Publications

Abstract

Tropical ecosystems are known for high species diversity. Adaptations permitting niche differentiation enable species to coexist. Historically, research focused primarily on morphological and behavioral adaptations for foraging, roosting, and other basic ecological factors. Another important factor, however, is differences in sensory capabilities. So far, studies mainly have focused on the output of behavioral strategies of predators and their prey preference. Understanding the coexistence of different foraging strategies, however, requires understanding underlying cognitive and neural mechanisms. In this study, we investigate hearing in bats and how it shapes bat species coexistence. We present the hearing thresholds and echolocation calls of 12 different gleaning bats from the ecologically diverse Phyllostomid family. We measured their auditory brainstem responses to assess their hearing sensitivity. The audiograms of these species had similar overall shapes but differed substantially for frequencies below 9 kHz and in the frequency range of their echolocation calls. Our results suggest that differences among bats in hearing abilities contribute to the diversity in foraging strategies of gleaning bats. We argue that differences in auditory sensitivity could be important mechanisms shaping diversity in sensory niches and coexistence of species.

Abstract

Comparative studies of vocal learning and vocal non-learning animals can increase our understanding of the neurobiology and evolution of vocal learning and human speech. Mammalian vocal learning is understudied: most research has either focused on vocal learning in songbirds or its absence in non-human primates. Here we focus on a highly promising model species for the neurobiology of vocal learning: grey seals. We provide a neuroanatomical atlas (based on dissected brain slices and magnetic resonance images), a labelled MRI template, a 3D model with volumetric measurements of brain regions, and histological cortical stainings. Four main features of the grey seal brain stand out. (1) It is relatively big and highly convoluted. (2) It hosts a relatively large temporal lobe and cerebellum, structures which could support developed timing abilities and acoustic processing. (3) The cortex is similar to humans in thickness and shows the expected six-layered mammalian structure. (4) Expression of FoxP2 - a gene involved in vocal learning and spoken language - is present in deeper layers of the cortex. Our results could facilitate future studies targeting the neural and genetic underpinnings of mammalian vocal learning, thus bridging the research gap from songbirds to humans and non-human primates.Competing Interest StatementThe authors have declared no competing interest.

Abstract

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.

Abstract

Vocal production learning (VPL) is the capacity to learn to produce new vocalizations, which is a rare ability in the animal kingdom and thus far has only been identified in a handful of mammalian taxa and three groups of birds. Over the last few decades, approaches to the demonstration of VPL have varied among taxa, sound production systems and functions. These discrepancies strongly impede direct comparisons between studies. In the light of the growing number of experimental studies reporting VPL, the need for comparability is becoming more and more pressing. The comparative evaluation of VPL across studies would be facilitated by unified and generalized reporting standards, which would allow a better positioning of species on any proposed VPL continuum. In this paper, we specifically highlight five factors influencing the comparability of VPL assessments: (i) comparison to an acoustic baseline, (ii) comprehensive reporting of acoustic parameters, (iii) extended reporting of training conditions and durations, (iv) investigating VPL function via behavioural, perception-based experiments and (v) validation of findings on a neuronal level. These guidelines emphasize the importance of comparability between studies in order to unify the field of vocal learning.

Abstract

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, hear-
ing 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’.

Abstract

Differences in auditory perception between species are influenced by phylogenetic origin and the perceptual challenges imposed by the natural environment, such as detecting prey- or predator-generated sounds and communication signals. Bats are well suited for comparative studies on auditory perception since they predominantly rely on echolocation to perceive the world, while their social calls and most environmental sounds have low frequencies. We tested if hearing sensitivity and stimulus level coding in bats differ between high and low-frequency ranges by measuring auditory brainstem responses (ABRs) of 86 bats belonging to 11 species. In most species, auditory sensitivity was equally good at both high- and low-frequency ranges, while amplitude was more finely coded for higher frequency ranges. Additionally, we conducted a phylogenetic comparative analysis by combining our ABR data with published data on 27 species. Species-specific peaks in hearing sensitivity correlated with peak frequencies of echolocation calls and pup isolation calls, suggesting that changes in hearing sensitivity evolved in response to frequency changes of echolocation and social calls. Overall, our study provides the most comprehensive comparative assessment of bat hearing capacities to date and highlights the evolutionary pressures acting on their sensory perception.

Abstract

Comprising more than 1,400 species, bats possess adaptations unique among mammals including powered flight, unexpected longevity, and extraordinary immunity. Some of the molecular mechanisms underlying these unique adaptations includes DNA repair, metabolism and immunity. However, analyses have been limited to a few divergent lineages, reducing the scope of inferences on gene family evolution across the Order Chiroptera. We conducted an exhaustive comparative genomic study of 37 bat species, one generated in this study, encompassing a large number of lineages, with a particular emphasis on multi-gene family evolution across immune and metabolic genes. In agreement with previous analyses, we found lineage-specific expansions of the APOBEC3 and MHC-I gene families, and loss of the proinflammatory PYHIN gene family. We inferred more than 1,000 gene losses unique to bats, including genes involved in the regulation of inflammasome pathways such as epithelial defense receptors, the natural killer gene complex and the interferon-gamma induced pathway. Gene set enrichment analyses revealed genes lost in bats are involved in defense response against pathogen-associated molecular patterns and damage-associated molecular patterns. Gene family evolution and selection analyses indicate bats have evolved fundamental functional differences compared to other mammals in both innate and adaptive immune system, with the potential to enhance anti-viral immune response while dampening inflammatory signaling. In addition, metabolic genes have experienced repeated expansions related to convergent shifts to plant-based diets. Our analyses support the hypothesis that, in tandem with flight, ancestral bats had evolved a unique set of immune adaptations whose functional implications remain to be explored.

