Embryonic evidence uncovers convergent origins of laryngeal echolocation in bats

Nojiri, Taro; Wilson, L. T.; López‐Aguirre, Camilo; Tú, Vương Tân; Kuratani, Shigeru; Ito, Kai; Higashiyama, Hiroki; Sơn, Nguyễn Trường; Fukui, Dai; Sadier, Alexa; Sears, Karen E.; Endo, Hideki; Kamihori, Satoshi; Koyabu, Daisuke

doi:10.1016/j.cub.2020.12.043

Cited by 37 publications

(42 citation statements)

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“…However, such a loss of hippocampal theta should be predicted from the sensory world of an echolocating bat [171,176]. Laryngeal echolocation (vocal emission) has evolved multiple times, in both suborders of bats [177]. Lingual echolocation (tongue clicking) has only evolved in one genus in one family, the genus Rousettus in the family Pteropodidae (fruit bats) [172].…”

Section: (C) the Hippocampus In Extreme Environmentsmentioning

confidence: 99%

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How the evolution of air breathing shaped hippocampal function

Jacobs

2021

Phil. Trans. R. Soc. B

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To make maps from airborne odours requires dynamic respiratory patterns. I propose that this constraint explains the modulation of memory by nasal respiration in mammals, including murine rodents (e.g. laboratory mouse, laboratory rat) and humans. My prior theories of limbic system evolution offer a framework to understand why this occurs. The answer begins with the evolution of nasal respiration in Devonian lobe-finned fishes. This evolutionary innovation led to adaptive radiations in chemosensory systems, including the emergence of the vomeronasal system and a specialization of the main olfactory system for spatial orientation. As mammals continued to radiate into environments hostile to spatial olfaction (air, water), there was a loss of hippocampal structure and function in lineages that evolved sensory modalities adapted to these new environments. Hence the independent evolution of echolocation in bats and toothed whales was accompanied by a loss of hippocampal structure (whales) and an absence of hippocampal theta oscillations during navigation (bats). In conclusion, models of hippocampal function that are divorced from considerations of ecology and evolution fall short of explaining hippocampal diversity across mammals and even hippocampal function in humans. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

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Section: (C) the Hippocampus In Extreme Environmentsmentioning

confidence: 99%

“…This rules out the use of the MOS to track odours dissolved in water in these groups. Instead, one suborder, the toothed whales, have evolved echolocation, in a striking evolutionary convergence with bats, even to the point of convergent genetic mechanisms [177,189,190].…”

Section: (C) the Hippocampus In Extreme Environmentsmentioning

confidence: 99%

How the evolution of air breathing shaped hippocampal function

Jacobs

2021

Phil. Trans. R. Soc. B

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Section: Discussionmentioning

confidence: 99%

“…[11,47,60,61]). Indeed, prenatal work demonstrated that Rousettus pup cochlear growth rate occurs predominantly in utero but slows greatly postnatally compared to laryngeal bats [62], and that the developmental trajectory of ear features in lingual bats was more similar to non-echolocating mammals than to laryngeal bats [63]. Kössl et al [59] found that certain neuronal circuits for echolocation ranging in the auditory cortex were already functional prior to the onset of echolocation in laryngeal pups.…”

Section: Discussionmentioning

confidence: 99%

Hearing, echolocation, and beam steering from day 0 in tongue-clicking bats

2021

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Little is known about the ontogeny of lingual echolocation. We examined the echolocation development of Rousettus aegyptiacus , the Egyptian fruit bat, which uses rapid tongue movements to produce hyper-short clicks and steer the beam's direction. We recorded from day 0 to day 35 postbirth and assessed hearing and beam-steering abilities. On day 0, R. aegyptiacus pups emit isolation calls and hyper-short clicks in response to acoustic stimuli, demonstrating hearing. Auditory brainstem response recordings show that pups are sensitive to pure tones of the main hearing range of adult Rousettus and to brief clicks. Newborn pups produced clicks in the adult paired pattern and were able to use their tongues to steer the sonar beam. As they aged, pups produced click pairs faster, converging with adult intervals by age of first flights (7–8 weeks). In contrast with laryngeal bats, Rousettus echolocation frequency and duration are stable through to day 35, but shift by the time pups begin to fly, possibly owing to tongue-diet maturation effects. Furthermore, frequency and duration shift in the opposite direction of mammalian laryngeal vocalizations. Rousettus lingual echolocation thus appears to be a highly functional sensory system from birth and follows a different ontogeny from that of laryngeal bats.

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“…Although echolocation occurred in several mammalian lineages ( He et al., 2021 ), its origin and elaboration have been widely studied only in bats and whales ( Jones, 2005 , 2010 ; Jones and Teeling, 2006 ). In contrast to a single origin of echolocation in the last common ancestor (LCA) of toothed whales supported by fossil records, molecular evolution, and gene functional experiments ( Churchill et al., 2016 ; Geisler et al., 2014 ; Liu et al., 2018 ; Park et al., 2016 ), the evolutionary origin(s) of laryngeal echolocation in bats remain contentious ( Jones and Teeling, 2006 ; Nojiri et al., 2021 ; Wang et al., 2017 ).…”

Section: Introductionmentioning

confidence: 98%