17. Genetic Diversity of Primate Color Vision
267
present.in the intron 4 sequences of all of the NWM alleles studied but absent from
both human genes. This conclusion is further supported by the finding that the Alu
repeat in intron 4 is also present in the three alleles from the capuchin, tamarin,
and saki monkey (Fig. 3). In addition, the two howler monkey genes and the two
human genes evidently have separated origins because the former contain the Alu
repeat while the latter do not (Fig. 3)
Shyue et al.'s (1995) intron 4 sequence data favored the multi-origin hypothesis
over the single-origin hypothesis because the three alleles in the squirrel monkey
formed one monophyletic group, and so did the three alleles in the marmoset. The
monophyly of the alleles in each species is also found in the capuchin, tamarin, and
saki monkey (Fig. 3). This tree was inferred by the neighbor-joining method (Saitou
and Nei 1987). For the parsimony analysis of insertions and deletions (indels, Fig.
3), the monophyly of the alleles in a species is supported by 6 indels in the marmoset, 1 indel in the tamarin, 5 indels in the squirrel monkey, and 7 indels in the
capuchin. Therefore, both the neighbor-joining tree and the indel analysis strongly
support the multi-origin hypothesis; in fact, they imply five independent origins for
the triallelic system, one in each species (Fig. 3). Further, Fig. 3 implies that the
two duplicate genes in the howler monkey had an origin independent of the triallelic
system in the other NW monkeys.
However, the clustering of the alleles in each species is probably due to gene
conversion. As described above, gene conversion occurs often between alleles in a
population. Previously, it was thought that transferring of indels between alleles is
unlikely to occur, so the clustering of alleles within each species was taken as evidence for an independent origin. However, the indel from positions 29 to 39 in
intron 4 of capuchin P562 has obviously been transferred to P535c (Fig. 2). In Fig.
3, the indels within each species also suggest indel transferring. For example, in
tamarin, 2 indels are shared by P543 and P562, 4 by P562 and P556, and 1 by P543
and P556. It is highly unlikely that so many indels arose independently in different
alleles. So, this pattern suggests the transfer of indels between alleles by gene conversion, partially homogenizing the allelic sequences.
As gene conversion can drastically mislead phylogenetic analysis at noncritical
sites for spectral tuning, the best data for inferring the evolutionary history of these
X-linked color vision alleles and duplicate genes are probably the amino acid changes
at the critical sites. Sites 180, 277, and 285 are the major critical sites, while sites
116, 229, 230, 233, and 309 have minor spectral tuning effects (see above). Sites
229 and 233 show a substitution pattern highly consistent with the three major sites
(Fig. 3). However, sites 230 and 309 show very minor variation among sequences,
so they are not informative for our purpose and will not be considered further. Site
116 is in exon 2, which is not under study. In terms of parsimony, Fig. 3 is highly
implausible because it requires many parallel amino acid changes at the five critical sites considered. For example, at position 180, at least seven parallel changes
between serine (S) and alanine (A) are required to explain the differences among
alleles and genes at this site. When all five critical sites are considered together, the
minimum number of substitutions required is 37 or 38, depending on whether one
assumes that the amino acids at sites 180, 229, 233, 277, and 285 in the common
267
present.in the intron 4 sequences of all of the NWM alleles studied but absent from
both human genes. This conclusion is further supported by the finding that the Alu
repeat in intron 4 is also present in the three alleles from the capuchin, tamarin,
and saki monkey (Fig. 3). In addition, the two howler monkey genes and the two
human genes evidently have separated origins because the former contain the Alu
repeat while the latter do not (Fig. 3)
Shyue et al.'s (1995) intron 4 sequence data favored the multi-origin hypothesis
over the single-origin hypothesis because the three alleles in the squirrel monkey
formed one monophyletic group, and so did the three alleles in the marmoset. The
monophyly of the alleles in each species is also found in the capuchin, tamarin, and
saki monkey (Fig. 3). This tree was inferred by the neighbor-joining method (Saitou
and Nei 1987). For the parsimony analysis of insertions and deletions (indels, Fig.
3), the monophyly of the alleles in a species is supported by 6 indels in the marmoset, 1 indel in the tamarin, 5 indels in the squirrel monkey, and 7 indels in the
capuchin. Therefore, both the neighbor-joining tree and the indel analysis strongly
support the multi-origin hypothesis; in fact, they imply five independent origins for
the triallelic system, one in each species (Fig. 3). Further, Fig. 3 implies that the
two duplicate genes in the howler monkey had an origin independent of the triallelic
system in the other NW monkeys.
However, the clustering of the alleles in each species is probably due to gene
conversion. As described above, gene conversion occurs often between alleles in a
population. Previously, it was thought that transferring of indels between alleles is
unlikely to occur, so the clustering of alleles within each species was taken as evidence for an independent origin. However, the indel from positions 29 to 39 in
intron 4 of capuchin P562 has obviously been transferred to P535c (Fig. 2). In Fig.
3, the indels within each species also suggest indel transferring. For example, in
tamarin, 2 indels are shared by P543 and P562, 4 by P562 and P556, and 1 by P543
and P556. It is highly unlikely that so many indels arose independently in different
alleles. So, this pattern suggests the transfer of indels between alleles by gene conversion, partially homogenizing the allelic sequences.
As gene conversion can drastically mislead phylogenetic analysis at noncritical
sites for spectral tuning, the best data for inferring the evolutionary history of these
X-linked color vision alleles and duplicate genes are probably the amino acid changes
at the critical sites. Sites 180, 277, and 285 are the major critical sites, while sites
116, 229, 230, 233, and 309 have minor spectral tuning effects (see above). Sites
229 and 233 show a substitution pattern highly consistent with the three major sites
(Fig. 3). However, sites 230 and 309 show very minor variation among sequences,
so they are not informative for our purpose and will not be considered further. Site
116 is in exon 2, which is not under study. In terms of parsimony, Fig. 3 is highly
implausible because it requires many parallel amino acid changes at the five critical sites considered. For example, at position 180, at least seven parallel changes
between serine (S) and alanine (A) are required to explain the differences among
alleles and genes at this site. When all five critical sites are considered together, the
minimum number of substitutions required is 37 or 38, depending on whether one
assumes that the amino acids at sites 180, 229, 233, 277, and 285 in the common