Phyllostomus Discolor Research Articles

Auditory cortical regions show resting-state functional connectivity with the default mode-like network in echolocating bats

Echolocating bats are among the most social and vocal of all mammals. These animals are ideal subjects for functional MRI (fMRI) studies of auditory social communication given their relatively hypertrophic limbic and auditory neural structures and their reduced ability to hear MRI gradient noise. Yet, no resting-state networks relevant to social cognition (e.g., default mode-like networks or DMLNs) have been identified in bats since there are few, if any, fMRI studies in the chiropteran order. Here, we acquired fMRI data at 7 Tesla from nine lightly anesthetized pale spear-nosed bats (Phyllostomus discolor). We applied independent components analysis (ICA) to reveal resting-state networks and measured neural activity elicited by noise ripples (on: 10 ms; off: 10 ms) that span this species' ultrasonic hearing range (20 to 130 kHz). Resting-state networks pervaded auditory, parietal, and occipital cortices, along with the hippocampus, cerebellum, basal ganglia, and auditory brainstem. Two midline networks formed an apparent DMLN. Additionally, we found four predominantly auditory/parietal cortical networks, of which two were left-lateralized and two right-lateralized. Regions within four auditory/parietal cortical networks are known to respond to social calls. Along with the auditory brainstem, regions within these four cortical networks responded to ultrasonic noise ripples. Iterative analyses revealed consistent, significant functional connectivity between the left, but not right, auditory/parietal cortical networks and DMLN nodes, especially the anterior-most cingulate cortex. Thus, a resting-state network implicated in social cognition displays more distributed functional connectivity across left, relative to right, hemispheric cortical substrates of audition and communication in this highly social and vocal species.

Landscape of IGH germline genes of Chiroptera and the pattern of Rhinolophus affinis bat IGH CDR3 repertoire.

The emergence and re-emergence of abundant viruses from bats that impact human and animal health have resulted in a resurgence of interest in bat immunology. Characterizing the immune receptor repertoire is critical to understanding how bats coexist with viruses in the absence of disease and developing new therapeutics to target viruses in humans and susceptible livestock. In this study, IGH germline genes of Chiroptera including Rhinolophus ferrumequinum, Phyllostomus discolor, and Pipistrellus pipistrellus were annotated, and we profiled the characteristics of Rhinolophus affinis (RA) IGH CDR3 repertoire. The germline genes of Chiroptera are quite different from those of human, mouse, cow, and dog in evolution, but the three bat species have high homology. The CDR3 repertoire of RA is unique in many aspects including CDR3 subclass, V/J genes access and pairing, CDR3 clones, and somatic high-frequency mutation compared with that of human and mouse, which is an important point in understanding the asymptomatic nature of viral infection in bats. This study unveiled a detailed map of bat IGH germline genes on chromosome level and provided the first immune receptor repertoire of bat, which will stimulate new avenues of research that are directly relevant to human health and disease.IMPORTANCEThe intricate relationship between bats and viruses has been a subject of study since the mid-20th century, with more than 100 viruses identified, including those affecting humans. While preliminary investigations have outlined the innate immune responses of bats, the role of adaptive immunity remains unclear. This study presents a pioneering contribution to bat immunology by unveiling, for the first time, a detailed map of bat IGH germline genes at the chromosome level. This breakthrough not only provides a foundation for B cell receptor research in bats but also contributes to primer design and sequencing of the CDR3 repertoire. Additionally, we offer the first comprehensive immune receptor repertoire of bats, serving as a crucial library for future comparative analyses. In summary, this research significantly advances the understanding of bats' immune responses, providing essential resources for further investigations into viral tolerance and potential zoonotic threats.

Expanded diversity of novel hemoplasmas in rare and undersampled Neotropical bats

Hemotropic mycoplasmas are emerging as a model system for studying bacterial pathogens in bats, but taxonomic coverage of sampled host species remains biased. We leveraged a long-term field study in Belize to uncover novel hemoplasma diversity in bats by analyzing 80 samples from 19 species, most of which are infrequently encountered. PCR targeting the partial 16S rRNA gene found 41% of bats positive for hemoplasmas. Phylogenetic analyses found two novel host shifts of hemoplasmas, four entirely new hemoplasma genotypes, and the first hemoplasma detections in four bat species. One of these novel hemoplasmas (from Neoeptesicus furinalis) shared 97.6% identity in the partial 16S rRNA gene to a human hemoplasma (Candidatus Mycoplasma haemohominis). Additional analysis of the partial 23S rRNA gene allowed us to also designate two novel hemoplasma species, in Myotis elegans and Phyllostomus discolor, with the proposed names Candidatus Mycoplasma haematomyotis sp. nov. and Candidatus Mycoplasma haematophyllostomi sp. nov., respectively. Our analyses show that additional hemoplasma diversity in bats can be uncovered by targeting rare or undersampled host species.

