Zoological Studies 38(4): 379-386 (1999)

Molecular Evolutionary Analyses of the Rh Blood Group Genes andRh50 Genes in Mammals
Takashi Kitano, Satoshi OOta and Naruya Saitou*
Laboratory of Evolutionary Genetics, National Institute of Genetics, Mishima 411-8540, Japan(Accepted May 1, 1999)

Takashi Kitano, Satoshi OOta and Naruya Saitou (1999) Molecular evolutionary analyses of the Rh bloodgroup genes and Rh50 genes in mammals. Zoological Studies 38(4): 379-386. All mammals probably possess
the Rh blood group gene and its homologous Rh50 gene coded membrane proteins. In this study, we compared
nucleotide sequences of Rh and Rh50 genes for primates and rodents. We found that the rates of synonymous
substitutions of both genes were roughly constant, and the divergence time between mouse and rat was estimated to be about 30 million years ago (mya). Heterogeneity of the evolutionary rate between primates androdents was suggested. We also compared amino acid changes of outer-, inner-, and trans-membrane regionsof the Rh and Rh50 proteins. Amino acid changes of outer-membrane regions were more frequent except for
primate Rh genes. To obtain an improved estimation of divergence time, it is better to have multiple calibration
points for the molecular clock. The time of gene duplication that produced the Rh and Rh50 genes was estimated to be about 340-380 mya.
Key words: Rh and Rh50 genes, Relative rates, Divergence time.

The human Rh blood group plays importantroles in transfusion and clinical medicine, including
haemolytic diseases of newborns, autoimmune
diseases, and mild haemolytic anemia. Rh polypeptides were observed to be phosphorylated 30-32 kD
membrane proteins by using SDS-PAGE and immunoprecipitation (Gahmberg 1982, Moore et al. 1982),
and the Rh blood group system was shown to becomposed of 2 closely linked D and CE loci (Mouroet al. 1993). A protein was obtained together with the
Rh gene product on immunoprecipitation with antiRh antibodies from human, and named the 50kD
glycoprotein (Moore and Green 1987). This glycoprotein was considered to form a heterotetramer with
Rh blood group gene products on erythrocyte membranes (Eyers et al. 1994). The nucleotide sequenceof the human 50kD glycoprotein (Rh50) was determined, and its amino acid sequence was homologous with that of the human Rh gene (Ridgwell et al.
1992). That protein was also predicted to have the
12 trans-membrane domains which are similar to
those of the Rh blood group gene product (Avent etal. 1990).
Nucleotide sequences of Rh genes in nonhuman primates have been reported (Mouro et al.
1994, Salvignol et al. 1994 1995, etc.). We recently
analyzed those published Rh blood group genes ofprimates and found more nonsynonymous substitutions than synonymous ones, clear evidence of positive Darwinian evolution (Kitano and Saitou, 1999).
To see if a similar evolutionary pattern also exists inrodents, we determined nucleotide sequences of Rh
and Rh50 genes in mouse and rat as well as that of
the Rh50 gene for the crab-eating macaque (Kitano
et al. 1998). Results indicated that the Rh50 genehas been evolving about 2 times more slowly thanthe Rh blood group gene. Matassi et al. (1999) also
obtained a similar result.
In this study, we compare evolutionary rates ofRh and Rh50 genes for primates and rodents. We
also analyze the evolutionary relationship of thesegenes and examine the effect of numbers of OTUs
(operational taxonomic units) for estimation of divergence time.

*To whom correspondence and reprint requests should be addressed. Tel: 81-559-816790. Fax: 81-559-816789. E-mail: nsaitou@genes.
nig.ac.jp

379

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Zoological Studies 38(4): 379-386 (1999)

MATERIALS AND METHODS
Nucleotide sequence data for Rh, Rh50, andtheir related genes were retrieved from the DDBJ/
EMBL/GenBank international nucleotide sequence
database. Human RhD (X63097; Le Van Kim et al.
1992), human RhcE (X54534, M34015; Avent et al.
1990, Cherif-Zahar et al. 1990; both are identical),crab-eating macaque Rh (L37054; Salvignol et al.
1995), mouse Rh (AB015189; Kitano et al. 1998), rat
Rh (AB015191; Kitano et al. 1998), human Rh50
(X64594; Ridgwell et al. 1992), crab-eating macaqueRh50 (AB015467; Kitano et al. 1998), mouse Rh50
(AB015192; Kitano et al. 1998), rat Rh50
(AB015194; Kitano et al. 1998), and the Rh related
genes for nematode Caenorhabditis elegans(Z74026-B0240.1 and U64847-F08F3.3; Wilson etal. 1994.) and that for sponge (Y12397; Seack et al.
1997) were used.
CLUSTAL W version 1.6 (Thompson et al.
1994) was used for multiple alignments. The go/0
program (OOta and Saitou 1997) was used for constructing phylogenetic trees by the maximum likelihood method (Felsenstein 1981). The PredictProtein
server (EMBL) was used for analyses of trans-membrane helix location of these proteins.

