Although language, and therefore spoken language or speech, is often considered unique to humans, the past several decades have seen a surge in nonhuman animal studies that inform us about human ...spoken language. Here, I present a modern, evolution-based synthesis of these studies, from behavioral to molecular levels of analyses. Among the key concepts drawn are that components of spoken language are continuous between species, and that the vocal learning component is the most specialized and rarest and evolved by brain pathway duplication from an ancient motor learning pathway. These concepts have important implications for understanding brain mechanisms and disorders of spoken language.
Humans and song-learning birds communicate acoustically using learned vocalizations. The characteristic features of this social communication behavior include vocal control by forebrain motor areas, ...a direct cortical projection to brainstem vocal motor neurons, and dependence on auditory feedback to develop and maintain learned vocalizations. These features have so far not been found in closely related primate and avian species that do not learn vocalizations. Male mice produce courtship ultrasonic vocalizations with acoustic features similar to songs of song-learning birds. However, it is assumed that mice lack a forebrain system for vocal modification and that their ultrasonic vocalizations are innate. Here we investigated the mouse song system and discovered that it includes a motor cortex region active during singing, that projects directly to brainstem vocal motor neurons and is necessary for keeping song more stereotyped and on pitch. We also discovered that male mice depend on auditory feedback to maintain some ultrasonic song features, and that sub-strains with differences in their songs can match each other's pitch when cross-housed under competitive social conditions. We conclude that male mice have some limited vocal modification abilities with at least some neuroanatomical features thought to be unique to humans and song-learning birds. To explain our findings, we propose a continuum hypothesis of vocal learning.
Brain evolution by brain pathway duplication Chakraborty, Mukta; Jarvis, Erich D.
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
12/2015, Volume:
370, Issue:
1684
Journal Article
Peer reviewed
Open access
Understanding the mechanisms of evolution of brain pathways for complex behaviours is still in its infancy. Making further advances requires a deeper understanding of brain homologies, novelties and ...analogies. It also requires an understanding of how adaptive genetic modifications lead to restructuring of the brain. Recent advances in genomic and molecular biology techniques applied to brain research have provided exciting insights into how complex behaviours are shaped by selection of novel brain pathways and functions of the nervous system. Here, we review and further develop some insights to a new hypothesis on one mechanism that may contribute to nervous system evolution, in particular by brain pathway duplication. Like gene duplication, we propose that whole brain pathways can duplicate and the duplicated pathway diverge to take on new functions. We suggest that one mechanism of brain pathway duplication could be through gene duplication, although other mechanisms are possible. We focus on brain pathways for vocal learning and spoken language in song-learning birds and humans as example systems. This view presents a new framework for future research in our understanding of brain evolution and novel behavioural traits.
The Origin and Diversification of Birds Brusatte, Stephen L.; O’Connor, Jingmai K.; Jarvis, Erich D.
Current biology,
10/2015, Volume:
25, Issue:
19
Journal Article
Peer reviewed
Open access
Birds are one of the most recognizable and diverse groups of modern vertebrates. Over the past two decades, a wealth of new fossil discoveries and phylogenetic and macroevolutionary studies has ...transformed our understanding of how birds originated and became so successful. Birds evolved from theropod dinosaurs during the Jurassic (around 165–150 million years ago) and their classic small, lightweight, feathered, and winged body plan was pieced together gradually over tens of millions of years of evolution rather than in one burst of innovation. Early birds diversified throughout the Jurassic and Cretaceous, becoming capable fliers with supercharged growth rates, but were decimated at the end-Cretaceous extinction alongside their close dinosaurian relatives. After the mass extinction, modern birds (members of the avian crown group) explosively diversified, culminating in more than 10,000 species distributed worldwide today.
In this review, Brusatte et al. discuss the wealth of new fossil discoveries and phylogenetic and macroevolutionary studies that have transformed our understanding of the origin, early diversification, and rise to dominance of birds.
Single-molecule sequencing instruments can generate multikilobase sequences with the potential to greatly improve genome and transcriptome assembly. However, the error rates of single-molecule reads ...are high, which has limited their use thus far to resequencing bacteria. To address this limitation, we introduce a correction algorithm and assembly strategy that uses short, high-fidelity sequences to correct the error in single-molecule sequences. We demonstrate the utility of this approach on reads generated by a PacBio RS instrument from phage, prokaryotic and eukaryotic whole genomes, including the previously unsequenced genome of the parrot Melopsittacus undulatus, as well as for RNA-Seq reads of the corn (Zea mays) transcriptome. Our long-read correction achieves >99.9% base-call accuracy, leading to substantially better assemblies than current sequencing strategies: in the best example, the median contig size was quintupled relative to high-coverage, second-generation assemblies. Greater gains are predicted if read lengths continue to increase, including the prospect of single-contig bacterial chromosome assembly.
