Evolution of inner ear neuroanatomy of bats and implications for echolocation.

Phylogenomics of bats suggests that their echolocation either evolved separately in the bat suborders Yinpterochiroptera and Yangochiroptera, or had a single origin in bat ancestors and was later lost in some yinpterochiropterans1-6. Hearing for echolocation behaviour depends on the inner ear, of which the spiral ganglion is an essential structure. Here we report the observation of highly derived structures of the spiral ganglion in yangochiropteran bats: a trans-otic ganglion with a wall-less Rosenthal's canal. This neuroanatomical arrangement permits a larger ganglion with more neurons, higher innervation density of neurons and denser clustering of cochlear nerve fascicles7-13. This differs from the plesiomorphic neuroanatomy of Yinpterochiroptera and non-chiropteran mammals. The osteological correlates of these derived ganglion features can now be traced into bat phylogeny, providing direct evidence of how Yangochiroptera differentiated from Yinpterochiroptera in spiral ganglion neuroanatomy. These features are highly variable across major clades and between species of Yangochiroptera, and in morphospace, exhibit much greater disparity in Yangochiroptera than Yinpterochiroptera. These highly variable ganglion features may be a neuroanatomical evolutionary driver for their diverse echolocating strategies4,14-17 and are associated with the explosive diversification of yangochiropterans, which include most bat families, genera and species.

Physical constraints on thermoregulation and flight drive morphological evolution in bats.

Body size and shape fundamentally determine organismal energy requirements by modulating heat and mass exchange with the environment and the costs of locomotion, thermoregulation, and maintenance. Ecologists have long used the physical linkage between morphology and energy balance to explain why the body size and shape of many organisms vary across climatic gradients, e.g., why larger endotherms are more common in colder regions. However, few modeling exercises have aimed at investigating this link from first principles. Body size evolution in bats contrasts with the patterns observed in other endotherms, probably because physical constraints on flight limit morphological adaptations. Here, we develop a biophysical model based on heat transfer and aerodynamic principles to investigate energy constraints on morphological evolution in bats. Our biophysical model predicts that the energy costs of thermoregulation and flight, respectively, impose upper and lower limits on the relationship of wing surface area to body mass (S-MR), giving rise to an optimal S-MR at which both energy costs are minimized. A comparative analysis of 278 species of bats supports the model's prediction that S-MR evolves toward an optimal shape and that the strength of selection is higher among species experiencing greater energy demands for thermoregulation in cold climates. Our study suggests that energy costs modulate the mode of morphological evolution in bats­hence shedding light on a long-standing debate over bats' conformity to ecogeographical patterns observed in other mammals­and offers a procedure for investigating complex macroecological patterns from first principles.

Plecotus macrobullaris sarmaticus subsp. nov. (Vespertilionidae, Chiroptera) from the Early Pleistocene of Crimea.

The extinct mountain long-eared bat Plecotus macrobullaris sarmaticus subsp. nov. is described on the base of jaw remains from the Lower Pleistocene of the Taurida cave in central Crimea. This is the first record of the genus Plecotus in the Lower Pleistocene of Russia and the first fossil find of P. macrobullaris Kuzyakin, 1965, documenting the early stage of the evolutionary history of the species.

New gliding mammaliaforms from the Jurassic.

Stem mammaliaforms are Mesozoic forerunners to mammals, and they offer critical evidence for the anatomical evolution and ecological diversification during the earliest mammalian history. Two new eleutherodonts from the Late Jurassic period have skin membranes and skeletal features that are adapted for gliding. Characteristics of their digits provide evidence of roosting behaviour, as in dermopterans and bats, and their feet have a calcaneal calcar to support the uropagatium as in bats. The new volant taxa are phylogenetically nested with arboreal eleutherodonts. Together, they show an evolutionary experimentation similar to the iterative evolutions of gliders within arboreal groups of marsupial and placental mammals. However, gliding eleutherodonts possess rigid interclavicle-clavicle structures, convergent to the avian furculum, and they retain shoulder girdle plesiomorphies of mammaliaforms and monotremes. Forelimb mobility required by gliding occurs at the acromion-clavicle and glenohumeral joints, is different from and convergent to the shoulder mobility at the pivotal clavicle-sternal joint in marsupial and placental gliders.

Facial muscle modification associated with chiropteran noseleaf development: Insights into the developmental basis of a movable rostral appendage in mammals.

