* Institute of Zoology, Academic Sinica, Taipei, Taiwan
Department of Ecology and Evolution, University of Chicago
Human Genetics Center, University of Texas Houston Health Science Center
Department of Wildlife & Fisheries Sciences, Texas A&M University
|| Taipei Zoo, Taipei, Taiwan
Correspondence: E-mail:whli{at}uchicago.edu.
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Abstract |
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Key Words: bats opsin genes color vision nocturnal life opsin duplication
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Introduction |
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Bats of the suborder Microchiroptera occupy a nocturnal niche, and although they possess sight, members of this suborder use acoustic orientation (echolocation), rather than vision, as a major means of perceiving their environment (Bhatnagar 1975; Fuzessery et al. 1993; Heffner, Koay, and Heffner 2001). Thus, bats may represent the ideal model for studying the influence of a nocturnal life-style on the evolution of color vision genes.
The monophyly of the order Chiroptera (bats) was questioned earlier (Pettigrew 1986) but has been supported by recent studies (Nikaido et al. 2000; Teeling et al. 2000, 2002). Chiroptera is divided into two suborders, Megachiroptera (megabats) and Microchiroptera (microbats). Megachiroptera has only one family, Pteropodidae, and megabat species are either frugivorous or nectarivorous, lacking laryngeal echolocation and relying on olfaction or vision to search food. The flying fox (family Pteropodidae, genus Pteropus) is known to possess a highly developed visual system (Kalko, Herre, and Handley 1996; Schnitzler and Kalko 1998; Phillips 2000). However, as seen in typically nocturnal mammals, Pteropus giganteus has a very low cone/rod ratio (1/250) (Jacobs 1993), and consequently, its S or M/L opsin may not be functional. The suborder Microchiroptera contains 17 families, and although families like the Phyllostomidae reveal a diverse array of feeding preferences, members of most families are predominantly insectivorous. In addition, microbats have the ability to produce ultrasounds via the larynx, and members of this suborder rely on echolocation rather than a nocturnal eye for exploiting their environment (Bhatnagar 1975; Fuzessery et al. 1993; Schnitzler and Kalko 1998; Phillips 2000). Although one might predict that microbats may have lost functional opsin genes, Joshi and Chandrashekaran (1985) in their study of Hipposideros speoris found that this species responds to visual spectra of 430 and 520 nm, suggesting the existence of functional M and S opsins.
To our knowledge, no previous molecular study has examined the function and evolution of color vision genes in bats. Therefore, we have sequenced the M/L and S opsin genes in two megabats (pigmy fruitbat and flying fox) and one microbat (little brown bat).
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Materials and Methods |
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The polymerase chain reaction (PCR) was used to amplify M/L and S opsin genes. The PCR primers were designed using conserved regions of the opsin genes of primates, mice, and squirrels. As a result of variation in these genes, both PCR and sequencing primers were degenerate (table 1). Overlapping products of exons 2 (or 1) through 4 and exon 4 through exon 6 (or 5) of the M/L and S opsin genes were amplified and sequenced using these primers.
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All DNA fragments were cycle sequenced using BigDye sequencing kits (Applied Biosystems) and an ABI 377A automated DNA sequencer. Removal of excess fluorescent terminators was accomplished by Sephadex spin column. To avoid artifacts, multiple clones were sequenced. In H. fischeri, two copies of the M/L opsin were sequenced. To identify whether the two copies belong to one or two loci, 10 individuals were sequenced for polymorphism.
Sequence alignments were performed using Seqman (DNASTAR, Madison, Wis). We estimated the phylogeny of vertebrate opsins by a variety of methods. First, we determined the best-fit model of nucleotide evolution using hierarchical likelihood ratio tests (LRT) implemented in Modeltest (Posada and Crandall 1998). We also used LRT to compare a model that assumes that rate heterogeneity is partitioned among sites of codons, i.e. different rates are assumed for first, second, and third positions of codons. Next, we used the best-fit model to perform a heuristic search in PAUP*4.0 (Swofford 1999). We also performed bootstrap analysis with 1,000 pseudo-replicates using both the parsimony method and, separately, the Neighbor-Joining method employing ML distances from the best-fit model.
