Brain evolution by brain pathway duplication

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“One of the duplicated genes may then acquire a mutation in coding or regulatory sequences, which enables it to acquire a new function that then undergoes selection, a process known as neofunctionalization [12–15].”

“With the recent availability of genomes across the avian [93,177,178] and eventually primate [179,180] family trees, it becomes possible to discover candidate genes.”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“One overall hypothesis is that significant changes in the brain can be generated by novel gene functions owing to gene duplications or expansion of gene regulatory networks [7,9–12].”

“These results corroborated some earlier single gene expression, developmental, functional, and connectivity studies [24,52,63–67].”

“The brain also has evolved in a mosaic pattern, with some regions changing dramatically, while others have remained little changed through the course of evolution [23].”

“Duplication itself may modify the selection pressure on both structures, thereby allowing the individual structures to use the once single functional space in a mechanism reminiscent of adaptive radiation [38].”

“Many animals, such as annelids, have repeated parallel body segments or specialized limb types among species, where the replicated parts are thought to be owing to a repeating developmental genomic programme [121,122].”

“The pallium is largely layered in mammals, and mostly nuclear in birds, reptiles and other vertebrates, but with divergences among them [24,25].”

“One overall hypothesis is that significant changes in the brain can be generated by novel gene functions owing to gene duplications or expansion of gene regulatory networks [7,9–12].”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“Several alternative hypotheses have been proposed for evolution of vocal learning pathways, including that the pathways in humans and song-learning birds originated out of either a pre-existing auditory pathway [57,58], a non-motor cognitive region [59,60], a combined auditory–motor pathway [61], or completely de novo…”

“During development, neural stem cell/progenitor cells that give rise to forebrain circuits derive mainly from stem cells in the ventricular zone [129–131].”

“During development, neural stem cell/progenitor cells that give rise to forebrain circuits derive mainly from stem cells in the ventricular zone [129–131].”

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“However, there is as yet no evidence for loss of non-vocal motor or other functions in vocal learning species, but rather gain of functions even beyond vocal learning (such as learning how to dance) [94,96,97,99] and increases in relative brain-to-body sizes [103].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“The concept of neofunctionalization of genes [14] and subfunctionalization of genes [148] match those proposed for structural duplications [128,149,150].”

“Vocal learning is a rare trait, so far discovered in five distantly related groups of mammals (humans, bats, elephants, cetaceans (dolphins and whales) and pinnipeds (seals and sea lions)) and three distantly related groups of birds (parrots, songbirds and hummingbirds) [1,40–42].”

“In this regard, various hypotheses have been proposed to explain evolution of complex behavioural traits, including increases in brain or brain region size relative to body size, increases in total number of neurons or neuron density, and presence versus absence of particular neural networks that control a specific ty…”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“However, such an anatomical position is not present in hummingbirds, parrots, or humans [1,2].”

“B 3700150056 (b) Parrots contain a song system within a song system Parrots surpass other vocal learning avian species in their ability to imitate human speech and also rival non-human primates in their display of advanced cognitive skills and ability for tool use [2,69–74].”

“Allman and Kaas also proposed that development of the brain could be altered owing to a gene mutation so that a given area is duplicated [33,37].”

“SRGAP2 modulates activity of the ROBO axon guidance receptors, which are in turn activated by the SLIT family of protein ligands to modulate axonal/dendritic migration and branching in various brain regions [163–167].”

“B 3700150056 (b) Parrots contain a song system within a song system Parrots surpass other vocal learning avian species in their ability to imitate human speech and also rival non-human primates in their display of advanced cognitive skills and ability for tool use [2,69–74].”

“With the recent availability of genomes across the avian [93,177,178] and eventually primate [179,180] family trees, it becomes possible to discover candidate genes.”

“SRGAP2 modulates activity of the ROBO axon guidance receptors, which are in turn activated by the SLIT family of protein ligands to modulate axonal/dendritic migration and branching in various brain regions [163–167].”

“An example relevant to the topic of vocal learning and cognition is the Slit-Robo GTPase 2 gene (SRGAP2), which has undergone two partial duplications (SRGAP2B and SRGAP2C) uniquely in humans relative to other mammals [26,27,162].”