Genetic diversity of adenovirus in neotropical bats from Brazil.

Bats can harbor a diversity of viruses, such as adenovirus. Ten different species of bat adenoviruses (BtAdV A to J) have been previousdescribedworlwide. In Brazil, BtAdV was described in three species of phyllostomid species: Artibeus lituratus, Desmodus rotundus, and Sturnira lilium. There are around 180 bat species in Brazil, with 67% inhabiting the Atlantic Forest, with few information about the circulation of BtAdV in this biome. We aimed to describe the molecular detection and the phylogenetic characterization and suggest a classification of BtAdVs circulating in bats from the Brazilian Atlantic Forest. We collected 382 oral and rectal swabs from 208 bats between 2014-2015 and 2020-2021 fromSão Paulo, Pernambuco, and Santa Catarina Brazilian states. The adenovirus detection was done by a nested PCR targeting the DNA polymerase gene, and all positive samples were sequenced by the Sanger method. The phylogenetic analyses were based on the amino acid sequences using the MEGA 7 and BEAST software. We obtained 16 positive animals (detection rate 7.7%) belonging to seven bat species: Artibeus lituratus, Carollia perspicillata, Sturnira lilium, Molossus molossus, and the first record of Phyllostomus discolor, Eptesicus diminutus, and Myotis riparius. The phylogenetic analysis based on partial amino acid sequences showed that all obtained AdV sequences belong to the Mastadenovirus genus. We observed a high genetic diversity of BtAdV and identified eleven potential BtAdV species circulating in Brazil (BtAdV K to U). Our results contribute to the epidemiological surveillance of adenovirus, increasing the knowledge about the viral diversity and the distribution of AdV in bats from the Atlantic Forest.

New insights into the germline genes and CDR3 repertoire of the TCRβ chain in Chiroptera.

Bats are recognized as natural reservoirs for many viruses, and their unique immune system enables them to coexist with these viruses without frequently exhibiting disease symptoms. However, the current understanding of the bat adaptive immune system is limited due to the lack of a database or tool capable of processing T-cell receptor (TCR) sequences for bats. We performed germline gene annotation in three bat species using homologous genes and RSSs (Recombinational Signal Sequences) scanning method. Then we used the conserved C gene to construct the TCRβ chain receptor library of the Intermediate Horseshoe Bat. Bats' TCRβ data will be analyzed using MiXCR and constructed reference library. Regarding the annotation results, we found that the Pale Spear-nosed Bat has 37 members in the TRBV12 family, which is more than the total number of TRBV genes in the Greater Horseshoe Bat. The average number of unique TCRβ chain receptor sequences in each Intermediate Horseshoe Bat sample reached 24,904. The distinct variations in the distribution of TRBV genes among the three types of bats could have a direct impact on the diversity of the TCR repertoire, as evidenced by the presence of conserved amino acids that indicate the T-cell recognition of antigens in bats is MHC-restricted. The bats' TCRβ repertoire is formed through the rearrangement of the V-D-J-C genes, with D-J/V-D deletions and insertions resulting in high diversity.

Species-Specific Adaptation for Ongoing High-Frequency Action Potential Generation in MNTB Neurons.

