Parallel and Convergent Evolution of the Dim-Light Vision Gene RH1 in Bats (Order: Chiroptera)

Yong-Yi Shen,Ya-Ping Zhang,David M. Irwin,Jie Liu,Konrad Scheffler

doi:10.1371/journal.pone.0008838

Abstract

Rhodopsin, encoded by the gene Rhodopsin (RH1), is extremely sensitive to light, and is responsible for dim-light vision. Bats are nocturnal mammals that inhabit poor light environments. Megabats (Old-World fruit bats) generally have well-developed eyes, while microbats (insectivorous bats) have developed echolocation and in general their eyes were degraded, however, dramatic differences in the eyes, and their reliance on vision, exist in this group. In this study, we examined the rod opsin gene (RH1), and compared its evolution to that of two cone opsin genes (SWS1 and M/LWS). While phylogenetic reconstruction with the cone opsin genes SWS1 and M/LWS generated a species tree in accord with expectations, the RH1 gene tree united Pteropodidae (Old-World fruit bats) and Yangochiroptera, with very high bootstrap values, suggesting the possibility of convergent evolution. The hypothesis of convergent evolution was further supported when nonsynonymous sites or amino acid sequences were used to construct phylogenies. Reconstructed RH1 sequences at internal nodes of the bat species phylogeny showed that: (1) Old-World fruit bats share an amino acid change (S270G) with the tomb bat; (2) Miniopterus share two amino acid changes (V104I, M183L) with Rhinolophoidea; (3) the amino acid replacement I123V occurred independently on four branches, and the replacements L99M, L266V and I286V occurred each on two branches. The multiple parallel amino acid replacements that occurred in the evolution of bat RH1 suggest the possibility of multiple convergences of their ecological specialization (i.e., various photic environments) during adaptation for the nocturnal lifestyle, and suggest that further attention is needed on the study of the ecology and behavior of bats.

Highlights

Vision plays an extraordinary role in animals and is often basic for their survival
The aligned bat RH1 nucleotide sequence was 834bp in length, of which 147 were variable, but only 24 of these sites cause amino acid sequence variation (Figure 1)
For the two color vision genes, the M/LWS gene was successfully amplified for all bat species (Figure S1), while the SWS1 gene failed to amplify in all Rhinolophoidea and Rousettus species, implying the loss of function of short wavelength opsin in this species, in agreement with a recent study [20]

Summary

Introduction

Vision plays an extraordinary role in animals and is often basic for their survival. Due to the high degree of variation in light conditions and presence of various wavelengths of light in different environments, the evolution of vision to various photic environments and lifestyles is among the most significant mammalian adaptations [1]. To examine adaption to a dim-light environment and differences on the reliance on sight, we amplified and sequenced the dim-light vision gene (RH1), and two color vision genes (SWS1 and M/LWS) from the total RNA from retina samples from 23 species of bats, to provide a more complete perspective on the evolution of vision in bats.

Results

Conclusion