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The evolution of language-readiness in the hominin lineage: an analysis of open chromatin regions implicated in gene regulation

Name
Konstantin
Surname
Gunbin
Scientific organization
Center of Brain Neurobiology and Neurogenetics, Institute of Cytology and Genetics SB RAS
Academic degree
Ph.D.
Position
Staff Researcher
Scientific discipline
Life Sciences & Medicine
Topic
The evolution of language-readiness in the hominin lineage: an analysis of open chromatin regions implicated in gene regulation
Abstract
Language evolution studies rely on indirect evidence, mostly related to speech organs and human behaviour. Comparative genomic studies have demonstrated >99.9% of identity between modern human, Neanderthal and Denisovan protein-coding sequences, which is in sharp contrast with the significant evolutionary distance between these three hominin species and with their physical distinctive features. Therefore, it is reasonable to anticipate an elevated rate of changes in the regulatory regions of the genes.
Keywords
DNAseI Hypersensitive Sites (DHSs), molecular evolution, language-readiness, extinct vs. extant hominins, early vs. present-day modern humans, self-domestication hypothesis
Summary

Motivation and Aim: Language evolution studies rely on indirect evidence, mostly related to speech organs and human behaviour. The successful retrieval of ancient genomes is expected to contribute significantly to our knowledge of the biological changes that shaped hominin cognition and communication abilities. Comparative genomic studies have demonstrated >99.9% of identity between modern human (M) and Neanderthal (N) and Denisovan (D) protein-coding gene sequences, which is in sharp contrast with the significant (~1 MYA) evolutionary distance between these three hominin species and with their behavioral and physical distinctive features [1,2]. Therefore, it is reasonable to anticipate an elevated rate of changes in the regulatory regions of the genes, particularly, of those involved in brain development and function. In our past research we have put forth a list of candidate genes that may account for the evolutionary emergence of our language-readiness (i.e. our species-specific ability to learn and use languages), that we expect to have resulted from changes in the brain wiring and neuronal workspace linked to the globularization of the human skull [3-5]. Interestingly, some of these genes are also involved in (or interact with genes involved in) the development and function of the neural crest [6], whose hypofunction has been hypothesized to give rise to the constellation of traits linked the domestication of mammals [7]. Self-domestication of the human species has been argued to have created the suitable cultural niche for the emergence of complex, modern languages [8-10]. Some of the genes encompassing our list of candidates show differences with the N and D homologues, which affect their regulatory regions, their coding regions, and/or their methylation patterns [3-5]. Our aim was to look for additional signatures of differential expression patterns of these genes important for language-readiness and self-domestication between M, N, and D, but also with Ust’-Ishim (UI) humans, examining the distribution of open chromatin regions implicated in gene regulation.

Methods and Algorithms: First, we aligned SNPs and indels from D [11], N [12], and UI [13] that are not found in M. Second, we mapped common changes in the D-N and D-N-UI branches onto DNAse I Hypersensitive Sites (DHSs) from M with an annotated effect (activation or repression) on gene expression [14]. Third, we checked if the positions evolved in D-N and D-N-UI overlapped with transcription factor binding sites showing signatures of negative or positive selection in M (using ENCODE RegTfbs data track and INSIGHT approach [15]). This allowed us to put forth a list of putative genes affected by changes in DHSs in humans as a whole and in present-day humans, respectively. Finally, we analyzed the nearest interactions between these two lists and our list of candidates for language-readiness and self-domestication using GeneMania data (http://genemania.org/).

Results: Our results are suggestive of potential differences between M and N, D and UI regarding the regulation pattern of genes involved in osteogenesis, brain function, and immunity. This is interesting in view of the hypothesized link between the emergence of language-readiness and changes in the skull-brain cross-talk [3], but also in the brain-immune system cross-talk [16]. We have also found that the regulation of FOXP1 (in D), and CNTNAP2 (in N), two genes related to language function [17,18] could have been affected by severe changes in DHSs these hominin species. Finally, we found that several of our candidates for language-readiness and self-domestication are predicted to interact with genes expected to have changed in their regulation pattern in our species, but also with others that could be differentially expressed in M compared to UI. In the whole our findings give support to the view that differences in the expression patterns of known candidates for cognitive development and language evolution may account for the presumed differences in cognitive and linguistic abilities between extinct and extant hominins, but also between early and present-day humans.

Availability: Data available upon the requests to the authors.

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