Parallel and convergent evolution of the dim-light vision gene RH1 in bats (Order: Chiroptera)

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.

Figure 1. Divergent amino acid sites in the RH1 gene sequences of bats.

Figure 2. The phylogenetic topology of the RH1 gene based on nucleotide sequences.

Numbers above the branches are the ML bootstrap values, while those under the branches are the Bayesian posterior probabilities.

Figure 3. NJ tree based on synonymous sites of RH1 gene.

Numbers above the branches are the NJ bootstrap values.

Figure 4. NJ tree based on amino acid sequences and nonsynonymous sites of RH1 gene.

The numbers above the branches are NJ bootstrap values of amino acid sequences, while the numbers under the branches are the values from the nonsynonymous sites.

Figure 5. Species tree based on the previous study of Teeling et al. 2005.

The numbers and symbols above the branches are the positions and amino acid replacements. The numbers in brackets below the branches are the numbers of nonsynonymous and synonymous substitutions. The sequences of the internal nodes and Ka/Ks were reconstructed by Maximum Likelihood method in PAML.

Figure 6. The secondary structure of the rhodopsin based on the bovine model with the 24 amino acid replacements among bats identified.

Each circle represents one amino acid residue. The numbers around the circles are the positions of the amino acid replacements.

Figure 7. NJ trees based on nucleotide sequences of aligned RH1 gene, but excluding sites that evolve in parallel.

(A) excluding the sites corresponding to amino acid site 270; (B) excluding the sites corresponding to amino acid site 104; (C) excluding the sites corresponding to amino acid site 183; (D) excluding the sites corresponding to amino acid sites 104 and 183; (E) excluding the sites corresponding to amino acid sites 104, 183, and 270; (F) excluding the sites corresponding to amino acid sites 157 and 173.