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

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.

Selective Gene Loss of Visual and Olfactory Guanylyl Cyclase Genes Following the Two Rounds of Vertebrate-Specific Whole-Genome Duplications

“…Most microbats are insectivores hunting during night hours. Consequently, eyes of microbats are commonly rudimentary, serving merely to detect changes in illumination ( Rydell and Eklöf 2003 ; Liu et al. 2015 ).…”

Foraging shifts and visual preadaptation in ecologically diverse bats

“…Additional analyses correlated foraging modes (e.g., aerial vs. gleaning insectivory) and visual evolution by contrasting selection intensity between two sets of species with divergent foraging ecologies, but were again restricted to the opsins (Gutierrez, Schott, et al, 2018). However, the visual photopigments represent only a minute fraction of the genes expressed in the eye, including those that convert light into electrical signals via the phototransduction pathway and structural proteins involved in the refraction of light (Liu et al., 2015; Mustafi et al., 2016; Wistow et al., 2008). Therefore, much remains to be learnt concerning how the visual systems of noctilionoid bats have adapted in response to changes in both foraging and diet throughout their evolution.…”

“…aerial insectivory, Chiroptera, diet, gleaning, molecular adaptation, vision represent only a minute fraction of the genes expressed in the eye, including those that convert light into electrical signals via the phototransduction pathway and structural proteins involved in the refraction of light (Liu et al, 2015;Mustafi et al, 2016;Wistow et al, 2008). Therefore, much remains to be learnt concerning how the visual systems of noctilionoid bats have adapted in response to changes in both foraging and diet throughout their evolution.…”

Blindness in echolocating bats

“…Contrary to the popular belief, bats are not blind. Indeed, the vision in flying mammals plays an important role in light detection, long-range orientation and environmental recognition (Eklöf 2003, Geva-Sagiv et al 2015, Liu et al 2015, as well as in enabling leader-follower behaviors in groups of conspecifics (Kong et al 2016). In echolocating bats, functional vision works complementary to their sonar system (Eklöf 2003, Denzinger andSchnitzler 2013), and some species [e.g.…”