BACKGROUND: Mammal evolution has generated diverse craniofacial morphologies, including remarkable movable rostral appendages. However, the muscular and skeletal architecture providing the mobility of these appendages remains largely unexplored. Here, we focus on chiropteran noseleaves and compare the three-dimensional internal morphology of late-stage embryos between the greater horseshoe bat Rhinolophus ferrumequinum, which possesses a noseleaf, and the Asian bent-winged bat Miniopterus fuliginosus and Egyptian fruit bat Rousettus aegyptiacus, which do not. We also assess earlier stage cell proliferation within the rostrum to elucidate cellular mechanisms underlying noseleaf-associated morphological modifications. RESULTS: The musculus maxillolabialis inserted into proximal vibrissae follicles in M fuliginosus and R aegyptiacus embryos but instead inserted into the horseshoe plate in R ferrumequinum. This modification suggests that the M maxillolabialis has adapted to controlling the noseleaf rather than vibrissae in rhinolophid bats. Our cellular analysis showed higher cell proliferation within the maxillary and frontonasal processes of St. 14 embryos in R ferrumequinum compared to M fuliginosus and R aegyptiacus, suggesting that the spatial alteration of noseleaf-associated muscle is derived from changes in facial morphogenesis that occur by St. 14. CONCLUSION: This is the first study clarifying the morphological and cellular bases underlying the development of mammalian rostral appendages.

On the sequence heterochrony of cranial ossification of bats in light of Haeckel's recapitulation theory.

Haeckel's recapitulation theory has been a controversial topic in evolutionary biology. However, we have seen some recent cases applying Haeckel's view to interpret the interspecific variation of prenatal ontogeny. To revisit the validity of Haeckel's recapitulation theory, we take bats that have undergone drastic morphological changes and possess a characteristic ecology as a case study. All members of Rhinolophoidea and Yangochiroptera can generate an ultrasonic pulse from the larynx to interpret surrounding objects (laryngeal echolocation) whereas Pteropodidae lacks such ability. It is known that the petrosal bone is particularly derived in shape and expanded in laryngeal echolocators. If Haeckel's recapitulation theory holds, the formation of this derived trait should occur later than those of other bones. Therefore, we compared the prenatal ossification timing of the petrosal in 15 bat species and five outgroup species. We found that the ossification of the petrosal is accelerated in laryngeal echolocators while it is the last bone to ossify in non-laryngeal echolocating bats and non-volant mammals, which runs counter to the prediction generated by Haeckel's recapitulation theory. We point out the evolutionarily labile nature of trait developmental timing and emphasize that Haeckel's recapitulation theory does not hold in many cases. We caution that generating predictions on ancestral conditions and evolutionary history leading from Haeckel's recapitulation theory is not well supported.

The hyoid as a sound conducting apparatus in laryngeally echolocating bats.

The morphology of the stylohyal-tympanic bone articulation found in laryngeally echolocating bats is highly indicative of a function associated with signal production. One untested hypothesis is that this morphology allows the transfer of a sound signal from the larynx to the tympanic bones (auditory bulla) via the hyoid apparatus during signal production by the larynx. We used µCT data and finite element analysis to model the propagation of sound through the hyoid chain into the tympanic bones to test this hypothesis. We modeled sound pressure (dB) wave propagation from the basihyal to the tympanic bones, vibratory behavior (m) of the stylohyal-tympanic bone unit, and the stylohyal and tympanic bones when the stylohyal bone is allowed to pivot on the tympanic bone. Sound pressure wave propagation was modeled using the harmonic acoustics solver in ANSYS and vibratory behavior was modeled using coupled modal and harmonic response analyses in ANSYS. For both analyses (harmonic acoustics and harmonic response), the input excitation on the basihyal and thyrohyals was modeled as the estimated pressure (Pa) imposed by the collision of the vibrating thyroid cartilage of the larynx against these bones during signal production. Our models support the hypothesis that this stereotypical hyoid morphology found in laryngeally echolocating bats can transfer sound to the auditory bullae at an amplitude that is likely heard for the species Artibeus jamaicensis and Rhinolophus pusillus.

Phylogeny and foraging behaviour shape modular morphological variation in bat humeri.