the study of Easteal et al. (1995). Relative evolutionary distances between mouse and rat, and between
human and macaque were 0.35 and 0.1, respectively, when the distance between rodents and primates
was 1.0. If we assume that the relative evolutionaryrate (R) between primate and rodent lineages is

Fig. 1. Comparison of synonymous substitutions between Rh
and Rh50 genes of primates (human and crab-eating macaque)and rodents (mouse and rat). Boxes show points of dS with standard errors for Rh and Rh50 genes. Numbers in parentheses are
relative rates.

RESULTS AND DISCUSSION
Evidence for higher rates of nucleotide
substitution in rodents than in primates
We previously estimated numbers of synonymous (dS) and nonsynonymous (dN) substitutions for
Rh and Rh50 genes (Table 2 of Kitano et al. 1998).
Figure 1 shows a comparison of dS between Rh andRh50 genes based on their results. Because dS values were similar between Rh and Rh50 genes, they
were plotted close to the line of an angle of 45° (dSfor Rh = dS for Rh50). This suggests that thesegenes evolve at similar rates in terms of dS, and amolecular clock (constancy of evolutionary rate) exists for both Rh and Rh50 genes. Numbers in parentheses in this figure are relative evolutionary distances.
It has been suggested that mutation rates of rodents are higher than those of primates (Wu and Li
1985, Gu and Li 1992). We estimated relative evolutionary rates between primate and rodent lineages
and the divergence time between mouse and rat.
Figure 2A shows the scheme for this procedure. The
divergence time between primates and rodents was
assumed to be 122 million years ago (mya) based on

Fig. 2. Examination of relative evolutionary rate (R) between primate and rodent lineage. (A) The scheme for this procedure.
Numbers show R for each assumed divergence point between
primate and rodent lineage. (B) The relationship between R anddivergence time.

Kitano et al. − Evolution of Rh Blood Group Genes

equal (indicated by the arrow with number 1 in Fig.
2A), divergence times between human and macaque and between mouse and rat are estimated tobe 12.2 mya {= (0.1/1) × [122(mya)/2] × (2/1)} and42.7 mya {= (0.35/1) × [122(mya)/2] × (2/1)}, respectively. If we assume R = 2 (2 times higher in rodents
than primates; indicated by arrow 2 in Fig. 2A), thedivergence times between human and macaque andbetween mouse and rat are estimated to be 18.3
mya {= (0.1/1) × [122(mya)/2] × (3/1)} and 32.025
mya {= (0.35/1) × [122(mya)/2] × (3/2)}, respectively.
These values are given by the following formulas:

Thm = (Dhm/Dpr) × (Tpr/2) × (R + 1)
= (0.1/1) × (122/2) × (R + 1),
Tmr = (Dmr/Dpr) × (Tpr/2) × ([R + 1]/R)= (0.35/1) × (122/2) × ([R + 1]/R),

381

(1)
(2)

where Thm, Tmr, and Tpr are divergence times (mya)between human and macaque, between mouse andrat, and between primates and rodents, respectively.
Dhm, Dmr, and Dpr are relative evolutionary distances
between mouse and rat (0.35), between human andmacaque (0.1), and between primates and rodents(1.0), respectively.

Fig. 3. The multiple alignment of amino acid sequences of the Rh blood group genes and their related genes. Gaps are denoted bydashes. Asterisks and dots indicate invariant sites and sites occupied by chemically similar amino acids, respectively. The letters, i, t,and o, indicate regions of inner-membrane, trans-membrane, and outer-membrane, respectively. The 12 predicted hydrophobic membrane-spanning regions are boxed.