The number of nucleotide substitutions between sequences, the number of substitutions per nonsynonymous site (KA), and the number of substitutions per synonymous site (KS) were calculated by DnaSP (Rozas and Rozas 1999).
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Results |
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The best-fit model for middle/long wavelength vertebrate opsin data (fig. 3B) was Hasegawa-Kishino-Yano with Invariant sites and Gamma distributed rate heterogeneity (HKY85 + I + G). Parameter values were as follows: base composition A = 0.209, C = 0.314, and G = 0.244; transition/transversion ratio = 1.782; gamma shape = 1.290; proportion of invariant sites = 0.397. For neither data set did a model with rate heterogeneity partitioned among codon sites fit the data better than the gamma rate models. A model partitioning rate heterogeneity among different codon positions did not describe the data better than the gamma distribution. The resulting tree suggests that the L opsin may represent the ancestral state of the mammals and that it has been preserved in bats and cats but became an M (green) opsin in rodents, horses, and rabbits. In higher primates, a duplication of the L opsin occurred, and one of the two opsins became an M opsin. However, the bootstrap values in many of the nodes of the tree are weak, so the above scenario is uncertain and it is possible that the ancestral opsin of mammals was an M opsin and not an L opsin.
Duplication of the M/L Opsin Gene in H. fischeri
When we sequenced the region from exon 4 to exon 5 of the M/L opsin gene in an individual from H. fischeri, an additional copy was found. While exons 4 and 5 of the two copies were identical at nonsynonymous sites, the two copies of intron 4 differed by 20 nucleotides and 11 indels, including one large indel of 750 bp and involving a total of 794 sites. These differences appeared to be too large to represent two alleles of the same locus, indicating the possibility of two duplicate genes. Indeed, the sequence data from intron 5 revealed three different sequences, denoted as 51, 52, and 53 (fig. 4). Whereas introns 51 and 52 may represent two polymorphic alleles from the same locus, intron 53 differs from intron 51 at 10 sites and should represent another locus. (Because a locus can have at most only two different sequences, the presence of three sequences should indicate a gene duplication.) When we saw the above sequence differences, we decided to perform PCR on the same region from 10 more individuals. We found that each of them had two 2-gel bands. Sequencing of the two bands revealed the same differences in intron 4 (including one large indel), a finding that supports the presence of two duplicate M/L loci. Furthermore, the sequencing of exon 5 also revealed two different copies of the exon, as shown in table 3; all the differences are synonymous.
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Discussion |
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The three S opsin sequences of bats show conservation at the functional critical sitesi.e., the disulphide linkage of Cys109 and Cys186, the Schiff's base counterion Glu113 and at the site of retinylidene Schiff's base formation Lys295. Their interhelical cytoplasmic loops and luminal loops are more conserved than those found in primates (Shimmin, Mai, and Li 1997). The conservative cytoplasmic loops are related to the function in binding of transduction and initiation of phototransduction (Hunt et al. 1995). However, in nocturnal animals the S opsin tends to lose its function (Jacobs 1993; Jacobs, Neitz, and Neitz 1996). We note that the owl monkey Aotus diverged from Callithrix approximately 13 MYA, but it has lost its S opsin. The Syrian golden hamster also lost the S opsin after separation from other members of the subfamily Cricetinae approximately 2029 MYA (O'hUigin and Li 1992; Calderone and Jacobs 1999). In contrast, it has been suggested that bats have occupied a nocturnal niche for some 80 myr (Nikaido et al. 2000), yet both suborders still maintain a functional S opsin gene. Thus, it is possible that the two bat lineages have evolved the nocturnal life-style only relatively recently or have not been strongly nocturnal for a very long time; otherwise, they would have lost the S opsin gene.
