Human language seems to be unique and has often been studied as an isolated phenomenon, but few traits are entirely without precedent. As originally suggested by Darwin, our extraordinary capacity to acquire language should be explicable as the product of descent with modification.
Molecular methods offer a new kind of data for shedding light on language evolution, especially in tandem with changing views of neural substrates according to which language depends on a distributed network of cortical and subcortical circuits with substantial overlap with other cognitive domains.
Comparisons between the genomes of humans and chimpanzees, our closest extant non-speaking relatives, show over 35 million substitutions and 5 million indels, with most changes resulting from neutral drift. Large-scale between- and within-species sequence comparisons have not yet uncovered specific genes that are related to language.
Genes that are expressed in the brain tend to show less human–chimpanzee divergence than other genes, both in terms of protein structure and expression level, probably owing to higher functional constraint in neural tissue. Nonetheless, against this background, there seems to have been accelerated change for brain-related genes on the human lineage when compared with the branch leading to the chimpanzee.
Expression-profiling studies have yet to identify any particular human gene (or set of genes) that is uniquely expressed in language-related regions of adult brains. Most observed expression differences between the brains of humans and chimpanzees have been found to be common to all cortical regions, although this might reflect a lack of power when using current approaches.
Positional cloning studies of human neurodevelopmental disorders, such as specific language impairment, developmental dyslexia and autism, can provide candidate genes for targeted evolutionary investigation.
Direct evidence of a specific gene that influences language acquisition has come from a rare monogenic communication disorder, caused by mutation of a forkhead box transcription factor (FOXP2). Disruption of FOXP2 leads to problems in learning and producing complex sequences of mouth movements, accompanied by wide-ranging linguistic deficits.
FOXP2 is highly conserved in distant vertebrates, but underwent a 60-fold increase in amino-acid substitution rate on the human lineage — of three changes that distinguish human and mouse orthologues, two occurred on the human branch after splitting from the chimpanzee. The human within-species variability flanking these substitutions indicates a recent selective sweep.
Human FOXP2 gene expression shows intriguing overlaps with sites of pathology identified by structural/functional neuroimaging of patients with FOXP2-associated disorder. These data implicate FOXP2 in the development and/or function of circuitry involving the frontal cortex, striatum and cerebellum — networks that support (among other processes) learning and production of speech sequences.
Rodents, birds, reptiles and fish similarly show FoxP2 expression in circuits related to sensory-motor function and control of skilled coordinated movements. Species-specific differences in FoxP2 regulation in the song system of vocal-learning birds seem to relate to changes in vocal plasticity; ancient neural functions of FoxP2 might have been co-opted to subserve vocal communication on more than one occasion.
Although FoxP2 is probably just one piece of the evolutionary puzzle, research into the gene highlights how multidisciplinary studies of the functions of language-related genes in humans, animals and birds offer new routes for addressing old questions about the neural systems that subserve language.
The human capacity to acquire complex language seems to be without parallel in the natural world. The origins of this remarkable trait have long resisted adequate explanation, but advances in fields that range from molecular genetics to cognitive neuroscience offer new promise. Here we synthesize recent developments in linguistics, psychology and neuroimaging with progress in comparative genomics, gene-expression profiling and studies of developmental disorders. We argue that language should be viewed not as a wholesale innovation, but as a complex reconfiguration of ancestral systems that have been adapted in evolutionarily novel ways.
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We thank W. Enard for his helpful comments on this manuscript, and C. S. Lai and F. J. Liégeois for assistance with the figures. S.E.F. is a Royal Society Research Fellow, and his research is also supported by the Wellcome Trust, the 6th European Community Framework Programme and the Brain Sciences Initiative of the UK Medical Research Council. G.F.M. thanks the US National Institutes of Health and the Human Frontier Science Program for financial support.
The authors declare no competing financial interests.
The scientific study of language.
The study of the production, perception and physical properties of speech sounds.
The study of the sound systems of languages and the ways in which speech sounds can be combined.
- Cerebral cortex
The outer layer of the mammalian cerebrum, which is involved in processes such as sensation, perception, cognition and (in humans) language.
A single evolutionary event that has large-scale effects on a phenotype, which involves concurrent alteration of numerous characteristics.