“Vocal learning is a rare trait, so far discovered in five distantly related groups of mammals (humans, bats, elephants, cetaceans (dolphins and whales) and pinnipeds (seals and sea lions)) and three distantly related groups of birds (parrots, songbirds and hummingbirds) [1,40–42].”

“Adapted from [2,50].”

“Many invertebrates and Amphioxus possess one Hox gene cluster, whereas the remaining vertebrates have four Hox gene clusters, in part owing to two whole-genome duplication events that occurred early in vertebrate evolution [151,154–158].”

“An example of loss of gene function and functional redundancy leading to duplication of structure is the Mauthner (M) cells, a pair of reticulospinal neurons that control escape behaviour in zebra fishes [139,172–174].”

“A long proposed explanation for generating increased cortical complexity is that a single region gradually differentiates into two or more areas [30–35].”

“An example relevant to the topic of vocal learning and cognition is the Slit-Robo GTPase 2 gene (SRGAP2), which has undergone two partial duplications (SRGAP2B and SRGAP2C) uniquely in humans relative to other mammals [26,27,162].”

“[101,102] showed that there is a comparable area 44-like region involved in orofacial musculature functions in macaque monkeys.”

“An example of loss of gene function and functional redundancy leading to duplication of structure is the Mauthner (M) cells, a pair of reticulospinal neurons that control escape behaviour in zebra fishes [139,172–174].”

“Once daughter cells reach their target location in the brain, they find their connecting partners in a process that requires cell adhesion and axon guidance genes [137,138].”

“However, there is as yet no evidence for loss of non-vocal motor or other functions in vocal learning species, but rather gain of functions even beyond vocal learning (such as learning how to dance) [94,96,97,99] and increases in relative brain-to-body sizes [103].”

“Several alternative hypotheses have been proposed for evolution of vocal learning pathways, including that the pathways in humans and song-learning birds originated out of either a pre-existing auditory pathway [57,58], a non-motor cognitive region [59,60], a combined auditory–motor pathway [61], or completely de novo…”

“These are transcription factors that control the anterior–posterior body plan axis and are situated in the genome in the same order as the body plan they control [136,151,152].”

“[101,102] showed that there is a comparable area 44-like region involved in orofacial musculature functions in macaque monkeys.”

“Both the core and shell song regions were functionally active in the production of learned vocalizations, as revealed by vocalizing-driven immediate early gene expression (EGR-1, C-FOS and DUSP-1), whereas the surrounding brain regions were active in production of non-singing motor behaviour, as revealed by rhythmic c…”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“However, there is as yet no evidence for loss of non-vocal motor or other functions in vocal learning species, but rather gain of functions even beyond vocal learning (such as learning how to dance) [94,96,97,99] and increases in relative brain-to-body sizes [103].”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“These results corroborated some earlier single gene expression, developmental, functional, and connectivity studies [24,52,63–67].”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“B 3700150056 (b) Parrots contain a song system within a song system Parrots surpass other vocal learning avian species in their ability to imitate human speech and also rival non-human primates in their display of advanced cognitive skills and ability for tool use [2,69–74].”

“Neural tracing and singing-regulated immediate early gene studies revealed some differences in connectivity and position or shape of song nuclei in parrots, but no clear differences were noted in the presence or absence of song system structures [55,75,76,78–80].”

“differential gene expression experiments, which show that the avian pallium has a functional columnar organization similar to the mammalian pallial domain [39,52–54].”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“differential gene expression experiments, which show that the avian pallium has a functional columnar organization similar to the mammalian pallial domain [39,52–54].”

“SRGAP2 modulates activity of the ROBO axon guidance receptors, which are in turn activated by the SLIT family of protein ligands to modulate axonal/dendritic migration and branching in various brain regions [163–167].”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“Connectivity based on summaries in [39,55,56,76,83,84].”

“Several alternative hypotheses have been proposed for evolution of vocal learning pathways, including that the pathways in humans and song-learning birds originated out of either a pre-existing auditory pathway [57,58], a non-motor cognitive region [59,60], a combined auditory–motor pathway [61], or completely de novo…”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“Neural tracing and singing-regulated immediate early gene studies revealed some differences in connectivity and position or shape of song nuclei in parrots, but no clear differences were noted in the presence or absence of song system structures [55,75,76,78–80].”