Comparative analysis of evolutionarily conserved neuronal circuits between phylogenetically distant mammals highlights the relevant mechanisms and specific adaptations to information processing. The medial nucleus of the trapezoid body (MNTB) is a conserved mammalian auditory brainstem nucleus relevant for temporal processing. While MNTB neurons have been extensively investigated, a comparative analysis of phylogenetically distant mammals and the spike generation is missing. To understand the suprathreshold precision and firing rate, we examined the membrane, voltage-gated ion channel and synaptic properties in Phyllostomus discolor (bat) and in Meriones unguiculatus (rodent) of either sex. Between the two species, the membrane properties of MNTB neurons were similar at rest with only minor differences, while larger dendrotoxin (DTX)-sensitive potassium currents were found in gerbils. Calyx of Held-mediated EPSCs were smaller and frequency dependence of short-term plasticity (STP) less pronounced in bats. Simulating synaptic train stimulations in dynamic clamp revealed that MNTB neurons fired with decreasing success rate near conductance threshold and at increasing stimulation frequency. Driven by STP-dependent conductance decrease, the latency of evoked action potentials increased during train stimulations. The spike generator showed a temporal adaptation at the beginning of train stimulations that can be explained by sodium current inactivation. Compared with gerbils, the spike generator of bats sustained higher frequency input-output functions and upheld the same temporal precision. Our data mechanistically support that MNTB input-output functions in bats are suited to sustain precise high-frequency rates, while for gerbils, temporal precision appears more relevant and an adaptation to high output-rates can be spared.SIGNIFICANCE STATEMENT Neurons in the mammalian medial nucleus of the trapezoid body (MNTB) convey precise, faithful inhibition vital for binaural hearing and gap detection. The MNTB's structure and function appear evolutionarily well conserved. We compared the cellular physiology of MNTB neurons in bat and gerbil. Because of their adaptations to echolocation or low frequency hearing both species are model systems for hearing research, yet with largely overlapping hearing ranges. We find that bat neurons sustain information transfer with higher ongoing rates and precision based on synaptic and biophysical differences in comparison to gerbils. Thus, even in evolutionarily conserved circuits species-specific adaptations prevail, highlighting the importance for comparative research to differentiate general circuit functions and their specific adaptations.

Molecular evidence of Borrelia spp. in bats from Córdoba Department, northwest Colombia

BackgroundThe genus Borrelia is composed of two well-defined monophyletic groups, the Borrelia burgdorferi sensu lato complex (Bb) and the relapsing fever (RF) group borreliae. Recently, a third group, associated with reptiles and echidnas, has been described. In general, RF group borreliae use rodents as reservoir hosts; although neotropical bats may also be involved as important hosts, with scarce knowledge regarding this association. The objective of this study was to detect the presence of Borrelia spp. DNA in bats from the department of Córdoba in northwest Colombia.MethodsDuring September 2020 and June 2021, 205 bats were captured in six municipalities of Córdoba department, Colombia. Specimens were identified using taxonomic keys and DNA was extracted from spleen samples. A Borrelia-specific real-time PCR was performed for the 16S rRNA gene. Fragments of the 16S rRNA and flaB genes were amplified in the positive samples by conventional PCR. The detected amplicons were sequenced by the Sanger method. Phylogenetic reconstruction was performed in IQ-TREE with maximum likelihood based on the substitution model TPM3+F+I+G4 with bootstrap values deduced from 1000 replicates.ResultsOverall, 10.2% (21/205) of the samples were found positive by qPCR; of these, 81% (17/21) and 66.6% (14/21) amplified 16S rRNA and flaB genes, respectively. qPCR-positive samples were then subjected to conventional nested and semi-nested PCR to amplify 16S rRNA and flaB gene fragments. Nine positive samples for both genes were sequenced, and seven and six sequences were of good quality for the 16S rRNA and flaB genes, respectively. The DNA of Borrelia spp. was detected in the insectivorous and fruit bats Artibeus lituratus, Carollia perspicillata, Glossophaga soricina, Phyllostomus discolor, and Uroderma sp. The 16S rRNA gene sequences showed 97.66–98.47% identity with “Borrelia sp. clone Omi3,” “Borrelia sp. RT1S,” and Borrelia sp. 2374; the closest identities for the flaB gene were 94.02–98.04% with “Borrelia sp. Macaregua.” For the 16S rRNA gene, the phylogenetic analysis showed a grouping with “Candidatus Borrelia ivorensis” and “Ca. Borrelia africana,” and for the flaB gene showed a grouping with Borrelia sp. Macaregua and Borrelia sp. Potiretama. The pathogenic role of the Borrelia detected in this study is unknown.ConclusionsWe describe the first molecular evidence of Borrelia spp. in the department of Córdoba, Colombia, highlighting that several bat species harbor Borrelia spirochetes.Graphical

Morphological specialization to nectarivory in Phyllostomus discolor (Wagner, 1843) (Chiroptera: Phyllostomidae).

