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

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.

Transposable elements resistant to epigenetic resetting in the human germline are epigenetic hotspots for development and disease

“…4b). One notable example is provided by FOXP2 49 , which has facilitated language development during human evolution 49,50 . Accordingly, these data further demonstrate that hPGC-methylated regions are strongly enriched within enhancers and gene-networks that are primarily active during corticogenesis, and importantly with those that show differential expression within the developing cortex.…”

Understanding Language Evolution: Beyond Pan‐Centrism

“…New evidence includes and is not limited to, for example, the capacity for vocal invention, vocal learning, production of consonant‐ and vowel‐like calls, learned vocal production at speech‐like rhythm, complex (non‐Markovian) vocal sequences, call traditions and cultures, vocal tools and manipulations for the generation of rare acoustic phenomena, intentional vocalizations, deceptive vocal responses, and time–space vocal displacement . Findings for advanced vocal skills in great apes are supported by convergent inter‐disciplinary lines of evidence, from great ape genomics to great ape neurology and neurophysiology, indicating that “the inter‐mediate vocal phenotype of non‐human great apes (between Old‐World monkeys and humans) suggests that selection for increased vocal–motor control had already begun at the time of the last common ancestor of the great ape lineage.”…”

“…It is not a measure of the genetic similitude between genome sections that have known implications for the development of behavioral and/or cognitive mechanisms, including those underpinning language. Analyses of hominid genome regions known to encode structures and functions involved in communicative behavior and cognition, such as the FOXP2 great ape orthologs, for example, render a much subtler picture than that sketched by overall genetic relatedness or bare cladistics. Humans with altered versions of the FOXP2 gene show, besides severe speech and language impartment, changes in the structure and activation of the cortex, basal ganglia, and cerebellum .…”

“…However, other types of genetic alterations within FOXP2 that occur across all great apes indicate that any single‐species model is unsuitable. For example, it is now established that microsatellite variation and nonsynonymous polymorphisms occur across orangutans, gorillas, and chimpanzees in non‐negligible frequencies . Such variation only partially overlaps between great apes and could tie back to cases of voluntary breathing control and variation in vocal repertoire composition in gorillas or described events of vocal learning, intentional vocal signaling, and concurrent activations and architectural changes in Broca's homolog brain region in chimpanzees .…”

No Evidence for Recent Selection at FOXP2 among Diverse Human Populations

“…FOXP2 has been shown in vitro and in vivo to affect brain development and neural plasticity in humans and mice (Chiu et al, 2014; Enard et al, 2009; Reimers-Kipping et al, 2011; Španiel et al, 2011), and its altered expression affects brain function in language-related cortical areas (Fujita-Jimbo and Momoi, 2014; Konopka et al, 2009; Pinel et al, 2012; Spiteri et al, 2007). Intriguingly, it has also been shown to affect language-like behaviors in other animals, including in birdsong and juvenile mouse vocalizations (Chabout et al, 2016; Haesler et al, 2004; Shu et al, 2005; Teramitsu et al, 2010) as well as other primates (Staes et al, 2017). To date, FOXP2 is the only known autosomal-dominant language-related gene.…”