In addition, we found that the S opsins of the three bats studied are actually sensitive to UV light according to Yokoyama and Yongsheng's (2000) five-site rules. Sites T52, F86, T93, A114, and S118 are also noted to be the ancestral amino acids of the UV pigment shared by chameleon, rat, and mouse (Yokoyama and Yongsheng 2000). One the one hand, UV vision may shift to blue vision by introducing a single change F86Y, or by accumulating any two of the critical amino acid changes (Yokoyama and Radlwimmer 2001; Cowing et al. 2002). On the other hand, fish, chameleon, mouse, and rat pigments have retained their UV sensitivities by accumulating no more than one of the five amino acid changes (Yokoyama and Yongsheng 2000). Bats may have preserved the UV pigment for an important purpose related to vision, even though the UV light is not available in the dark (Hut, Scheper, and Daan 2000). This hypothesis is supported by the evidence that visual pigments of vertebrates have usually been under strong selective pressure (Bowmaker 1991), and that most mammals have shifted to blue light. Alternatively, the preservation of UV light sensitivity in bats may suggest a short history of nocturnal life.
Two different evolutionary scenarios, flight-first or echolocation-first, have been proposed for the origin of acoustic orientation and true flight in bats (Arita and Fenton 1997; Simmons and Geisler 1998). The flight-first hypothesis suggests that ancestral bats possessed enhanced vision, followed by a reduction and simplification of the visual system as more emphasis was placed on laryngeal echolocation in microbats. In contrast, the echolocation-first hypothesis suggests that megabats lost laryngeal echolocation and developed better vision independently. Recent studies support the idea that flight evolved before echolocation (Arita and Fenton 1997; Simmons and Geisler 1998). However, vision in some microbats did not become less acute (Pettigrew et al. 1988). Some microbats possess similar numbers of retinal ganglion cells to those seen in rats and cats, and the visual acuity of microbats appears to be no less than that of megabats (Pettigrew et al. 1988; Heffner, Koay, and Heffner 2001). Vision may serve an important role in microbats that migrate long distances (Suthers and Wallis 1970), and some microbats even use vision in capturing prey (Bell 1985). Therefore, it is possible that microbats still retain multiple opsins for special occasions under light, or that the preservation of visual acuity (UV opsin) may enhance flight in the only nocturnal flying mammal. It is interesting to note that most microbats use vision quite well, and on moonlit nights they can avoid capture nets, not by using echolocation but by vision.
The critical functional sites of the M/L opsin include sites 180, 197, 277, 285, and 308, which had correctly predicted the in vitro-expressed pigment of many mammals studied to date (Sun, Macke, and Nathans 1997; Yokoyama and Radlwimmer 2001; Deeb et al. 2003). Compared to human M opsin (530 nm), H. fischeri and P. dasymallus formosus M/L opsins have two substitutions (F277Y, A285T), and M. velifer has three substitutions (A180S, F277Y, A285T), and these substitutions should shift their spectral sensitivity peaks toward red by 23 and
28 nm, respectively (Neitz, Neitz, and Jabobs 1991; Asenjo, Rim, and Oprian 1994; Yokoyama and Radlwimmer 2001). We have therefore proposed that these bats have the L-type opsin, although this proposal needs to be substantiated by a functional study. It seems that these species of bats have enjoyed the red vision, while some other mammals have shifted to the green vision (e.g., horse, dolphin, mouse, and rabbit), because it appears that the common ancestor of vertebrates had the L opsin (Yokoyama and Radlwimmer 2001). This finding is in agreement with the fact that H. fischeri and P. dasymallus formosus are fruigivorous, and thus may use color vision while foraging for ripe fruits. Interestingly, M. velifer (microbat) has one more substitution (A180S), which probably causes another 7-nm shift toward red. In these strong nocturnal insectivores with echolocation, the putative red shift suggests that either microbats have not been strongly nocturnal for a very long time or that the L opsin in micrbats may serve a purpose unrelated to vision.
