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

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.

脊椎动物视蛋白基因分子进化的研究进展

国家自然科学基金重点项目(30530120); 国家重点基础研究发展计划(2007CB411600)资助

Relaxed purifying selection of rhodopsin gene within a Chinese endemic cavefish genus Sinocyclocheilus (Pisces: Cypriniformes)

The cyprinid fish genus Sinocyclocheilus, as the most cavefish rich genus, includes many species showing striking adaptation to caves and convergent reduction or even loss of eyes and pigmentation. RH1 is responsible for dim vision. In order to explore the evolution of RH1 gene in this genus, we sequenced the complete gene from 28 individuals of 16 representative species of Sinocyclocheilus, with cave and surface species included. Phylogenetic analyses supported the monophyly of Sinocyclocheilus and polyphyly of the cave species. Codon models implemented in PAML were used to infer the evolution of RH1. We found that Sinocyclocheilus had a significantly higher evolutionary rate for amino acids than other cyprinid fishes compared, which might be the result of relaxation of purifying selection and could be ascribed to cave habit of this genus. In contrast to previous hypotheses, both cave and surface lineages exhibited a similar rate of molecular evolution, so the RH1 of cave species may still be functional, although these species were highly adapted to cave environment. Two amino acid substitutions (D83G and E122V) that were not reported before were found, which may be useful for site-directed mutagenesis in the future.

Different electronic structures and spectroscopic properties of cationic [M(ppy)2(N--N)]+ (M = Rh, Ir; N--N = Hcmbpy, H2dcbpy), a DFT study.

We report a comparative quantum-chemical study of the electronic structures and optical properties of a series of cationic complexes [M(ppy)(2)(N--N)](+) (N--N = Hcmbpy = 4-carboxy-4'-methylbpy, M = Rh (Rh1), Ir(Ir2); N--N = H(2)dcbpy = 4,4'-dicarboxy-bpy, M = Rh (Rh3) and Ir (Ir4)). The theoretical calculation reveals that the increased number of -COOH groups on the bpy ligand can decrease the energy levels of LUMO more than HOMO and narrow down the HOMO-LUMO energy gaps, which results in the red-shifted of the lowest-lying absorption and phosphorescent spectra. The lowest-lying singlet absorptions were categorized as d(M,M = Rh or Ir) + pi(ppy) -->pi*(bpy) with MLCT and LLCT characters.

Gene loss, adaptive evolution and the co-evolution of plumage coloration genes with opsins in birds.

BACKGROUND: The wide range of complex photic systems observed in birds exemplifies one of their key evolutionary adaptions, a well-developed visual system. However, genomic approaches have yet to be used to disentangle the evolutionary mechanisms that govern evolution of avian visual systems. RESULTS: We performed comparative genomic analyses across 48 avian genomes that span extant bird phylogenetic diversity to assess evolutionary changes in the 17 representatives of the opsin gene family and five plumage coloration genes. Our analyses suggest modern birds have maintained a repertoire of up to 15 opsins. Synteny analyses indicate that PARA and PARIE pineal opsins were lost, probably in conjunction with the degeneration of the parietal organ. Eleven of the 15 avian opsins evolved in a non-neutral pattern, confirming the adaptive importance of vision in birds. Visual conopsins sw1, sw2 and lw evolved under negative selection, while the dim-light RH1 photopigment diversified. The evolutionary patterns of sw1 and of violet/ultraviolet sensitivity in birds suggest that avian ancestors had violet-sensitive vision. Additionally, we demonstrate an adaptive association between the RH2 opsin and the MC1R plumage color gene, suggesting that plumage coloration has been photic mediated. At the intra-avian level we observed some unique adaptive patterns. For example, barn owl showed early signs of pseudogenization in RH2, perhaps in response to nocturnal behavior, and penguins had amino acid deletions in RH2 sites responsible for the red shift and retinal binding. These patterns in the barn owl and penguins were convergent with adaptive strategies in nocturnal and aquatic mammals, respectively. CONCLUSIONS: We conclude that birds have evolved diverse opsin adaptations through gene loss, adaptive selection and coevolution with plumage coloration, and that differentiated selective patterns at the species level suggest novel photic pressures to influence evolutionary patterns of more-recent lineages.