Bats show a remarkable ecological diversity that is reflected both in dietary and foraging guilds (FGs). Cranial ecomorphological adaptations linked to diet have been widely studied in bats, using a variety of anatomical, computational and mathematical approaches. However, foraging-related ecomorphological adaptations and the concordance between cranial and postcranial morphological adaptations remain unexamined in bats and limited to the interpretation of traditional aerodynamic properties of the wing (e.g. wing loading [WL] and aspect ratio [AR]). For this reason, the postcranial ecomorphological diversity in bats and its drivers remain understudied. Using 3D virtual modelling and geometric morphometrics (GMM), we explored the phylogenetic, ecological and biological drivers of humeral morphology in bats, evaluating the presence and magnitude of modularity and integration. To explore decoupled patterns of variation across the bone, we analysed whole-bone shape, diaphyseal and epiphyseal shape. We also tested whether traditional aerodynamic wing traits correlate with humeral shape. By studying 37 species from 20 families (covering all FGs and 85% of dietary guilds), we found similar patterns of variation in whole-bone and diaphyseal shape and unique variation patterns in epiphyseal shape. Phylogeny, diet and FG significantly correlated with shape variation at all levels, whereas size only had a significant effect on epiphyseal morphology. We found a significant phylogenetic signal in all levels of humeral shape. Epiphyseal shape significantly correlated with wing AR. Statistical support for a diaphyseal-epiphyseal modular partition of the humerus suggests a functional partition of shape variability. Our study is the first to show within-structure modular morphological variation in the appendicular skeleton of any living tetrapod. Our results suggest that diaphyseal shape correlates more with phylogeny, whereas epiphyseal shape correlates with diet and FG.

Reliable Phylogenetic Regressions for Multivariate Comparative Data: Illustration with the MANOVA and Application to the Effect of Diet on Mandible Morphology in Phyllostomid Bats.

Understanding what shapes species phenotypes over macroevolutionary timescales from comparative data often requires studying the relationship between phenotypes and putative explanatory factors or testing for differences in phenotypes across species groups. In phyllostomid bats for example, is mandible morphology associated to diet preferences? Performing such analyses depends upon reliable phylogenetic regression techniques and associated tests (e.g., phylogenetic Generalized Least Squares, pGLS, and phylogenetic analyses of variance and covariance, pANOVA, pANCOVA). While these tools are well established for univariate data, their multivariate counterparts are lagging behind. This is particularly true for high-dimensional phenotypic data, such as morphometric data. Here, we implement much-needed likelihood-based multivariate pGLS, pMANOVA, and pMANCOVA, and use a recently developed penalized-likelihood framework to extend their application to the difficult case when the number of traits $p$ approaches or exceeds the number of species $n$. We then focus on the pMANOVA and use intensive simulations to assess the performance of the approach as $p$ increases, under various levels of phylogenetic signal and correlations between the traits, phylogenetic structure in the predictors, and under various types of phenotypic differences across species groups. We show that our approach outperforms available alternatives under all circumstances, with greater power to detect phenotypic differences across species group when they exist, and a lower risk of improperly detecting nonexistent differences. Finally, we provide an empirical illustration of our pMANOVA on a geometric-morphometric data set describing mandible morphology in phyllostomid bats along with data on their diet preferences. Overall our results show significant differences between ecological groups. Our approach, implemented in the R package mvMORPH and illustrated in a tutorial for end-users, provides efficient multivariate phylogenetic regression tools for understanding what shapes phenotypic differences across species. [Generalized least squares; high-dimensional data sets; multivariate phylogenetic comparative methods; penalized likelihood; phenomics; phyllostomid bats; phylogenetic MANOVA; phylogenetic regression.].

Neural timing of stimulus events with microsecond precision.

Temporal analysis of sound is fundamental to auditory processing throughout the animal kingdom. Echolocating bats are powerful models for investigating the underlying mechanisms of auditory temporal processing, as they show microsecond precision in discriminating the timing of acoustic events. However, the neural basis for microsecond auditory discrimination in bats has eluded researchers for decades. Combining extracellular recordings in the midbrain inferior colliculus (IC) and mathematical modeling, we show that microsecond precision in registering stimulus events emerges from synchronous neural firing, revealed through low-latency variability of stimulus-evoked extracellular field potentials (EFPs, 200-600 Hz). The temporal precision of the EFP increases with the number of neurons firing in synchrony. Moreover, there is a functional relationship between the temporal precision of the EFP and the spectrotemporal features of the echolocation calls. In addition, EFP can measure the time difference of simulated echolocation call-echo pairs with microsecond precision. We propose that synchronous firing of populations of neurons operates in diverse species to support temporal analysis for auditory localization and complex sound processing.

