Divergence of dim-light vision among bats (order: Chiroptera) as estimated by molecular and electrophysiological methods.

He-Qun Liu,Fu-Qiang Xu,Li Zhong,Xin-Tian Hu,Joshua D Rizak,Rui-Qi Wu,Yong-Yi Shen,Ming-Shan Wang,Bo Li,Jing-Kuan Wei,Ya-Ping Zhang,Lu Wang

doi:10.1038/srep11531

Abstract

Dim-light vision is present in all bats, but is divergent among species. Old-World fruit bats (Pteropodidae) have fully developed eyes; the eyes of insectivorous bats are generally degraded, and these bats rely on well-developed echolocation. An exception is the Emballonuridae, which are capable of laryngeal echolocation but prefer to use vision for navigation and have normal eyes. In this study, integrated methods, comprising manganese-enhanced magnetic resonance imaging (MEMRI), f-VEP and RNA-seq, were utilized to verify the divergence. The results of MEMRI showed that Pteropodidae bats have a much larger superior colliculus (SC)/ inferior colliculus (IC) volume ratio (3:1) than insectivorous bats (1:7). Furthermore, the absolute visual thresholds (log cd/m2•s) of Pteropodidae (−6.30 and −6.37) and Emballonuridae (−3.71) bats were lower than those of other insectivorous bats (−1.90). Finally, genes related to the visual pathway showed signs of positive selection, convergent evolution, upregulation and similar gene expression patterns in Pteropodidae and Emballonuridae bats. Different results imply that Pteropodidae and Emballonuridae bats have more developed vision than the insectivorous bats and suggest that further research on bat behavior is warranted.

Highlights

Visual processing in the visual system is believed to occur in two steps: first, optic signals are transduced from the environment into neuronal signals in the retina via cis/trans retinal isomerization, cGMP-gated signaling, synaptic transmission, and action potentials[1,2,3,4,5]; the neuronal signals are transformed and integrated into the visual pathway and eventually rebuilt into a pattern in the brain[6]
At the optic chiasm, most axons crossed to the contralateral side, where the projections continued to the lateral geniculate nucleus and superior colliculus (SC)
We identified 914 genes showing higher expression in Pteropodidae bats and T. melanopogon than H. armiger and M. laniger, but no significant differences in expression were observed between the Pteropodidae bats and T. melanopogon

Summary

Introduction

Visual processing in the visual system is believed to occur in two steps: first, optic signals are transduced from the environment into neuronal signals in the retina via cis/trans retinal isomerization, cGMP-gated signaling, synaptic transmission, and action potentials[1,2,3,4,5]; the neuronal signals are transformed and integrated into the visual pathway and eventually rebuilt into a pattern in the brain[6]. Reliability in dim light, including improving the capture of photons in the retina[9,10], like Gekko gecko, that has pure-rod retinas[8] Such adaptive changes in the retina suggested that these animals might have specific structures through the visual pathway to process differential visual information[11], little previous experimental research has verified this model. We hypothesized that certain anatomical structures associated with the visual pathway, visual capacity, and genes participating in the visual pathway have diverged within Chiroptera To test this hypothesis, the present study used MEMRI (manganese-enhanced magnetic resonance imaging), which produces images with high spatial resolution for understanding anatomy and has been applied to detect neuronal activity in vivo and explore neuronal structures[26,27], to measure the brain anatomy of selected species of bats. Our study used a combination of imaging, electrophysiology, and RNA-seq methods to elaborate on the visual divergence in bats and showed that Pteropodidae and Emballonuridae rely more on vision than insectivorous bats, suggesting that the behavior of bats requires additional attention

Methods

Results

Conclusion