Publications

Abstract

Bats possess extraordinary adaptations, including flight, echolocation, extreme longevity and unique immunity. High-quality genomes are crucial for understanding the molecular basis and evolution of these traits. Here we incorporated long-read sequencing and state-of-the-art scaffolding protocols1 to generate, to our knowledge, the first reference-quality genomes of six bat species (Rhinolophus ferrumequinum, Rousettus aegyptiacus, Phyllostomus discolor, Myotis myotis, Pipistrellus kuhlii and Molossus molossus). We integrated gene projections from our ‘Tool to infer Orthologs from Genome Alignments’ (TOGA) software with de novo and homology gene predictions as well as short- and long-read transcriptomics to generate highly complete gene annotations. To resolve the phylogenetic position of bats within Laurasiatheria, we applied several phylogenetic methods to comprehensive sets of orthologous protein-coding and noncoding regions of the genome, and identified a basal origin for bats within Scrotifera. Our genome-wide screens revealed positive selection on hearing-related genes in the ancestral branch of bats, which is indicative of laryngeal echolocation being an ancestral trait in this clade. We found selection and loss of immunity-related genes (including pro-inflammatory NF-κB regulators) and expansions of anti-viral APOBEC3 genes, which highlights molecular mechanisms that may contribute to the exceptional immunity of bats. Genomic integrations of diverse viruses provide a genomic record of historical tolerance to viral infection in bats. Finally, we found and experimentally validated bat-specific variation in microRNAs, which may regulate bat-specific gene-expression programs. Our reference-quality bat genomes provide the resources required to uncover and validate the genomic basis of adaptations of bats, and stimulate new avenues of research that are directly relevant to human health and disease

Abstract

Vocal production learning (VPL), or the ability to modify vocalizations through the imitation of sounds, is a rare trait in the animal kingdom. While humans are exceptional vocal learners, few other mammalian species share this trait. Owing to their singular ecology and lifestyle, bats are highly specialized for the precise emission and reception of acoustic signals. This specialization makes them ideal candidates for the study of vocal learning, and several bat species have previously shown evidence supportive of vocal learning. Here we use a sophisticated automated set-up and a contingency training paradigm to explore the vocal learning capacity of pale spear-nosed bats. We show that these bats are capable of directional change of the fundamental frequency of their calls according to an auditory target. With this study, we further highlight the importance of bats for the study of vocal learning and provide evidence for the VPL capacity of the pale spear-nosed bat.

Abstract

The comparative approach can provide insight into the evolution of human speech, language and social communication by studying relevant traits in animal systems. Bats are emerging as a model system with great potential to shed light on these processes given their learned vocalizations, close social interactions, and mammalian brains and physiology. A recent framework outlined the multiple levels of investigation needed to understand vocal learning across a broad range of non-human species, including cetaceans, pinnipeds, elephants, birds and bats. Here, we apply this framework to the current state-of-the-art in bat research. This encompasses our understanding of the abilities bats have displayed for vocal learning, what is known about the timing and social structure needed for such learning, and current knowledge about the prevalence of the trait across the order. It also addresses the biology (vocal tract morphology, neurobiology and genetics) and evolution of this trait. We conclude by highlighting some key questions that should be answered to advance our understanding of the biological encoding and evolution of speech and spoken communication. This article is part of the theme issue 'What can animal communication teach us about human language?'

Abstract

Theories addressing the biological basis of language must be built on
an appreciation of the ways that molecular and neurobiological substrates
can contribute to aspects of human cognition. Here, we lay out
the principles by which a genome could potentially encode the necessary
information to produce a language-ready brain. We describe
what genes are; how they are regulated; and how they affect the formation,
function, and plasticity of neuronal circuits. At each step,
we give examples of molecules implicated in pathways that are important
for speech and language. Finally, we discuss technological advances
in genomics that are revealing considerable genotypic variation in
the human population, from rare mutations to common polymorphisms,
with the potential to relate this variation to natural variability
in speech and language skills. Moving forward, an interdisciplinary
approach to the language sciences, integrating genetics, neurobiology,
psychology, and linguistics, will be essential for a complete understanding
of our unique human capacities.

Abstract

Background Bats are able to employ an astonishingly complex vocal repertoire for navigating their environment and conveying social information. A handful of species also show evidence for vocal learning, an extremely rare ability shared only with humans and few other animals. However, despite their potential for the study of vocal communication, bats remain severely understudied at a molecular level. To address this fundamental gap we performed the first transcriptome profiling and genetic interrogation of molecular networks in the brain of a highly vocal bat species, Phyllostomus discolor. Results Gene network analysis typically needs large sample sizes for correct clustering, this can be prohibitive where samples are limited, such as in this study. To overcome this, we developed a novel bioinformatics methodology for identifying robust co-expression gene networks using few samples (N=6). Using this approach, we identified tissue-specific functional gene networks from the bat PAG, a brain region fundamental for mammalian vocalisation. The most highly connected network identified represented a cluster of genes involved in glutamatergic synaptic transmission. Glutamatergic receptors play a significant role in vocalisation from the PAG, suggesting that this gene network may be mechanistically important for vocal-motor control in mammals. Conclusion We have developed an innovative approach to cluster co-expressing gene networks and show that it is highly effective in detecting robust functional gene networks with limited sample sizes. Moreover, this work represents the first gene network analysis performed in a bat brain and establishes bats as a novel, tractable model system for understanding the genetics of vocal mammalian communication.