Dedicated nectarivory is a derived feeding habit that requires specialized cranial and soft-tissue morphologies to extract nectar from flowers. Nectarivory has evolved many times in terrestrial vertebrates, and in four bat families (Pteropodidae, Phyllostomidae, Vespertilionidae, and Mystacinidae). Within phyllostomids, specializations to nectarivory have been well documented in two subfamilies, Glossophaginae and Lonchophyllinae. However, nectarivory has also evolved independently in the genus Phyllostomus (subfamily Phyllostominae). Since Phyllostomus species have an omnivorous diet with a high consumption of nectar, they can be used to explore the basic morphological modifications linked to evolving a nectarivorous habit. Here, we focused on describing and comparing the morphological features potentially associated with nectarivory in Phyllostomus discolor. We present the first detailed tongue and palate morphological descriptions for P. discolor and perform skull morphometric analysis including 10 species. We found hair-like papillae on the tongue of P. discolor, a convergent feature with Glossophaginae and nectarivorous Pteropodids; these papillae likely confer an advantage when feeding on nectar. P. discolor does not show skull morphological features characteristic of nectarivorous bats, such as a long and narrow snout. We pose that the consumption of a variety of food, such as hard insects and fruits, and the large size of P. discolor relative to specialized nectarivores may create trade-offs against morphological specialization of the skull towards nectarivory. In contrast, a long and mobile tongue with hair-like papillae may be an evolutionary solution for nectar extraction that does not have a major impact on this species' ability to feed on other resources.

Multilayer Networks Assisting to Untangle Direct and Indirect Pathogen Transmission in Bats.

The importance of species that connect the different types of interactions is becoming increasingly recognized, and this role may be related to specific attributes of these species. Multilayer networks have two or more layers, which represent different types of interactions, for example, between different parasites and hosts that are nonetheless connected. The understanding of the ecological relationship between bats, ectoparasites, and vector-borne bacteria could shed some light on the complex transmission cycles of these pathogens. In this study, we investigated a multilayer network in Brazil formed by interactions between bat-bacteria, bat-ectoparasite, and ectoparasite-bacteria, and asked how these interactions overlap considering different groups and transmission modes. The multilayer network was composed of 31 nodes (12 bat species, 14 ectoparasite species, and five bacteria genera) and 334 links, distributed over three layers. The multilayer network has low modularity and shows a core-periphery organization, that is, composed of a few generalist species with many interactions and many specialist species participating in few interactions in the multilayer network. The three layers were needed to accurately describe the multilayer structure, while aggregation leads to loss of information. Our findings also demonstrated that the multilayer network is influenced by a specific set of species that can easily be connected to the behavior, life cycle, and type of existing interactions of these species. Four bat species (Artibeus lituratus, A. planirostris, Phyllostomus discolor, and Platyrrhinus lineatus), one ectoparasite species (Steatonyssus) and three bacteria genera (Ehrlichia, hemotropic Mycoplasma and Neorickettsia) are the most important species for the multilayer network structure. Finally, our study brings an ecological perspective under a multilayer network approach on the interactions between bats, ectoparasites, and pathogens. By using a multilayer approach (different types of interactions), it was possible to better understand these different ecological interactions and how they affect each other, advancing our knowledge on the role of bats and ectoparasites as potential pathogen vectors and reservoirs, as well as the modes of transmission of these pathogens.

The pale spear-nosed bat: A neuromolecular and transgenic model for vocal learning.

Vocal learning, the ability to produce modified vocalizations via learning from acoustic signals, is a key trait in the evolution of speech. While extensively studied in songbirds, mammalian models for vocal learning are rare. Bats present a promising study system given their gregarious natures, small size, and the ability of some species to be maintained in captive colonies. We utilize the pale spear-nosed bat (Phyllostomus discolor) and report advances in establishing this species as a tractable model for understanding vocal learning. We have taken an interdisciplinary approach, aiming to provide an integrated understanding across genomics (Part I), neurobiology (Part II), and transgenics (Part III). In Part I, we generated new, high-quality genome annotations of coding genes and noncoding microRNAs to facilitate functional and evolutionary studies. In Part II, we traced connections between auditory-related brain regions and reported neuroimaging to explore the structure of the brain and gene expression patterns to highlight brain regions. In Part III, we created the first successful transgenic bats by manipulating the expression of FoxP2, a speech-related gene. These interdisciplinary approaches are facilitating a mechanistic and evolutionary understanding of mammalian vocal learning and can also contribute to other areas of investigation that utilize P. discolor or bats as study species.

