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Ecological and genetic properties in high auditory capabilities in mammals and birds

Lida Sanchez Sanchez 東北大学

2020.09.25

概要

Acoustic communication consists of both transmission and perception of sound information. This system plays significant roles in multiple animal behavioral contexts, such as mating, foraging, and avoiding predators. A plethora of literature had reported the features and functions of animal communication calls, as well as the hearing ranges for a wide variety of groups. For some small mammals, such as shrews, acoustic communication has been described as a way of guidance through the environment, termed as echo-based orientation (Siemers et al., 2009). This has been a topic under conflict for several decades, and no studies had presented experiments to describe how animals might extract environmental information from their vocalizations. I evaluated this hypothesis using shrew’s vocalizations under various experimental conditions (Chapter 1). Audible-to-ultrasonic click, noisy and different types of tonal calls were recorded under all experimental conditions. While exploring and facing the obstacles, shrews increased their calling rate, and adjusted some features of their calls among the experimental conditions (Sanchez et al., 2019).

Among acoustic communication, other captivating query is how some species have acquired their enhanced auditory capabilities, i.e., greater proficiencies to analyze acoustic information in the environment, and how these are essential to decode environmental information. Some vertebrates stand out for their enhanced hearing sensitivities, such as the cat and the barn owl (Manley, 2001). These species fed on similar prey items, for which it may had represented a selective pressure over the hearing sensitivity on these species. Despite the published results addressing the hearing abilities in these two species, the molecular basis of the greater sensitivities. I sought for candidate genes shared byt the cat and the barn owl, possibly linked to their auditory abilities.

Candidate genes related to hearing abilities in mammals and birds

Materials and methods
Twelve and fourteen species were selected according to their reported hearing sensitivities, in mammals and birds respectively. The cat and the barn owl were qualified as high sensitive, and the rest as low sensitive hearing. A genome-wide analysis was conducted to detect positively selected genes in the cat and the barn owl, in comparison to other members of mammals and birds, respectively. To detect positive selection, the dN/dS ratios were calculated, using codeml (PAML) and aBSREL (HyPhy) packages, for the branches of interest, and compared with those species considered as low hearing sensitive.The analysis was conducted using gene trees and species trees as reference for both birds and mammals.

Results and Discussion
Seven genes were found to be positively selected in common in the overall analyses for the cat and the barn owl genome, and these were considered to be candidate genes associated with their enhanced hearing abilities. Two of these genes, CACNA1G and NOS1, have been reported to be linked with the modulation of acoustic information throughout the nervous system, and auditory recovery after noise exposure. Data showed that multiple amino acid substitutions were under selection in the protein sequences of these commonly detected genes, most of which were located in protein domains with recognized functions. When compared, these obtained amino acid changes in the NOS1, to their previous reported mutations, are located in nearby regions within the sequence, localized on its protein domains (Fig. 1). The functions of these domains have been well-described, with specific roles in the catalytic activity of this protein. Several studies reported mutations in these particular domains affecting the catalytic activity of the NOS1 (Hess et al., 1998; Panda, Ghosh and Stuehr, 2001; Shen et al., 2005). Despite not having experimental evidence of the effect of these amino acid substitutions found positively selected in the cat and barn owl, experiments in the future could be focused to test these effects and evaluate their implications over the hearing mechanisms in these two species.

Conclusively, I addressed two topics among acoustic communications, addressing questions for which behavioral and molecular data wasn’t tested till the date. The hypothesis of the use of acoustic information for the guidance among different environments in shrews was confirmed, and allegedly referred an involvement of the genes positively selected for the cat and the barn owl, in their hearing sensitivities

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参考文献

Hess, A. et al. (1998) ‘Nitric oxide synthase in the vestibulocochlear system of mice’, Brain Research, 813(1), pp. 97–102. doi: 10.1016/S0006-8993(98)00997-4.

Manley, G. A. (2001) ‘Evidence for an active process and a cochlear amplifier in nonmammals’, Journal of Neurophysiology, 86(2), pp. 541–549. doi: 10.1152/jn.2001.86.2.541.

Panda, K., Ghosh, S. and Stuehr, D. J. (2001) ‘Calmodulin Activates Intersubunit Electron Transfer in the Neuronal Nitric-oxide Synthase Dimer’, Journal of Biological Chemistry, 276(26), pp. 23349–23356. doi: 10.1074/jbc.M100687200.

Sanchez, L. et al. (2019) ‘Acoustic emissions of Sorex unguiculatus (Mammalia: Soricidae): Assessing the echo-based orientation hypothesis’, Ecology and Evolution, 9(5), pp. 2629–2639. doi: 10.1002/ece3.4930.

Shen, J. et al. (2005) ‘Involvement of the nitric oxide-cyclic GMP pathway and neuronal nitric oxide synthase in ATP-induced Ca2+ signalling in cochlear inner hair cells’, European Journal of Neuroscience, 21(11), pp. 2912–2922. doi: 10.1111/j.1460-9568.2005.04135.x.

Siemers, B. M. et al. (2009) ‘Why do shrews twitter? Communication or simple echo-based orientation.’, Biology letters, 5(5), pp. 593–6. doi: 10.1098/rsbl.2009.0378.

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