As Blind as a Bat? Opsin Phylogenetics Illuminates the Evolution of Color Vision in Bats

Abstract

Through their unique use of sophisticated laryngeal echolocation bats are considered sensory specialists amongst mammals and represent an excellent model in which to explore sensory perception. Although several studies have shown that the evolution of vision is linked to ecological niche adaptation in other mammalian lineages, this has not yet been fully explored in bats. Recent molecular analysis of the opsin genes, which encode the photosensitive pigments underpinning color vision, have implicated high-duty cycle (HDC) echolocation and the adoption of cave roosting habits in the degeneration of color vision in bats. However, insufficient sampling of relevant taxa has hindered definitive testing of these hypotheses. To address this, novel sequence data was generated for the SWS1 and MWS/LWS opsin genes and combined with existing data to comprehensively sample species representing diverse echolocation types and niches (SWS1 n = 115; MWS/LWS n = 45). A combination of phylogenetic analysis, ancestral state reconstruction, and selective pressure analyses were used to reconstruct the evolution of these visual pigments in bats and revealed that although both genes are evolving under purifying selection in bats, MWS/LWS is highly conserved but SWS1 is highly variable. Spectral tuning analyses revealed that MWS/LWS opsin is tuned to a long wavelength, 555–560 nm in the bat ancestor and the majority of extant taxa. The presence of UV vision in bats is supported by our spectral tuning analysis, but phylogenetic analyses demonstrated that the SWS1 opsin gene has undergone pseudogenization in several lineages. We do not find support for a link between the evolution of HDC echolocation and the pseudogenization of the SWS1 gene in bats, instead we show the SWS1 opsin is functional in the HDC echolocator, Pteronotus parnellii. Pseudogenization of the SWS1 is correlated with cave roosting habits in the majority of pteropodid species. Together these results demonstrate that the loss of UV vision in bats is more widespread than was previously considered and further elucidate the role of ecological niche specialization in the evolution of vision in bats.

Multifactorial processes underlie parallel opsin loss in neotropical bats

“…Therefore, several lines of evidence support loss of function of OPN1SW in these taxa. For C. micropus , our inferred intact ORF is based on PCR of ~100 codons (also seen in B. pumila ) and was supported by sequence data from two closely related species from the Natalidae (Emerling et al, 2015; Simões et al, 2018).…”

“…Although such patterns could also arise from methodological issues, some of our findings appear consistent with emerging trends. For example, within Pteronotus and the Mormoopidae family as a whole, there is increasing evidence to support an extremely complex evolutionary history of S-opsins (Gutierrez et al, 2018; Simões et al, 2018; Wu et al, 2018). In comparison, methodological artifacts are less easy to rule out as causes of variation among Carollia spp.…”

Making a bat: The developmental basis of bat evolution

“…However, research over the past 15 years has begun to highlight the importance of adaptations in other sensory structures to the evolutionary success of bats ( Davies et al , 2013 ), including variation in the sizes of the cochlea ( Davies et al , 2013 ), eyes ( Heffner and Heffner, 1992 ; Eklöf, 2003 ), olfactory epithelium and olfactory bulb, as well as in the vomeronasal epithelium and accessory olfactory bulb ( Bhatnagar and Smith, 2007 ; Smith et al , 2012 ; Yohe et al , 2017 ; Yohe and Brand, 2018 ). Of particular note, studies of the evolution of bat vision in the last two years have provided unprecedented insights into the role of sensory adaptations in bat evolution ( Gutierrez et al , 2018b ; Kries et al , 2018 ; Wu et al , 2018 ; Li et al , 2018 ; Simoes et al , 2019 ; Sadier et al 2018 ). Because of this, we further discuss the evolution of the visual systems of bats.…”

Foraging shifts and visual preadaptation in ecologically diverse bats

“…(commonly known as big‐eyed bats) (Eklöf, 2003; Thiagavel et al., 2018). Despite this, molecular ecology studies of noctilionoid vision have thus far been limited to visual opsins ( OPN1SW , OPN1LW and RHO ), and traced adaptations therein to changes in roosting habits, echolocation and diets (Kries et al., 2018; Li et al., 2018; Sadier et al., 2018; Simões et al., 2019; Wu, Jiao, Simmons, Lu, & Zhao, 2018). 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).…”