Genome assembly of the Pendlebury's roundleaf bat, Hipposideros pendleburyi, revealed the expansion of Tc1/Mariner DNA transposons in Rhinolophoidea.

Bats (Chiroptera) constitute the second largest order of mammals and have several distinctive features, such as true self-powered flight and strong immunity. The Pendlebury’s roundleaf bat, Hipposideros pendleburyi, is endemic to Thailand and listed as a vulnerable species. We employed the 10× Genomics linked-read technology to obtain a genome assembly of H. pendleburyi. The assembly size was 2.17 Gb with a scaffold N50 length of 15,398,518 bases. Our phylogenetic analysis placed H. pendleburyi within the rhinolophoid clade of the suborder Yinpterochiroptera. A synteny analysis showed that H. pendleburyi shared conserved chromosome segments (up to 105 Mb) with Rhinolophus ferrumequinum and Phyllostomus discolor albeit having different chromosome numbers and belonging different families. We found positive selection signals in genes involved in inflammation, spermatogenesis and Wnt signalling. The analyses of transposable elements suggested the contraction of short interspersed nuclear elements (SINEs) and the accumulation of young mariner DNA transposons in the analysed hipposiderids. Distinct mariners were likely horizontally transferred to hipposiderid genomes over the evolution of this family. The lineage-specific profiles of SINEs and mariners might involve in the evolution of hipposiderids and be associated with the phylogenetic separations of these bats from other bat families.

Object-specific adaptation in the auditory cortex of bats.

Identifying behaviorally relevant sounds is a vital function of the auditory system. Echolocating bats must negotiate a wealth of sounds during navigation and foraging. They must detect relatively rare but behaviorally relevant echoes and segregate them from many unimportant background echoes. For this, the bat's auditory system might rely on neural deviance detection-a process influencing the excitability of a neuron depending on the frequency of occurrence of a stimulus. To investigate neural deviance detection in the auditory cortex (AC) of anesthetized bats (Phyllostomus discolor), we designed sequences of repetitive virtual echoes differing in the spectrotemporal envelope, resembling those that bats might perceive in their natural environment. A standard echo was repeatedly played 10 times in these sequences, followed by a deviant echo at the end. Time intervals between echoes within the sequences varied. Our results show that neurons in the AC of the bat P. discolor are sensitive to novel virtual echoes presented at the end of these repetitive sequences: In 49% (62/126) of cortical neurons, extracellularly recorded responses adapted to the standard echo but showed a strong response to the deviant echo presented at the end. This effect depended strongly on the time intervals between echoes, with stronger adaptation at shorter intervals. This type of response might indicate a form of neuronal deviance detection mechanism in the AC that could help the bats to detect echoes of novel and potentially important objects within a stream of homogeneous background echoes.NEW & NOTEWORTHY In this study, we show that neurons in the auditory cortex of the bat Phyllostomus discolor are sensitive to novel acoustic stimuli in the context of repetitive virtual echo sequences differing in spectrotemporal envelope. This represents a form of neuronal deviance detection that might help the bats to detect echoes of rare but relevant objects among the clutter.

Genomewide Analysis and Biological Characterization of Cathelicidins with Potent Antimicrobial Activity and Low Cytotoxicity from Three Bat Species.

Cathelicidins are potent antimicrobial peptides with broad spectrum antimicrobial activity in many vertebrates and an important component of the innate immune system. However, our understanding of the genetic variations and biological characteristics of bat cathelicidins is limited. In this study, we performed genome-level analysis of the antimicrobial peptide cathelicidins from seven bat species in the six families, listed 19 cathelicidin-like sequences, and showed that the number of functional cathelicidin genes differed among bat species. Based on the identified biochemical characteristics of bat cathelicidins, three cathelicidins, HA-CATH (from Hipposideros armiger), ML-CATH (from Myotis lucifugus), and PD-CATH (from Phyllostomus discolor), with clear antimicrobial signatures were chemically synthesized and evaluated antimicrobial activity. HA-CATH showed narrow-spectrum antibacterial activity against a panel of 12 reference bacteria, comprising 6 Gram-negative and 6 Gram-positive strains. However, ML-CATH and PD-CATH showed potent antibacterial activity against a broad spectrum of Gram-negative and Gram-positive bacteria with minimum inhibitory concentration (MIC) of 1 and 3 μg/mL, respectively, against Staphylococcus aureus. ML-CATH and PD-CATH also showed antifungal activities against Candida albicans and Cryptococcus cuniculi with MIC of 5 to 40 μg/mL, respectively, and 80% inhibition of the metabolism of Mucor hiemalis hyphae at 80 μg/mL, while displaying minimal cytotoxicity to HaCaT cells. Taken together, although the spectrum and efficacy of bat cathelicidins were species-dependent, the antimicrobial activity of ML-CATH and PD-CATH was comparable to that of other highly active cathelicidins in vertebrates while having negligible cytotoxicity to mammalian cells. ML-CATH and PD-CATH can be exploited as promising candidates for the development of antimicrobial therapeutics.