Three-dimensional head-direction coding in the bat brain.

Navigation requires a sense of direction ('compass'), which in mammals is thought to be provided by head-direction cells, neurons that discharge when the animal's head points to a specific azimuth. However, it remains unclear whether a three-dimensional (3D) compass exists in the brain. Here we conducted neural recordings in bats, mammals well-adapted to 3D spatial behaviours, and found head-direction cells tuned to azimuth, pitch or roll, or to conjunctive combinations of 3D angles, in both crawling and flying bats. Head-direction cells were organized along a functional-anatomical gradient in the presubiculum, transitioning from 2D to 3D representations. In inverted bats, the azimuth-tuning of neurons shifted by 180°, suggesting that 3D head direction is represented in azimuth × pitch toroidal coordinates. Consistent with our toroidal model, pitch-cell tuning was unimodal, circular, and continuous within the available 360° of pitch. Taken together, these results demonstrate a 3D head-direction mechanism in mammals, which could support navigation in 3D space.

Lipid composition of the stratum corneum in different regions of the body of Kuhl's pipistrelle from the Negev Desert, Israel.

The most superficial epidermal layer in endotherms is the stratum corneum (SC), which is composed of dead corneocytes embedded in a lipid matrix with free fatty acids, cholesterol, ceramides, and cerebrosides; the lipid composition of the SC determines its permeability to water vapor. Lipids that are more polar, have longer hydrocarbon chains, and are less bulky are often packed in more ordered phase states to slow cutaneous evaporative water loss (CEWL); these lipids also resist transitions to more disordered phases at high ambient temperatures (Ta). In bats, wing and tail membranes (wing patagia and tail uropatagium, respectively) allow powered flight, but increase surface area, and hence CEWL, with implications for survival in arid environments. We captured Pipistrellus kuhlii from an arid habitat and measured the lipid composition of the SC of the plagiopatagium in the wing, the uropatagium, and the non-membranous region (NMR) of the body using thin layer chromatography and reversed phase high performance liquid chromatography coupled with atmospheric pressure photoionization mass spectrometry. The patagia contained more cholesterol and shorter-chained ceramides, and fewer cerebrosides than the NMR, indicating that the lipid phase transition temperature in the patagia is lower than in the NMR. Thus, at moderate Ta the lipids in the SC in all body regions will remain in an ordered phase state, allowing water conservation; but as Ta increases, the lipids in the SC of the patagia will more easily transition into a disordered phase, resulting in increased CEWL from the patagia facilitating efficient heat dissipation in hot environments.

Pleistocene Mammals from the Lang Trang Cave (Vietnam): New Data.

The following mammal assemblage was identified among the materials collected in 2020 from the Pleistocene of the Lang Trang cave (northern Vietnam): the primates Pongo sp., Trachypithecus sp., Macaca cf. nemestrina (Linnaeus, 1766), and Macaca sp.; the carnivorans Arctonyx collaris rostratus Matthew et Granger, 1923 and Panthera sp.; the chiropteran Ia io Thomas, 1902; the rodent Hystrix kiangsenensis Wang, 1931; the proboscidean Elephas sp.; the perissodactyls Tapirus indicus (Desmarest, 1819) and Dicerorhinus sumatrensis (Fischer, 1814); the artiodactyls Sus scrofa Linnaeus, 1758, S. barbatus Müller, 1838, Tragulus kanchil (Raffles, 1821), Hydropotes inermis Swinhoe, 1870, Muntiacus muntjak (Zimmermann, 1780), Axis porcinus (Zimmermann, 1780), Rusa unicolor (Kerr, 1792), and Capricornis sumatraensis (Bechstein, 1799). I. io, S. barbatus, T. kanchil, H. inermis, and A. porcinus were detected in the Lang Trang fauna for the first time. The mammal assemblage is dominated by inhabitants of tropical forests (from lowlands to mountains), subtropical forms are also present.

Reinforcement of the larynx and trachea in echolocating and non-echolocating bats.