“These results corroborated some earlier single gene expression, developmental, functional, and connectivity studies [24,52,63–67].”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“However, there is as yet no evidence for loss of non-vocal motor or other functions in vocal learning species, but rather gain of functions even beyond vocal learning (such as learning how to dance) [94,96,97,99] and increases in relative brain-to-body sizes [103].”

“It would be exciting to determine if similar duplications of brain pathways have occurred in humans, not only in the speech pathways but also for other advanced motor movements such as dancing [97–99].”

“However, there is as yet no evidence for loss of non-vocal motor or other functions in vocal learning species, but rather gain of functions even beyond vocal learning (such as learning how to dance) [94,96,97,99] and increases in relative brain-to-body sizes [103].”

“One overall hypothesis is that significant changes in the brain can be generated by novel gene functions owing to gene duplications or expansion of gene regulatory networks [7,9–12].”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“They do so by controlling regional neuronal identity, stem cell progenitors, cell migration and cell death [159,160].”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“Neural tracing and singing-regulated immediate early gene studies revealed some differences in connectivity and position or shape of song nuclei in parrots, but no clear differences were noted in the presence or absence of song system structures [55,75,76,78–80].”

“With the recent availability of genomes across the avian [93,177,178] and eventually primate [179,180] family trees, it becomes possible to discover candidate genes.”

“Some such changes may have occurred with the emergence of the telencephalon during the invertebrate to vertebrate transition, indicating that the central nervous system has been an important target of selection [4,6–8].”

“Many invertebrates and Amphioxus possess one Hox gene cluster, whereas the remaining vertebrates have four Hox gene clusters, in part owing to two whole-genome duplication events that occurred early in vertebrate evolution [151,154–158].”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“The direct projection to the brainstem vocal MN is considered critical for the evolution of vocal learning and spoken language, as it is either absent or very sparse in vocal non-learners [2,42,87–92].”

“Both the core and shell song regions were functionally active in the production of learned vocalizations, as revealed by vocalizing-driven immediate early gene expression (EGR-1, C-FOS and DUSP-1), whereas the surrounding brain regions were active in production of non-singing motor behaviour, as revealed by rhythmic c…”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“Overall, structural duplications have been proposed to be one mechanism that allows for morphological decoupling [126].”

“The daughter cells travel to their positions either by radial migration perpendicularly away from the ventricle (such as excitatory neurons within layers of the mammalian cortex), and/or by tangential migration parallel to the ventricle (such as inhibitory neurons that migrate from the basal ganglia into the cortex) […”

“Even theories on gene evolution through gene duplication have influenced the theories on brain evolution by morphological duplication [139,141].”

“Several alternative hypotheses have been proposed for evolution of vocal learning pathways, including that the pathways in humans and song-learning birds originated out of either a pre-existing auditory pathway [57,58], a non-motor cognitive region [59,60], a combined auditory–motor pathway [61], or completely de novo…”

“The concept of neofunctionalization of genes [14] and subfunctionalization of genes [148] match those proposed for structural duplications [128,149,150].”

“These results corroborated some earlier single gene expression, developmental, functional, and connectivity studies [24,52,63–67].”

“differential gene expression experiments, which show that the avian pallium has a functional columnar organization similar to the mammalian pallial domain [39,52–54].”

“Their local brain region identity is thought to be controlled by patterning transcription factors, such as the homeobox (Hox) genes [135,136].”

“Both the core and shell song regions were functionally active in the production of learned vocalizations, as revealed by vocalizing-driven immediate early gene expression (EGR-1, C-FOS and DUSP-1), whereas the surrounding brain regions were active in production of non-singing motor behaviour, as revealed by rhythmic c…”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“Based on these and other findings, it is generally proposed that the direct CM system of M1 is a recently evolved brain structure that conferred evolutionarily novel functions in the motor system in primates, including independent voluntary control of finger movements, which are more advanced in primates compared with…”

“Since all of the cortex is connected with all of the basal ganglia and thalamus [112], when a cortex region is duplicated, one would expect to see a concomitant duplication in the connected basal ganglia and thalamic regions [22,33].”

“The nuances for limited vocal plasticity and an associated neural circuit in mice and non-human primates are also still an ongoing debate that requires further investigation [104–111].”