Structural arrangement of auditory brainstem nuclei in the bats Phyllostomus discolor and Carollia perspicillata.

The structure of the mammalian auditory brainstem is evolutionarily highly plastic, and distinct nuclei arrange in a species-dependent manner. Such anatomical variability is present in the superior olivary complex (SOC) and the nuclei of the lateral lemniscus (LL). Due to the structure-function relationship in the auditory brainstem, the identification of individual nuclei supports the understanding of sound processing. Here, we comparatively describe the nucleus arrangement and the expression of functional markers in the auditory brainstem of the two bat species Phyllostomus discolor and Carollia perspicillata. Using immunofluorescent labeling, we describe the arrangement and identity of the SOC and LL nuclei based on the expression of synaptic markers (vesicular glutamate transporter 1 and glycine transporter 2), calcium-binding proteins, as well as the voltage-gated ion channel subunits Kv1.1 and HCN1. The distribution of excitatory and inhibitory synaptic labeling appears similar between both species and matches with that of other mammals. The detection of calcium-binding proteins indicates species-dependent differences and deviations from other mammals. Kv1.1 and HCN1 show largely the same expression pattern in both species, which diverges from other mammals, indicating functional adaptations in the cellular physiology of bat neurons.

Silvopastoral and conventional management of extensive livestock and the diversity of bats in fragments of tropical dry forest in C\xf3rdoba, Colombia

The establishment of extensive livestock systems in the Colombian Caribbean Region has historically generated a strong loss of the tropical dry forest (TDF) with negative effects on biodiversity. Currently, the implementation of silvopastoral systems (SPS) has been proposed with strategy to curb the loss of biodiversity caused by the conventional management system (CS). The objective was to evaluate the effect of SPS and CS of extensive livestock on the assemblage of bats associated with fragments of TDF. During a continuous year and a sampling effort of 30,240 h-net/night, the structure and composition of bat assemblage between SPS and CS were compared. 2788 bats belonging to six families, 23 genera, and 39 species were captured. The Phyllostomidae family presented the highest species richness (S = 30), with the greatest abundance in the Stenodermatinae subfamily (n = 1543). Bat assemblage in the SPS fragments was more equitable; and the relative abundance per species, per genera, and per foraging guilds was also significantly higher. The capture success showed significant variations between the climatic seasons (dry and rainy). The rate of species turnover was higher in the CS fragments. The species Artibeus planirostris, Artibeus lituratus, Carollia perspicillata, Carollia castanea, Phyllostomus discolor, Dermanura phaeotis, Uroderma convexum, Glossophaga soricina, C. brevicauda, and Sturnira lilium accounted for 92% of the captures. In conclusion, frugivorous bats were more abundant in the SPS, type of extensive livestock management that can generate greater temporal stability of bat assemblage. This research provides the first scientific evidence of the positive effect of silvopastoral management on the diversity of bats in tropical dry forest areas of the Colombian Caribbean region.

The vocal development of the pale spear-nosed bat is dependent on auditory feedback.

Human vocal development and speech learning require acoustic feedback, and humans who are born deaf do not acquire a normal adult speech capacity. Most other mammals display a largely innate vocal repertoire. Like humans, bats are thought to be one of the few taxa capable of vocal learning as they can acquire new vocalizations by modifying vocalizations according to auditory experiences. We investigated the effect of acoustic deafening on the vocal development of the pale spear-nosed bat. Three juvenile pale spear-nosed bats were deafened, and their vocal development was studied in comparison with an age-matched, hearing control group. The results show that during development the deafened bats increased their vocal activity, and their vocalizations were substantially altered, being much shorter, higher in pitch, and more aperiodic than the vocalizations of the control animals. The pale spear-nosed bat relies on auditory feedback for vocal development and, in the absence of auditory input, species-atypical vocalizations are acquired. This work serves as a basis for further research using the pale spear-nosed bat as a mammalian model for vocal learning, and contributes to comparative studies on hearing impairment across species.This article is part of the theme issue ‘Vocal learning in animals and humans’.

