Testing Convergent Evolution in Auditory Processing Genes between Echolocating Mammals and the Aye-Aye, a Percussive-Foraging Primate

Abstract

Several taxonomically distinct mammalian groups—certain microbats and cetaceans (e.g., dolphins)—share both morphological adaptations related to echolocation behavior and strong signatures of convergent evolution at the amino acid level across seven genes related to auditory processing. Aye-ayes (Daubentonia madagascariensis) are nocturnal lemurs with a specialized auditory processing system. Aye-ayes tap rapidly along the surfaces of trees, listening to reverberations to identify the mines of wood-boring insect larvae; this behavior has been hypothesized to functionally mimic echolocation. Here we investigated whether there are signals of convergence in auditory processing genes between aye-ayes and known mammalian echolocators. We developed a computational pipeline (Basic Exon Assembly Tool) that produces consensus sequences for regions of interest from shotgun genomic sequencing data for nonmodel organisms without requiring de novo genome assembly. We reconstructed complete coding region sequences for the seven convergent echolocating bat–dolphin genes for aye-ayes and another lemur. We compared sequences from these two lemurs in a phylogenetic framework with those of bat and dolphin echolocators and appropriate nonecholocating outgroups. Our analysis reaffirms the existence of amino acid convergence at these loci among echolocating bats and dolphins; some methods also detected signals of convergence between echolocating bats and both mice and elephants. However, we observed no significant signal of amino acid convergence between aye-ayes and echolocating bats and dolphins, suggesting that aye-aye tap-foraging auditory adaptations represent distinct evolutionary innovations. These results are also consistent with a developing consensus that convergent behavioral ecology does not reliably predict convergent molecular evolution.

The sensory ecology of primate food perception, revisited

“…Since then, at least 70 genes have been identified in humans as underlying the auditory sense, 20 but unfortunately, comparative study of the genetic basis of audition in nonhuman primates and other mammals remains almost nonexistent. A rare exception is recent work by Bankoff et al, 21 who compared seven genes involved in auditory processing across echolocating mammals (bats, cetaceans) and primates to study the molecular evolution of specialized hearing in aye‐ayes ( Daubentonia madagascariensis ). Aye‐ayes use a derived percussive foraging technique that utilizes hearing to locate hollow cavities caused by wood‐boring invertebrates, 21,22 and exhibit enhanced sensitivity to high frequencies relative to other strepsirrhines 18 .…”

“…A rare exception is recent work by Bankoff et al, 21 who compared seven genes involved in auditory processing across echolocating mammals (bats, cetaceans) and primates to study the molecular evolution of specialized hearing in aye‐ayes ( Daubentonia madagascariensis ). Aye‐ayes use a derived percussive foraging technique that utilizes hearing to locate hollow cavities caused by wood‐boring invertebrates, 21,22 and exhibit enhanced sensitivity to high frequencies relative to other strepsirrhines 18 . However, they found no evidence of convergent evolution between echolocating mammals and aye‐ayes.…”

“…Aye-ayes use a derived percussive foraging technique that utilizes hearing to locate hollow cavities caused by wood-boring invertebrates, 21,22 and exhibit enhanced sensitivity to high frequencies relative to other strepsirrhines. 18 However, they found no evidence of convergent evolution between echolocating mammals and aye-ayes.…”

The evolutionary tuning of hearing

“…Moreover, positive selection in inner-ear-expressed genes has also been reported within mammalian branches [38][39][40][41][42][43][44]. In addition, instances of parallel and/or convergent evolution between echolocating bats and whales have been identified in hearing-related genes [38,40,[45][46][47][48][49][50][51], potentially reflecting distinct environmental demands. Thus, the coding sequences of inner ear genes can be proposed as hotspots for evolutionary innovation in mammals.…”

Interpreting the Evolutionary Echoes of a Protein Complex Essential for Inner-Ear Mechanosensation

“…The ability to detect sound waves in air and with increased sensitivities would have imposed a significant evolutionary advantage on these early tetrapods, leading to a relatively rapid radiation in inner ear morphology and adaptation (Clack 2002;Coffin et al 2004;Manley and Clack 2004). In addition to modifications made to morphological features of the middle and inner ear throughout vertebrate evolution, the molecular machinery underlying this process presumably underwent a similarly extensive series of atomic level modifications (Bankoff et al 2017;Trigila et al 2021). However, the aversion to fossilization exhibited by biological macromolecules coupled with a relative lack of structural and biochemical information of non-mammalian molecules involved in sound detection leaves many questions regarding the molecular evolution of this highly conserved process unanswered.…”