The synchronization of flight mechanics with respiration and echolocation call emission by bats, while economizing these behaviors, presumably puts compressive loads on the cartilaginous rings that hold open the respiratory tract. Previous work has shown that during postnatal development of Artibeus jamaicensis (Phyllostomidae), the onset of adult echolocation call emission rate coincides with calcification of the larynx, and the development of flight coincides with tracheal ring calcification. In the present study, I assessed the level of reinforcement of the respiratory system in 13 bat species representing six families that use stereotypical modes of echolocation (i.e. duty cycle % and intensity). Using computed tomography, the degree of mineralization or ossification of the tracheal rings, cricoid, thyroid and arytenoid cartilages were determined for non-echolocators, tongue clicking, low-duty cycle low-intensity, low-duty cycle high-intensity, and high-duty cycle high-intensity echolocating bats. While all bats had evidence of cervical tracheal ring mineralization, about half the species had evidence of thoracic tracheal ring calcification. Larger bats (Phyllostomus hastatus and Pterpodidae sp.) exhibited more extensive tracheal ring mineralization, suggesting an underlying cause independent of laryngeal echolocation. Within most of the laryngeally echolocating species, the degree of mineralization or ossification of the larynx was dependent on the mode of echolocation system used. Low-duty cycle low-intensity bats had extensively mineralized cricoids, and zero to very minor mineralization of the thyroids and arytenoids. Low-duty cycle high-intensity bats had extensively mineralized cricoids, and patches of thyroid and arytenoid mineralization. The high-duty cycle high-intensity rhinolophids and hipposiderid had extensively ossified cricoids, large patches of ossification on the thyroids, and heavily ossified arytenoids. The high-duty cycle high-intensity echolocator, Pteronotus parnellii, had mineralization patterns and laryngeal morphology very similar to the other low-duty cycle high-intensity mormoopid species, perhaps suggesting relatively recent evolution of high-duty cycle echolocation in P. parnellii compared with the Old World high-duty cycle echolocators (Rhinolophidae and Hipposideridae). All laryngeal echolocators exhibited mineralized or ossified lateral expansions of the cricoid for articulation with the inferior horn of the thyroid, these were most prominent in the high-duty cycle high-intensity rhinolophids and hipposiderid, and least prominent in the low-duty cycle low-intensity echolocators. The non-laryngeal echolocators had extensively ossified cricoid and thyroid cartilages, and no evidence of mineralization/ossification of the arytenoids or lateral expansions of the cricoid. While the non-echolocators had extensive ossification of the larynx, it was inconsistent with that seen in the laryngeal echolocators.

Pliocene bats (Chiroptera) from Kanapoi, Turkana Basin, Kenya.

Fossil bats from the Pliocene of Africa are extremely rare, especially in East Africa where meager records have been reported only from two localities in the Omo River Basin Shungura Formation and from a scattering of localities in the Afar Depression, both in Ethiopia. Here we report on a diverse assemblage of bats from Kanapoi in the Turkana Basin that date to approximately 4.19 million years ago. The Kanapoi bat community consists of four different species of fruit bats including a new genus and two new species as well as five species of echolocating bats, the most common of which are two new species of the molossid genus Mops. Additionally, among the echolocating bats, a new species of the emballonurid Saccolaimus is documented at Kanapoi along with an additional Saccolaimus species and a potentially new species of the nycterid Nycteris. Compared to other East African Pliocene bat assemblages, the Kanapoi bat community is unique in preserving molossids and curiously lacks any evidence of cave dwelling bats like rhinolophids or hipposiderids, which are both common at other East African sites. The bats making up the Kanapoi community all typically roost in trees, with some preferring deeper forests and larger trees (molossids), while the others (pteropodids, nycterids and emballonurids) roost in trees near open areas. Living fruit bats that are related to Kanapoi species typically forage for fruits along the margins of forests and in open savannah. The echolocating forms from Kanapoi consist of groups that aerially hawk for insects in open areas between patches of forest and along water courses. The habitats preferred by living relatives of the Kanapoi bats are in agreement with those constructed for Kanapoi based on other lines of evidence.

Tongue-driven sonar beam steering by a lingual-echolocating fruit bat.

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.

Mind the gap: natural cleft palates reduce biting performance in bats.

