages. Our phytogeny provides a basis for evaluating previous hypotheses on the evolution of flight, echolocation, and foraging strategies. We propose that flight evolved before echolocation, and that the first bats used vision for orientation in their arboreal/aerial environment. The evolution of flight was followed by the origin of low-duty-cycle laryngeal echolocation in early members of the microchiropteran lineage. This system was most likely simple at first, permitting orientation and obstacle detection but not detection or tracking of airborne prey. Owing to the mechanical coupling of ventilation and flight, the energy costs of echolocation to flying bats were relatively low. In contrast, the benefits of aerial insectivory were substantial, and a more sophisticated low-duty-cycle echolocation system capable of detecting, tracking, and assessing airborne prey subsequently evolved rapidly. The need for an increasingly derived auditory system, together with limits on body size imposed by the mechanics of flight, echolocation, and prey capture, may have resulted in reduction and simplification of the visual system as echolocation became increasingly important. Our analysis confirms previous suggestions that Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx used echolocation. Foraging strategies of these forms were reconstructed based on postcranial osteology and wing form, cochlear size, and stomach contents. In the context of our phylogeny, we suggest that foraging behavior in the microchiropteran lineage evolved in a series of steps: (1) gleaning food objects during short flights from a perch using vision for orientation and obstacle detection; prey detection by passive means, including vision and/or listening for prey-generated sounds (no known examples in fossil record); (2) gleaning stationary prey from a perch using echolocation and vision for orientation and obstacle detection; prey detection by passive means (Icaronycteris, Archaeonycteris); (3) perch hunting for both stationary and flying prey using echolocation and vision for orientation and obstacle detection; prey detection and tracking using echolocation for flying prey and passive means for stationary prey (no known example, although Icaronycteris and/or Archaeonycteris may have done this at times); (4) combined perch hunting and continuous aerial hawking using echolocation and vision for orientation and obstacle detection; prey detection and tracking using echolocation for flying prey and passive means for stationary prey; calcar-supported uropatagium used for prey capture (common ancestor of Hassianycteris and Palaeochiropteryx; retained in Palaeochiropteryx); (5) exclusive reliance on continuous aerial hawking using echolocation and vision for orientation and obstacle detection; prey detection and tracking using echolocation (Hassianycteris; common ancestor of Microchiroptera). The transition to using echolocation to detect and track prey would have been difficult in cluttered envionments owing to interference produced by multiple returning echoes. We therefore propose that this transition occurred in bats that foraged in forest gaps and along the edges of lakes and rivers in situations where potential perch sites were adjacent to relatively clutter-free open spaces. Aerial hawking using echolocation to detect, track, and evalute prey was apparently the primitive foraging strategy for Microchiroptera. This implies that gleaning, passive prey detection, and perch hunting among extant microchiropterans are secondarily derived specializations rather than retentions of primitive habits. Each of these habits has apparently evolved multiple times. The evolution of continuous aerial hawking may have been the "key innovation" responsible for the burst of diversification in microchiropteran bats that occurred during the Eocene. Fossils referable to six major extant lineages are known from Middle-Late Eocene deposits, and reconstruction of ghost lineages leads to the conclusion that at least seven more extant lineages were minimally present by the end of the Eocene.
Molecular phylogenetics has rapidly established the evolutionary positions of most major mammal groups [1, 2], yet analyses have repeatedly failed to agree on that of bats (order Chiroptera) [3-6]. Moreover, the relationship among the major bat lineages has proven equally contentious, with ongoing disagreements about whether echolocating bats are paraphyletic [7-9] or a true group [10] having profound implications for whether echolocation evolved once or possibly multiple times. By generating new bat genome data and applying model-based phylogenomic analyses designed to accommodate heterogeneous evolutionary processes [4, 11], we show that-contrary to recent suggestions-bats are not closely related to odd-toed ungulates but instead have a more ancient origin as sister group to a large clade of carnivores, ungulates, and cetaceans. Additionally, we provide the first genome-scale support showing that laryngeal echolocating bats are not a true group and that this paraphyly is robust to their position within mammals. We suggest that earlier disagreements in the literature may reflect model misspecification, long-branch artifacts, poor taxonomic coverage, and differences in the phylogenetic markers used. These findings are a timely reminder of the relevance of experimental design and careful statistical analysis as we move into the phylogenomic era.
Computational brain maps as opposed to maps of receptor
surfaces strongly reflect functional neuronal design principles.
In echolocating bats, computational maps are established that
topographically represent the distance of objects. These target
range maps are derived from the temporal delay between
emitted call and returning echo and constitute a regular
representation of time (chronotopy). Basic features of these
maps are innate, and in different bat species the map size and
precision varies. An inherent advantage of target range maps is
the implementation of mechanisms for lateral inhibition and
excitatory feedback. Both can help to focus target ranging
depending on the actual echolocation situation. However,
these maps are not absolutely necessary for bat echolocation
since there are bat species without cortical target-distance
maps, which use alternative ensemble computation
mechanisms.
1. The distance at which bats (Myotis lucifugus) react to the presence of a row of small wires has been measured by a photographic determination of the distance at which the pulse repetition rate first increases as the bats fly towards the wires. Distinct changes in this rate were measured in almost every flight towards wires spaced 30 cm. apart and ranging in diameter from 0.18 to 3 mm.2. The interval between successive pulses averaged 60 to 80 msec as the bats flew along the room towards the row of wires, and dropped to 20-40 msec just before the barrier. The intervals decreased less with the smaller sizes of wire.3. All but the largest of these wires are well below one wave-length of the emitted sounds of these bats (50-60 kc, or 6-7 mm., at the peak intensity and 120 kc, or about 3 mm., at the very beginning of some pulses).4. Clear evidence that the wires had been detected was furnished at the point where the interval between pulses first dropped significantly below the level that prevailed before an...
Six R h i n o l o p h u s f e r r u m e q u i n u m were trained to fly through an array of vertical or horizontal wires. Obstacle avoidance performance was measured as the percentage of flights in which the bats did not touch the wires (successful flights). Bats with normal mobile pinnae scored between 70% and 90% successful flights both with vertical and horizontal wires. After surgically immobilizing the pinnae by cutting motor nerves and ear muscles, avoidance performance with vertical wires (horizontal target localization) was unchanged but the percentage of successful flights with horizontal wires (vertical target localization) decreased significantly. This demonstrates the importance of pinna movements for target localization in the vertical plane and supports the hypothesis that scanning movements with pinnae are used by R h i n o l o p h u s f e r r u m e q u i n u m for determination of target angle.