Rhodopsin gene polymorphism associated with divergent light environments in atlantic cod

The spectral sensitivity of visual pigments in vertebrate eyes is optimized for specific light conditions. One of such pigments, rhodopsin (RH1), mediates dim-light vision. Amino acid replacements at tuning sites may alter spectral sensitivity, providing a mechanism to adapt to ambient light conditions and depth of habitat in fish. Here we present a first investigation of RH1 gene polymorphism among two ecotypes of Atlantic cod in Icelandic waters, which experience divergent light environments throughout the year due to alternative foraging behaviour. We identified one synonymous single nucleotide polymorphism (SNP) in the RH1 protein coding region and one in the 3' untranslated region (3'-UTR) that are strongly divergent between these two ecotypes. Moreover, these polymorphisms coincided with the well-known panthophysin (Pan I) polymorphism that differentiates coastal and frontal (migratory) populations of Atlantic cod. While the RH1 SNPs do not provide direct inference for a specific molecular mechanism, their association with this dim-sensitive pigment indicates the involvement of the visual system in local adaptation of Atlantic cod.

Novel wasp toxin discriminates between neuronal and cardiac sodium channels

Pompilidotoxins (PMTXs), derived from the venom of solitary wasp has been known to facilitate synaptic transmission in the lobster neuromuscular junction, and a recent further study from rat trigeminal neurons revealed that the toxin slows Na+ channel inactivation without modifying activation process. Here we report that beta -PMTX modifies rat brain type II Na+ channel alpha -subunit (rBII) expressed in human embryonic kidney cells but fails to act on the rat heart alpha -subunit (rH1) at similar concentrations. We constructed a series of chimeric mutants of rBII and rH1 Na+ channels and compared modification of the steady-state Na+ currents by beta -PMTX. We found that a difference in a single amino acid between Glu-1616 in rBII and Gln-1615 in rH1 at the extracellular loop of D4S3-S4 is crucial for the action of beta -PMTX. PMTXs, which are small peptides with 13 amino acids, would be a potential tool for exploring a new functional moiety of Na+ channels.

Adaptive evolution of color vision of the Comoran coelacanth (Latimeria chalumnae)

The coelacanth, a “living fossil,” lives near the coast of the Comoros archipelago in the Indian Ocean. Living at a depth of about 200 m, the Comoran coelacanth receives only a narrow range of light, at about 480 nm. To detect the entire range of “color” at this depth, the coelacanth appears to use only two closely related paralogous RH1 and RH2 visual pigments with the optimum light sensitivities (λmax) at 478 nm and 485 nm, respectively. The λmax values are shifted about 20 nm toward blue compared with those of the corresponding orthologous pigments. Mutagenesis experiments show that each of these coadapted changes is fully explained by two amino acid replacements.

Molecular determinants of drug access to the receptor site for antiarrhythmic drugs in the cardiac Na+ channel.

The clinical efficacy of local anesthetic and antiarrhythmic drugs is due to their voltage- and frequency-dependent block of Na+ channels. Quaternary local anesthetic analogs such as QX-314, which are permanently charged and membrane-impermeant, effectively block cardiac Na+ channels when applied from either side of the membrane but block neuronal Na+ channels only from the intracellular side. This difference in extracellular access to QX-314 is retained when rat brain rIIA Na+ channel alpha subunits and rat heart rH1 Na+ channel alpha subunits are expressed transiently in tsA-201 cells. Amino acid residues in transmembrane segment S6 of homologous domain IV (IVS6) of Na+ channel alpha subunits have important effects on block by local anesthetic drugs. Although five amino acid residues in IVS6 differ between brain rIIA and cardiac rH1, exchange of these amino acid residues by site-directed mutagenesis showed that only conversion of Thr-1755 in rH1 to Val as in rIIA was sufficient to reduce the rate and extent of block by extracellular QX-314 and slow the escape of drug from closed channels after use-dependent block. Tetrodotoxin also reduced the rate of block by extracellular QX-314 and slowed escape of bound QX-314 via the extracellular pathway in rH1, indicating that QX-314 must move through the pore to escape. QX-314 binding was inhibited by mutation of Phe-1762 in the local anesthetic receptor site of rH1 to Ala whether the drug was applied extracellularly or intracellularly. Thus, QX-314 binds to a single site in the rH1 Na+ channel alpha subunit that contains Phe-1762, whether it is applied from the extracellular or intracellular side of the membrane. Access to that site from the extracellular side of the pore is determined by the amino acid at position 1755 in the rH1 cardiac Na+ channel.