Vocal learning in animals and humans.

Vocal learning in animals and humans.

Communication breakdown: Limits of spectro-temporal resolution for the perception of bat communication calls

During vocal communication, the spectro-temporal structure of vocalizations conveys important contextual information. Bats excel in the use of sounds for echolocation by meticulous encoding of signals in the temporal domain. We therefore hypothesized that for social communication as well, bats would excel at detecting minute distortions in the spectro-temporal structure of calls. To test this hypothesis, we systematically introduced spectro-temporal distortion to communication calls of Phyllostomus discolor bats. We broke down each call into windows of the same length and randomized the phase spectrum inside each window. The overall degree of spectro-temporal distortion in communication calls increased with window length. Modelling the bat auditory periphery revealed that cochlear mechanisms allow discrimination of fast spectro-temporal envelopes. We evaluated model predictions with experimental psychophysical and neurophysiological data. We first assessed bats’ performance in discriminating original versions of calls from increasingly distorted versions of the same calls. We further examined cortical responses to determine additional specializations for call discrimination at the cortical level. Psychophysical and cortical responses concurred with model predictions, revealing discrimination thresholds in the range of 8–15 ms randomization-window length. Our data suggest that specialized cortical areas are not necessary to impart psychophysical resilience to temporal distortion in communication calls.

Unusual orthologs shed new light on the binding mechanism of ghrelin to its receptor GHSR1a

The gastric peptide ghrelin has important functions in energy metabolism and cellular homeostasis by activating growth hormone secretagogue receptor type 1a (GHSR1a). The N-terminal residues of ghrelin orthologs from all vertebrates are quite conserved; however, in orthologs from Cavia porcellus and Phyllostomus discolor, Ser2 and Leu5 are replaced by a smaller Ala and a positively charged Arg, respectively. In the present study, we first demonstrated that the hydrophobic Leu5 is essential for the function of human ghrelin, because Ala replacement caused an approximately 100-fold decrease in activity. However, replacement of Leu5 by an Arg residue caused much less disruption; further replacement of Ser2 by Ala almost restored full activity, although the [S2A] mutation itself showed slight detriments, implying that the positively charged Arg5 in the [S2A,L5R] mutant might form alternative interactions with certain receptor residues to compensate for the loss of the essential Leu5. To identify the responsible receptor residues, we screened GHSR1a mutants in which all conserved negatively charged residues in the extracellular regions and all aromatic residues in the ligand-binding pocket were mutated separately. According to the decrease in selectivity of the mutant receptors towards [S2A,L5R]ghrelin, we deduced that the positively charged Arg5 of the ghrelin mutant primarily interacts with the essential aromatic Phe286 at the extracellular end of the sixth transmembrane domain of GHSR1a by forming cation−π and π−π interactions. The present study provided new insights into the binding mechanism of ghrelin with its receptor, and thus would facilitate the design of novel ligands for GHSR1a.

Individual differences show that only some bats can cope with noise-induced masking and distraction.

Anthropogenic noise is a widespread pollutant that has received considerable recent attention. While alarming effects on wildlife have been documented, we have limited understanding of the perceptual mechanisms of noise disturbance, which are required to understand potential mitigation measures. Likewise, individual differences in response to noise (especially via perceptual mechanisms) are likely widespread, but lacking in empirical data. Here we use the echolocating bat Phyllostomus discolor, a trained discrimination task, and experimental noise playback to explicitly test perceptual mechanisms of noise disturbance. We demonstrate high individual variability in response to noise treatments and evidence for multiple perceptual mechanisms. Additionally, we highlight that only some individuals were able to cope with noise, while others were not. We tested for changes in echolocation call duration, amplitude, and peak frequency as possible ways of coping with noise. Although all bats strongly increased call amplitude and showed additional minor changes in call duration and frequency, these changes could not explain the differences in coping and non-coping individuals. Our understanding of noise disturbance needs to become more mechanistic and individualistic as research knowledge is transformed into policy changes and conservation action.