Top panel shows mouse song system connectivity, highlighting the presence of a direct projection from M1 cortex to the vocal motor neurons of nucleus ambiguous (Amb). The bottom panel shows pitch ...imitation between C57 and BxD male mice over the course of 8weeks of co-housing in the presence of a female of either strain (conditions 1 and 2). Display omitted
► Mice have forebrain circuits active during singing. ► Mice have a direct motor cortical projection to vocal motor neurons. ► Mice make changes in vocalizations over early development that can not be explained by innate behavior alone. ► Mice have a partial dependence on auditory feedback to maintain acoustic features of their songs, but this is under debate. ► Mice can copy the pitch of another strain’s song as adults.
Mouse ultrasonic vocalizations (USVs) are often used as behavioral readouts of internal states, to measure effects of social and pharmacological manipulations, and for behavioral phenotyping of mouse models for neuropsychiatric and neurodegenerative disorders. However, little is known about the neurobiological mechanisms of rodent USV production. Here we discuss the available data to assess whether male mouse song behavior and the supporting brain circuits resemble those of known vocal non-learning or vocal learning species. Recent neurobiology studies have demonstrated that the mouse USV brain system includes motor cortex and striatal regions, and that the vocal motor cortex sends a direct sparse projection to the brainstem vocal motor nucleus ambiguous, a projection previously thought be unique to humans among mammals. Recent behavioral studies have reported opposing conclusions on mouse vocal plasticity, including vocal ontogeny changes in USVs over early development that might not be explained by innate maturation processes, evidence for and against a role for auditory feedback in developing and maintaining normal mouse USVs, and evidence for and against limited vocal imitation of song pitch. To reconcile these findings, we suggest that the trait of vocal learning may not be dichotomous but encompass a broad spectrum of behavioral and neural traits we call the continuum hypothesis, and that mice possess some of the traits associated with a capacity for limited vocal learning.
Oxytocin (OXT; hereafter OT) and arginine vasopressin or vasotocin (AVP or VT; hereafter VT) are neurotransmitter ligands that function through specific receptors to control diverse functions
. Here ...we performed genomic analyses on 35 species that span all major vertebrate lineages, including newly generated high-contiguity assemblies from the Vertebrate Genomes Project
. Our findings support the claim
that OT (also known as OXT) and VT (also known as AVP) are adjacent paralogous genes that have resulted from a local duplication, which we infer was through DNA transposable elements near the origin of vertebrates and in which VT retained more of the parental sequence. We identified six major oxytocin-vasotocin receptors among vertebrates. We propose that all six of these receptors arose from a single receptor that was shared with the common ancestor of invertebrates, through a combination of whole-genome and large segmental duplications. We propose a universal nomenclature based on evolutionary relationships for the genes that encode these receptors, in which the genes are given the same orthologous names across vertebrates and paralogous names relative to each other. This nomenclature avoids confusion due to differential naming in the pre-genomic era and incomplete genome assemblies, furthers our understanding of the evolution of these genes, aids in the translation of findings across species and serves as a model for other gene families.
New genome assemblies have been arriving at a rapidly increasing pace, thanks to decreases in sequencing costs and improvements in third-generation sequencing technologies
. For example, the number ...of vertebrate genome assemblies currently in the NCBI (National Center for Biotechnology Information) database
increased by more than 50% to 1,485 assemblies in the year from July 2018 to July 2019. In addition to this influx of assemblies from different species, new human de novo assemblies
are being produced, which enable the analysis of not only small polymorphisms, but also complex, large-scale structural differences between human individuals and haplotypes. This coming era and its unprecedented amount of data offer the opportunity to uncover many insights into genome evolution but also present challenges in how to adapt current analysis methods to meet the increased scale. Cactus
, a reference-free multiple genome alignment program, has been shown to be highly accurate, but the existing implementation scales poorly with increasing numbers of genomes, and struggles in regions of highly duplicated sequences. Here we describe progressive extensions to Cactus to create Progressive Cactus, which enables the reference-free alignment of tens to thousands of large vertebrate genomes while maintaining high alignment quality. We describe results from an alignment of more than 600 amniote genomes, which is to our knowledge the largest multiple vertebrate genome alignment created so far.
Routine haplotype-resolved genome assembly from single samples remains an unresolved problem. Here we describe an algorithm that combines PacBio HiFi reads and Hi-C chromatin interaction data to ...produce a haplotype-resolved assembly without the sequencing of parents. Applied to human and other vertebrate samples, our algorithm consistently outperforms existing single-sample assembly pipelines and generates assemblies of similar quality to the best pedigree-based assemblies.
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