Abstract

High-quality and complete reference genome assemblies are fundamental for the application of genomics to biology, disease, and biodiversity conservation. However, such assemblies are available for only a few non-microbial species1,2,3,4. To address this issue, the international Genome 10K (G10K) consortium5,6 has worked over a five-year period to evaluate and develop cost-effective methods for assembling highly accurate and nearly complete reference genomes. Here we present lessons learned from generating assemblies for 16 species that represent six major vertebrate lineages. We confirm that long-read sequencing technologies are essential for maximizing genome quality, and that unresolved complex repeats and haplotype heterozygosity are major sources of assembly error when not handled correctly. Our assemblies correct substantial errors, add missing sequence in some of the best historical reference genomes, and reveal biological discoveries. These include the identification of many false gene duplications, increases in gene sizes, chromosome rearrangements that are specific to lineages, a repeated independent chromosome breakpoint in bat genomes, and a canonical GC-rich pattern in protein-coding genes and their regulatory regions. Adopting these lessons, we have embarked on the Vertebrate Genomes Project (VGP), an international effort to generate high-quality, complete reference genomes for all of the roughly 70,000 extant vertebrate species and to help to enable a new era of discovery across the life sciences.

Abstract

Background

Heterozygous variants in CNTNAP2 have been implicated in a wide range of neurological phenotypes, including intellectual disability (ID), epilepsy, autistic spectrum disorder (ASD), and impaired language. However, heterozygous variants can also be found in unaffected individuals. Biallelic CNTNAP2 variants are rarer and cause a well-defined genetic syndrome known as CASPR2 deficiency disorder, a condition characterised by ID, early-onset refractory epilepsy, language impairment, and autistic features.
Case-report

A 7-year-old boy presented with hyperkinetic stereotyped movements that started during early infancy and persisted over childhood. Abnormal movements consisted of rhythmic and repetitive shaking of the four limbs, with evident stereotypic features. Additional clinical features included ID, attention deficit-hyperactivity disorder (ADHD), ASD, and speech impairment, consistent with CASPR2 deficiency disorder. Whole-genome array comparative genomic hybridization detected a maternally inherited 0.402 Mb duplication, which involved intron 1, exon 2, and intron 2 of CNTNAP2 (c.97 +?_209-?dup). The affected region in intron 1 contains a binding site for the transcription factor FOXP2, potentially leading to abnormal CNTNAP2 expression regulation. Sanger sequencing of the coding region of CNTNAP2 also identified a paternally-inherited missense variant c.2752C > T, p.(Leu918Phe).
Conclusion

This case expands the molecular and phenotypic spectrum of CASPR2 deficiency disorder, suggesting that Hyperkinetic stereotyped movements may be a rare, yet significant, clinical feature of this complex neurological disorder. Furthermore, the identification of an in-frame, largely non-coding duplication in CNTNAP2 points to a sophisticated underlying molecular mechanism, likely involving impaired FOXP2 binding.

Abstract

How learning affects vocalizations is a key question in the study of animal
communication and human language. Parallel efforts in birds and humans
have taught us much about how vocal learning works on a behavioural
and neurobiological level. Subsequent efforts have revealed a variety of
cases among mammals in which experience also has a major influence on
vocal repertoires. Janik and Slater (Anim. Behav. 60, 1–11. (doi:10.1006/
anbe.2000.1410)) introduced the distinction between vocal usage and pro-
duction learning, providing a general framework to categorize how
different types of learning influence vocalizations. This idea was built on
by Petkov and Jarvis (Front. Evol. Neurosci. 4, 12. (doi:10.3389/fnevo.2012.
00012)) to emphasize a more continuous distribution between limited and
more complex vocal production learners. Yet, with more studies providing
empirical data, the limits of the initial frameworks become apparent.
We build on these frameworks to refine the categorization of vocal learning
in light of advances made since their publication and widespread agreement
that vocal learning is not a binary trait. We propose a novel classification
system, based on the definitions by Janik and Slater, that deconstructs
vocal learning into key dimensions to aid in understanding the mechanisms
involved in this complex behaviour. We consider how vocalizations can
change without learning, and a usage learning framework that considers
context specificity and timing. We identify dimensions of vocal production
learning, including the copying of auditory models (convergence/
divergence on model sounds, accuracy of copying), the degree of change
(type and breadth of learning) and timing (when learning takes place, the
length of time it takes and how long it is retained). We consider grey
areas of classification and current mechanistic understanding of these beha-
viours. Our framework identifies research needs and will help to inform
neurobiological and evolutionary studies endeavouring to uncover the
multi-dimensional nature of vocal learning.
This article is part of the theme issue ‘Vocal learning in animals and
humans’.

Abstract

Exceptionally long-lived species, including many bats, rarely show overt signs of aging, making it difficult to determine why species differ in lifespan. Here, we use DNA methylation (DNAm) profiles from 712 known-age bats, representing 26 species, to identify epigenetic changes associated with age and longevity. We demonstrate that DNAm accurately predicts chronological age. Across species, longevity is negatively associated with the rate of DNAm change at age-associated sites. Furthermore, analysis of several bat genomes reveals that hypermethylated age- and longevity-associated sites are disproportionately located in promoter regions of key transcription factors (TF) and enriched for histone and chromatin features associated with transcriptional regulation. Predicted TF binding site motifs and enrichment analyses indicate that age-related methylation change is influenced by developmental processes, while longevity-related DNAm change is associated with innate immunity or tumorigenesis genes, suggesting that bat longevity results from augmented immune response and cancer suppression.