FOXP2 variation in great ape populations offers insight into the evolution of communication skills

Nicky Staes,John J Ely,Tomas Marques-Bonet,Marc De Manuel,William D Hopkins,Brenda J Bradley,Michael Massiah,Chet C Sherwood,Elaine E Guevara,Katharine Wright,Michael Krützen

doi:10.1038/s41598-017-16844-x

Abstract

The gene coding for the forkhead box protein P2 (FOXP2) is associated with human language disorders. Evolutionary changes in this gene are hypothesized to have contributed to the emergence of speech and language in the human lineage. Although FOXP2 is highly conserved across most mammals, humans differ at two functional amino acid substitutions from chimpanzees, bonobos and gorillas, with an additional fixed substitution found in orangutans. However, FOXP2 has been characterized in only a small number of apes and no publication to date has examined the degree of natural variation in large samples of unrelated great apes. Here, we analyzed the genetic variation in the FOXP2 coding sequence in 63 chimpanzees, 11 bonobos, 48 gorillas, 37 orangutans and 2 gibbons and observed undescribed variation in great apes. We identified two variable polyglutamine microsatellites in chimpanzees and orangutans and found three nonsynonymous single nucleotide polymorphisms, one in chimpanzees, one in gorillas and one in orangutans with derived allele frequencies of 0.01, 0.26 and 0.29, respectively. Structural and functional protein modeling indicate a biochemical effect of the substitution in orangutans, and because of its presence solely in the Sumatran orangutan species, the mutation may be associated with reported population differences in vocalizations.

Highlights

Language is a defining feature of human uniqueness
We identified 52 single nucleotide variants (SNV) among apes, of which 21 were fixed species-specific substitutions, and 31 were within-species single nucleotide polymorphisms (SNPs) (Fig. 1, Table S5)
A C/A SNP in exon 16 causes a Proline to Threonine substitution (Pro626Thr). The latter SNP is found only in Sumatran orangutans (Pongo abelii), with the ancestral C allele again present at a higher frequency (0.71)

Summary

Introduction

Language is a defining feature of human uniqueness. the cognitive, motor, and neural foundations that distinguish human speech and language from other animal communication systems have been a central focus of research in the social and biological sciences for more than 200 years[1,2]. Subsequent functional assessments of the human-specific changes to FOXP2 using mice engineered to express the human variant of the gene revealed changes in synaptic plasticity, axon and dendrite outgrowth, and physiological activity in medium spiny neurons of the striatum, supporting the idea that the human variant of FOXP2 causes alteration in brain development[36,39] To date, it remains unclear when in the past these amino acid substitutions first occurred, as modern humans share them with both Neanderthals and Denisovans, indicating they originated at least ~400,000 years ago[40]. Recent findings suggest that other regulatory changes in the gene unique to modern humans lie at the base of the selection signal[40], and experimental evidence shows that the human FOXP2 variant differentially regulates downstream targets compared to the ancestral version found in chimpanzees[41]

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