- Sexual selection
The evolution of a trait as a consequence of competition among members of one sex (usually males) for fertilization opportunities with the other sex.
Modern humans and all extinct human-like ancestors and their relatives that existed following divergence from other ape lineages. Includes all species of the genera Homo and Australopithecus, and other ancient forms such as Paranthropus and Ardipithecus.
The specialized upper portion of the respiratory tract that houses the vocal cords — folds of mucous membrane that provide the source for vocal sounds. The low position of the larynx in adult humans allows a rich phonetic repertoire, but its significance for language evolution remains a matter of debate.
The vocabulary and word forms of a language.
An inability to produce and/or comprehend language that is due to brain injury or disease.
Describes the brain structures that are below the cerebral cortex.
Part of the group of interconnected subcortical nuclei that are known as the basal ganglia. The striatum comprises two nuclei the — caudate and putamen — and is involved in the planning and modulation of movement pathways, as well as a range of other cognitive processes.
A forebrain structure that is located beneath the cerebral hemispheres and that modulates and relays sensory signals to and from the cerebral cortex.
A multilayered structure in the vertebrate hindbrain that comprises a complex mixture of different cell types. The cerebellum modulates the force and range of movements, maintains balance and is involved in motor learning.
- Hemispheric asymmetries
These are differences in the structure or function of the left and right hemisphere counterparts of a particular brain region.
- Motor control
The ability to direct and coordinate muscle movements.
Peaks in the acoustic energy spectrum that result from the resonant frequencies of vocal tracts.
A process by which ever more complex elements are generated through the repeated recombination of simpler elements.
- Positive selection
When a novel allele that increases the fitness of an organism becomes more prevalent in the population.
- Purifying selection
Selection against alleles that have harmful phenotypic effects, which leads to their loss from the population.
When two closely related species are compared, the status of the common ancestor (for example, at a site of substitution) could be deduced by including a more distant third species that branched from the parent group before the other two groups diverged.
- Functional constraint
The degree to which changes in gene sequence are tolerated. For genes that have higher functional constraints a larger proportion of potential mutations are deleterious, reducing the substitution rate.
- Maximum likelihood
A statistical method that is commonly used to make inferences about the most likely value of one of more parameters that underlie a given data set.
- Selective sweep
Occurs when an allele increases in frequency as a consequence of positive selection and concurrently eliminates neutral variation at linked chromosomal sites.
A difference between sequences of related genomes that results from an insertion or deletion event; a term that is especially used when the evolutionary direction of the change is unknown.
- Encephalization quotient
A measure of the relative brain size, in which the brain weight is compared with that of the average living mammal of equal body weight.
The cellular composition of a bodily structure. In neuroscience the term is used to refer to local differences in the arrangement of nerve cells in particular regions of the brain.
- Speech-sound disorder
An inability to produce speech sounds that would be expected on the basis of age and dialect, but in the absence of an obvious cause (such as cerebral palsy or hearing impairment). This disorder might occur in isolation or together with other linguistic deficits.
Social aspects of communication — in particular the influence of context on the interpretation of meaning.
A measurable intermediate trait that is assumed to provide a closer link to the neurobiological substrate of a disorder.
- Forkhead box
An 80–100 amino-acid motif that is found in a similar form in every member of the forkhead box family of transcription factors. It forms a winged-helix structure that allows the protein to bind to DNA.
- Nuclear localization signals
Short stretches of amino acids that help to mediate the transport of proteins to the nucleus of the cell.
The reappearance in an organism of characteristics that were typical of the organism's remote ancestors.
- Purkinje cells
The output neurons of the cerebellum, which integrate complex inputs and project to the deep motor nuclei of the brain.
- Inferior olivary nucleus
A precerebellar nucleus that provides direct input to the Purkinje cells through a network of climbing fibres. Olivocerebellar circuits have a crucial role in controlling movement.
- Area X
A striatal nucleus that is present in the song system in the brains of vocal-learning birds.
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Fisher, S., Marcus, G. The eloquent ape: genes, brains and the evolution of language. Nat Rev Genet 7, 9–20 (2006). https://doi.org/10.1038/nrg1747
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