Vocal learning-associated convergent evolution in mammalian proteins and regulatory elements

Wirthlin, Morgan; Schmid, Tobias A.; Elie, Julie E.; Zhang, Xiaomeng; Shvareva, Varvara A.; Rakuljic, Ashley; Ji, Maria B.; Bhat, Ninad; Kaplow, Irene M.; Schäffer, Daniel E.; Lawler, Alyssa J.; Annaldasula, Siddharth; Lim, Byung Kook; Azim, Eiman; Meyer, Wynn K.; Yartsev, Michael M.; Pfenning, Andreas R.

doi:10.1101/2022.12.17.520895

Cited by 7 publications

(13 citation statements)

References 126 publications

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“…The dashed lines show phylolm lines of best fit for each clade as a visual aid. (C) We also applied TACIT to associate motor cortex open chromatin with vocal learning, a binary trait, and here we show results for the Egyptian fruit bat open chromatin region PVIL01002568.1:139004-139596 in the GALC locus (permulations p FDR =0.0376), which was also associated with open chromatin specifically active in the orofacial motor cortex of bat 97 and which has previously been associated with severe speech and motor disabilities in humans 99 .…”

Section: Main Textmentioning

confidence: 61%

“…Zoonomia realizes that vision. In combination with existing resources such as ENCODE 38 and TOPMed 39 and new technologies including regulatory genomic assays 94, 97 , chromatin conformation capture 27, 51 , and massively parallel reporter assays 36 , Zoonomia’s alignments of hundreds of placental species address fundamental questions in mammalian evolution.…”

Section: Discussionmentioning

confidence: 99%

“…For vocal learning, we tested for both regulatory and coding changes using TACIT and RERconverge (detailed in 97 ). Vocal learning is the ability to mimic non-innate sounds, and it likely evolved convergently in humans, bats, cetaceans, and pinnipeds 98 .…”

Section: Main Textmentioning

confidence: 99%

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Evolutionary constraint and innovation across hundreds of placental mammals

Christmas¹,

Kaplow²,

Genereux³

et al. 2023

Preprint

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Evolutionary constraint and acceleration are powerful, cell-type agnostic measures of functional importance. Previous studies in mammals were limited by species number and reliance on human-referenced alignments. We explore the evolution of placental mammals, including humans, through reference-free whole-genome alignment of 240 species and protein-coding alignments for 428 species. We estimate 10.7% of the human genome is evolutionarily constrained. We resolve constraint to single nucleotides, pinpointing functional positions, and refine and expand by over seven-fold the catalog of ultraconserved elements. Overall, 48.5% of constrained bases are as yet unannotated, suggesting yet-to-be-discovered functional importance. Using species-level phenotypes and an updated phylogeny, we associate coding and regulatory variation with olfaction and hibernation. Focusing on biodiversity conservation, we identify genomic metrics that predict species at risk of extinction.

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Section: Main Textmentioning

confidence: 61%

Section: Discussionmentioning

confidence: 99%

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Evolutionary constraint and innovation across hundreds of placental mammals

Christmas¹,

Kaplow²,

Genereux³

et al. 2023

Preprint

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“…Stimulation of the vLMC 10,11 or dLMC 12 results in laryngeal contractions. Bats, which represent another clade of vocal learning mammals, have recently been shown to also possess these direct projections from M1 13,14 . Songbirds have analogous direct projections from the robust nucleus of the arcopallium (RA) to syringeal motor neurons in nucleus XII in the brainstem ( Figure 1B ) 15,16 .…”

Section: Introductionmentioning

confidence: 99%

A Functional and Non-Homuncular Representation of the Larynx in the Primary Motor Cortex of Mice, a Vocal Non-Learner

Vargas,

Agravat,

Waidmann

et al. 2024

Preprint

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Vocalization is a complex behavior ranging from fully innate to advanced vocal learning. Vocal learning species possess a vocal primary motor cortex (M1) region that makes direct projections to brainstem vocal motor neurons, which are thought to facilitate learning and fine modulation of vocalizations. Surprisingly, a similar, albeit sparse, direct projection from M1 was found in mice. Mice produce ultrasonic vocalizations (USV) which appear to be mostly innate. Modulation of these USVs is impacted by lesions to this M1 region, but genetic ablation of the cortex leads to few, if any, changes to USVs. It remained unclear whether M1 has any control over the vocal organ in a vocal non-learning species. In the current study, we found that stimulation in different parts of M1 in mice can generate contractions in laryngeal and jaw muscles, with different latencies suggestive of both direct and indirect projections to brainstem vocal motor neurons. Viral tracing reveals both single- and double-labeled populations of cortical neurons that simultaneously innervate laryngeal, jaw, and forelimb motor circuits. Chemical lesions reveal that an anterolateral orofacial region of M1 regulates the number of syllables in vocal sequences. Our results provide evidence that M1 in a vocal non-learner has some influence on vocal musculature, consistent with the continuum hypothesis of vocal learning. They also reveal that the representations of muscles for different behaviors across mouse M1 are more intermixed than previously considered. We discuss how these results impact hypotheses on the evolution of cortical vocal control and motor cortex organization.

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“…Previous conclusions on vocal learning abilities are weakened by the lack of reliable identification of vocalizing individuals 9–11 . Combined, these gaps limit thorough exploration of the neural mechanisms of vocal production learning in this species, although cutting-edge technologies for measuring brain activity are readily available 12–15…”

Section: Introductionmentioning

confidence: 99%

Role of auditory feedback for vocal production learning in the Egyptian fruit-bat

Elie,

Muroy,

Genzel

et al. 2023

Preprint

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SummarySome species have evolved the ability to use the sense of hearing to modify existing vocalizations, or even create new ones. This ability corresponds to various forms of vocal production learning that are all possessed by humans, and independently displayed by distantly related vertebrates. Among mammals, a few species, including the Egyptian fruit-bat, would possess such vocal production learning abilities. Yet the necessity of an intact auditory system for the development of the Egyptian fruit-bat typical vocal repertoire has not been tested. Furthermore, a systematic causal examination of learned and innate aspects of the entire repertoire has never been performed in any vocal learner. Here we addressed these gaps by eliminating pups’ sense of hearing at birth and assessing its effects on vocal production in adulthood. The deafening treatment enabled us to both causally test these bats vocal learning ability and discern learned from innate aspects of their vocalizations. Leveraging wireless individual audio recordings from freely interacting adults, we show that a subset of the Egyptian fruit-bat vocal repertoire necessitates auditory feedback. Intriguingly, these affected vocalizations belong to different acoustic groups in the vocal repertoire of males and females. These findings open the possibilities for targeted studies of the mammalian neural circuits that enable sexually dimorphic forms of vocal learning.

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Vocal learning-associated convergent evolution in mammalian proteins and regulatory elements

Cited by 7 publications

References 126 publications

Evolutionary constraint and innovation across hundreds of placental mammals

Evolutionary constraint and innovation across hundreds of placental mammals

A Functional and Non-Homuncular Representation of the Larynx in the Primary Motor Cortex of Mice, a Vocal Non-Learner

Role of auditory feedback for vocal production learning in the Egyptian fruit-bat

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