Abstract
FOXP2 is a transcription factor implicated in the development and neural control of orofacial coordination, particularly with respect to vocalisation. Observations that orthologues show almost no variation across vertebrates yet differ by two amino acids between humans and chimpanzees have led to speculation that recent evolutionary changes might relate to the emergence of language. Echolocating bats face especially challenging sensorimotor demands, using vocal signals for orientation and often for prey capture. To determine whether mutations in the FoxP2 gene could be associated with echolocation, we sequenced FoxP2 from echolocating and non-echolocating bats as well as a range of other mammal species. We found that contrary to previous reports, FoxP2 is not highly conserved across all nonhuman mammals but is extremely diverse in echolocating bats. We detected divergent selection (a change in selective pressure) at FoxP2 between bats with contrasting sonar systems, suggesting the intriguing possibility of a role for FoxP2 in the evolution and development of echolocation. We speculate that observed accelerated evolution of FoxP2 in bats supports a previously proposed function in sensorimotor coordination.
Highlights
The role of the forkhead transcription factor FOXP2 in communication was first suggested following the discovery that mutations at this locus cause impaired speech-related motor coordination and comprehension [1,2]
After combining with archived sequences, including those obtained from genomic bacterial artificial chromosome (BAC) libraries, our analyses of complete FoxP2 gene sequences were based on 13 bats, 22 additional eutherian mammals, 1 non-eutherian mammal, two birds and one reptile
The FOXP2/FoxP2 gene has been of tremendous interest in recent years, with sequence variation and patterns of expression linked to human speech defects [1,41,42], the evolution of language [5], vocal learning in animals [4,9,43], and sensorimotor performance more generally [7,11,44]
Summary
The role of the forkhead transcription factor FOXP2 in communication was first suggested following the discovery that mutations at this locus cause impaired speech-related motor coordination (orofacial dyspraxia) and comprehension (dysphasia) [1,2]. Echolocating bats face especially challenging sensorimotor demands, using vocal signals for orientation and prey capture. They can emit echolocation pulses at rates of up to 200 sounds per second, interpret the resulting echoes within time-windows as short as several milliseconds and make motor responses such as changes in flight manoeuvres during these short time intervals [12]. The reception of ultrasonic pulses for orientation, obstacle avoidance and prey capture in flight require complex aural and either orofacial or, in some species, nasofacial coordination [13,14,15]. Bat echolocation signals show great diversity, contain complex tonal information, and can be modified in response to echo feedback from targets [13,14]. Pulse-echo delay-tuned neurons encoding target distance are present in the cortex and thalamus (medial geniculate body) [22,23,24]
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