Novel morphological traits pose interesting evolutionary paradoxes when they become widespread in a lineage while being deleterious in others. Cleft palate is a rare congenital condition in mammals in which the incisor-bearing premaxilla bones of the upper jaw develop abnormally. However, ∼50% of bat species have natural, non-pathological cleft palates. We used the family Vespertilionidae as a model and linear and geometric morphometrics within a phylogenetic framework to (1) explore evolutionary patterns in cleft morphology, and (2) test whether cleft morphological variation is correlated with skull shape in bats. We also used finite element (FE) analyses to experimentally test how presence of a cleft palate impacts skull performance during biting in a species with extreme cleft morphology (hoary bat, Lasiurus cinereus). We constructed and compared the performance of two FE models: one based on the hoary bat's natural skull morphology, and another with a digitally filled cleft simulating a complete premaxilla. Results showed that cleft length and width are correlated with skull shape in Vespertilionidae, with narrower, shallower clefts seen in more gracile skulls and broader, deeper clefts in more robust skulls. FE analysis showed that the model with a natural cleft produced lower bite forces, and had higher stress and strain than the model with a filled cleft. In the rostrum, safety factors were 1.59-2.20 times higher in the model with a filled cleft than in the natural model. Our results demonstrate that cleft palates in bats reduce biting performance, and evolution of skull robusticity may compensate for this reduction in performance.

Dietary specializations and diversity in feeding ecology of the earliest stem mammals.

The origin and radiation of mammals are key events in the history of life, with fossils placing the origin at 220 million years ago, in the Late Triassic period. The earliest mammals, representing the first 50 million years of their evolution and including the most basal taxa, are widely considered to be generalized insectivores. This implies that the first phase of the mammalian radiation--associated with the appearance in the fossil record of important innovations such as heterodont dentition, diphyodonty and the dentary-squamosal jaw joint--was decoupled from ecomorphological diversification. Finds of exceptionally complete specimens of later Mesozoic mammals have revealed greater ecomorphological diversity than previously suspected, including adaptations for swimming, burrowing, digging and even gliding, but such well-preserved fossils of earlier mammals do not exist, and robust analysis of their ecomorphological diversity has previously been lacking. Here we present the results of an integrated analysis, using synchrotron X-ray tomography and analyses of biomechanics, finite element models and tooth microwear textures. We find significant differences in function and dietary ecology between two of the earliest mammaliaform taxa, Morganucodon and Kuehneotherium--taxa that are central to the debate on mammalian evolution. Morganucodon possessed comparatively more forceful and robust jaws and consumed 'harder' prey, comparable to extant small-bodied mammals that eat considerable amounts of coleopterans. Kuehneotherium ingested a diet comparable to extant mixed feeders and specialists on 'soft' prey such as lepidopterans. Our results reveal previously hidden trophic specialization at the base of the mammalian radiation; hence even the earliest mammaliaforms were beginning to diversify--morphologically, functionally and ecologically. In contrast to the prevailing view, this pattern suggests that lineage splitting during the earliest stages of mammalian evolution was associated with ecomorphological specialization and niche partitioning.

Retinal Ganglion Cell Topography and Spatial Resolving Power in Echolocating and Non-Echolocating Bats.

Bats are nocturnal mammals known for their ability to echolocate, yet all bats can see, and most bats of the family Pteropodidae (fruit bats) do not echolocate - instead they rely mainly on vision and olfaction to forage. We investigated whether echolocating bats, given their limited reliance on vision, have poorer spatial resolving power (SRP) than pteropodids and whether tongue click echolocating fruit bats differ from non-echolocating fruit bats in terms of visual performance. We compared the number and distribution of retinal ganglion cells (RGCs) as well as the maximum anatomical SRP derived from these distributions in 4 species of bats: Myotis daubentonii, a laryngeal echolocating bat from the family Vespertilionidae, Rousettus aegyptiacus, a tongue clicking echolocating bat from the family Pteropodidae, and Pteropus alecto and P. poliocephalus, 2 non-echolocating bats (also from the Pteropodidae). We find that all 3 pteropodids have a similar number (≈200,000 cells) and distribution of RGCs and a similar maximum SRP (≈4 cycles/degree). M. daubentonii has fewer (∼6,000 cells) and sparser RGCs than the pteropodids and thus a significantly lower SRP (0.6 cycles/degree). M. daubentonii also differs in terms of the distribution of RGCs by having a unique dorsal area of specialization in the retina. Our findings are consistent with the existing literature and suggest that M. daubentonii likely only uses vision for orientation, while for pteropodids vision is also important for foraging.