“Connectivity based on summaries in [39,55,56,76,83,84].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“Since all of the cortex is connected with all of the basal ganglia and thalamus [112], when a cortex region is duplicated, one would expect to see a concomitant duplication in the connected basal ganglia and thalamic regions [22,33].”

“In the past few decades, significant advances have been made in guiding our understanding of the evolution and mechanisms of brain pathways for vocal learning in birds and humans [2,40,42–49] (figure 1).”

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“Many invertebrates and Amphioxus possess one Hox gene cluster, whereas the remaining vertebrates have four Hox gene clusters, in part owing to two whole-genome duplication events that occurred early in vertebrate evolution [151,154–158].”

“Several alternative hypotheses have been proposed for evolution of vocal learning pathways, including that the pathways in humans and song-learning birds originated out of either a pre-existing auditory pathway [57,58], a non-motor cognitive region [59,60], a combined auditory–motor pathway [61], or completely de novo…”

“Other hypotheses posit that existing genes are modified, including changes in coding sequence, cis-regulatory motifs [16,17] or new alternative mRNA splice variants [18–21], a process known as subfunctionalization [12–14].”

“A striking example of independently evolved morphological duplications is the diversification of the adductor mandibular muscles in teleost fish jaws, which have independently subdivided several times during tetraodontiform evolution [123–125].”

“The daughter cells travel to their positions either by radial migration perpendicularly away from the ventricle (such as excitatory neurons within layers of the mammalian cortex), and/or by tangential migration parallel to the ventricle (such as inhibitory neurons that migrate from the basal ganglia into the cortex) […”

“Recently, based on comparative genomic analyses across the bird family tree, unique gene duplications were found in the songbird lineage and some of these genes had enriched or nearly exclusive expression in the song learning nuclei [161].”

“auditory Field L), but in parrots it receives additional auditory input from a small part of the nucleus basorostralis (B), the remainder of which is somatosensory [81].”

“Some such changes may have occurred with the emergence of the telencephalon during the invertebrate to vertebrate transition, indicating that the central nervous system has been an important target of selection [4,6–8].”

“B 3700150056 (b) Parrots contain a song system within a song system Parrots surpass other vocal learning avian species in their ability to imitate human speech and also rival non-human primates in their display of advanced cognitive skills and ability for tool use [2,69–74].”

“In addition, changes in the regulation of some genes that may allow greater vocal–motor–auditory integration in vocal learning systems could have influenced changes in the surrounding motor areas to allow greater auditory–motor entrainment and synchronizing of body movements to the rhythm of music for dance in parrots…”

“The daughter cells travel to their positions either by radial migration perpendicularly away from the ventricle (such as excitatory neurons within layers of the mammalian cortex), and/or by tangential migration parallel to the ventricle (such as inhibitory neurons that migrate from the basal ganglia into the cortex) […”

“Even theories on gene evolution through gene duplication have influenced the theories on brain evolution by morphological duplication [139,141].”

“B 3700150056 (b) Parrots contain a song system within a song system Parrots surpass other vocal learning avian species in their ability to imitate human speech and also rival non-human primates in their display of advanced cognitive skills and ability for tool use [2,69–74].”

“Neural tracing and singing-regulated immediate early gene studies revealed some differences in connectivity and position or shape of song nuclei in parrots, but no clear differences were noted in the presence or absence of song system structures [55,75,76,78–80].”

“In this regard, various hypotheses have been proposed to explain evolution of complex behavioural traits, including increases in brain or brain region size relative to body size, increases in total number of neurons or neuron density, and presence versus absence of particular neural networks that control a specific ty…”

“They do so by controlling regional neuronal identity, stem cell progenitors, cell migration and cell death [159,160].”

“An example relevant to the topic of vocal learning and cognition is the Slit-Robo GTPase 2 gene (SRGAP2), which has undergone two partial duplications (SRGAP2B and SRGAP2C) uniquely in humans relative to other mammals [26,27,162].”

“Gene duplications have been found to influence the development and function of many organs and tissues, including brains, eyes and wings [11,139–147].”

“Second, analyses of brain gene expression profiles strongly suggest that songbirds and parrots independently evolved vocal learning pathways by duplication of preexisting, surrounding motor circuits (57, 58).”