It has been commonly believed that LW (long wavelength) and SW (short wavelength)/UV pigments are the consequence of the nocturnal life of ancestral mammals. However, recent phylogenetic evidence indicates that the UV pigment was the ancestral pigment of vertebrates and that blue pigments evolved from UV pigments in different vertebrate lineages (Hunt et al. 2001; Cowing et al. 2002). Some rodents (Jacobs 1992; Jacobs, Fenwick, and Williams 2001) and the bats in this study are the only UV-sensitive mammals known to date. We note that the lens of some diurnal rodents absorbs UV light and reduces the light that reaches the retina by 50% (Hut, Scheper, and Daan 2000), and some rodents live a strong nocturnal life without benefit of UV light except for circadian rhythms (Jacobs, Fenwick, and Williams 2001). It has been noted that a higher ratio of 360:520 nm light is emitted at dawn and at dusk (Hut, Scheper, and Daan 2000). Because the flying fox is known to be active at dusk (Kalko, Herre, and Handley 1996; Schnitzler and Kalko 1998; Phillips 2000), it might benefit from UV light. However, it is not clear whether microbats, which are strongly nocturnal, benefit from UV light.
Primates are thus far the only mammals known to possess duplicate genes for the M and L opsins. The present investigation shows that H. fischeri has a duplication of the L-opsin gene. The duplication may be fairly old, because the two copies have accumulated 20 nucleotide substitutions and 11 indels in intron 4, although exons 4 and 5 remain identical at nonsynonymous sites. The selective advantage of this duplication is unclear. Many nocturnal mammals (e.g., subterranean blind mole rats), cavefish, and crayfish have preserved the M/L opsin, and the reason was suspected to be related to circadian rhythm (Jacobs 1993; Yokoyama et al. 1995; Crandall and Hillis 1997; Shimmin, Mai, and Li 1997; David-Gray et al. 1999; Dkhissi-Benyahya et al. 2001). Thus, duplication of the L opsin may facilitate the regulation of circadian rhythm. However, the raccoon and the kinkajou have a single cone that responds to spectrum 550560 nm, and the owl monkey and the thick-tailed bushbaby have a single cone sensitive to spectrum 543545 nm (Jacobs and Deegan 1992; Jacobs, Neitz, and Neitz 1996). Therefore, if max (the absorbance spectrum maximum) relates to circadian rhythm regulation, there appears to be less selective constraint on the visual spectra.
Theory suggests three alternative outcomes for duplicated genes: (1) one copy may become nonfunctional; (2) one copy may acquire a beneficial function and be preserved by natural selection; and (3) the functions of both copies may become suboptimal (Ohno 1970; Lynch and Conery 2000). The most common fate for duplicate genes has been thought to be loss of a functional copy (Ohno 1970). The duplication of the L opsin in H. fischeri has accumulated several mutations in the introns, but the exons have been conserved. It is likely that maintaining both copies is beneficial. Multiple M- and/or L-opsin expressions have been found in humans, with the expression level higher than that for a single copy (Sjoberg et al. 1998). Overlapping expression in a single cone cell was also found in invertebrates (a crab, Hemigrapsus sanguineus, and a butterfly, Papilio xuthus). These species express two similar opsins in a photoreceptor cell, and these two loci may serve to broaden the spectral sensitivity of the photoreceptors (Sakamoto et al. 1996; Kitamoto et al. 1998). Pteropus giganteus (megabat) has a very low cone/rod ratio (1/250) (Jacobs 1993); therefore, it is possible that the increase in mRNA may increase the expression level and facilitate the sensitivity of photoreceptor cell.
The duplication of the L opsin in H. fischeri is the first case of opsin duplication found in nonprimate eutherian mammals. However, a recent microspectrophotometry study suggested trichromacy in Australian marsupials (Arrese et al. 2002). These observations suggest that duplication of the M/L opsin gene may have a broader distribution among non-primate mammals than currently known.
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Footnotes |
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