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Zoological Studies 38(4): 379-386 (1999)

Figure 2B shows the relationship among R, Tmr,
and Thm. If we assume the divergence time between
human and macaque to be 23 mya (Kumar andHedges 1998), R becomes approximately 2.8, andthe divergence time between mouse and rat becomes ca. 30 mya. This suggests that the mutation
rate in rodents is about 3 times higher than that inprimates. In this case, rate of synonymous substitutions (per site per year) of primate and rodent lineage
are estimated to be about 1.6 × 10-9 and 4.4 × 10-9,
respectively.
The divergence time between mouse and rat iscontroversial. Wilson et al. (1977) argued that it canbe anywhere between 5 and 35 mya, whereas
Jacobs and Pilbeam (1980) estimated it to be 8-14
mya. Recently, Kumar and Hedges (1998) estimatedit to be 41 mya based on 343 gene comparisons.
This value is substantially higher than our result. In
their study, however, the variance of the divergencetime between mouse and rat was larger than that between human and macaque, especially for the upper
part. In any case, our result is shorter than Kumar
and Hedges’s (1998) estimate.
Comparison of numbers of amino acidsubstitutions for different regions of Rh
and Rh50 genes
Figure 3 shows the multiple alignments of aminoacid sequences of Rh blood group genes and theirrelated genes. The amino acid sequence lengths ofRh genes for human D, human cE, crab-eating
macaque, mouse, and rat are 417, 417, 417, 418,
and 422, respectively. The amino acid sequencelengths of Rh50 genes for human, crab-eating
macaque, mouse, and rat are 409, 428, 438, and450, respectively. The amino acid sequence lengthsof Rh related genes for C. elegans 1 (Z74026-

B0240.1), C. elegans 2 (U64847-F08F3.3), andsponge are 457, 463, and 523, respectively. Twelve
membrane-spanning regions are shown by boxes.
We analyzed patterns of amino acid changes for3 regions (trans-membrane, inner-membrane, andouter-membrane) of primates (human vs. crab-eating macaque) and rodents (mouse vs. rat) Rh andRh50 genes (Table 1). Numbers of amino acid substitutions were estimated by using Kimura’s (1983)
method. Numbers of amino acid substitutions weremore or less similar among the 3 regions in primate
Rh genes. It is interesting that the number of aminoacid substitutions of trans-membrane regions of primate Rh genes was higher than those of others.
This suggests that primate Rh genes have lower selective constraints than the other genes.
Using a one-sided t-test (at the 5% level) we
found in primate Rh50 genes, the number of aminoacid substitutions of outer-membrane regions is significantly greater than that of trans-membraneregions. In rodent Rh genes, the number of aminoacid substitutions of outer-membrane regions is significantly (at the 1% level) greater than those of
inner- and trans-membrane regions. In rodent Rh50
genes the number of amino acid substitutions ofouter-membrane regions is also significantly greaterthan those of other regions (5% and 1% for innerand trans-membrane regions, respectively). It is also
noted that outer-membrane regions of rodent Rh andRh50 genes contain 4 gaps, and 1 and 11 gaps, respectively. These observations are compatible withthe results of numbers of amino acid substitutions.
Effect of the number of sequences on theestimation of the gene duplication timefor Rh and Rh50 genes
Figure 4 shows the phylogenetic tree for Rh

Table 1. Comparisons of numbers of amino acid substitutions per site (dA) andamino acid differences (PA in %) for each region of Rh and Rh50 genes
Rh

Rh50

dA ± SEPA

dA ± S.E.

PA

Primatestrans-membrane
inner-membraneouter-membrane

0.280 ± 0.041
0.248 ± 0.054
0.233 ± 0.059

23.3 (52/223)
21.1 (23/109)
20.0 (17/85)

0.081 ± 0.020
0.159 ± 0.044
0.194 ± 0.052

7.6 (17/223)
14.3 (14/98)
17.1 (15/88)

Rodentstrans-membrane
inner-membraneouter-membrane

0.143 ± 0.027
0.170 ± 0.043
0.513 ± 0.102

13.0 (29/223)
15.2 (17/112)
37.4 (31/83)

0.056 ± 0.016
0.131 ± 0.036
0.282 ± 0.062

5.4 (12/223)
12.0 (14/117)
23.5 (23/98)

Numbers of different sites/numbers of sites compared are shown in parentheses.

Kitano et al. − Evolution of Rh Blood Group Genes

blood group genes and their related genes by using
the maximum likelihood method by the go/0 programof OOta and Saitou (1997). Because these regions
do not include gaps and are relatively conserved,
only amino acid sequences of membrane-spanning
regions (223 sites) were used for tree reconstruction(Fig. 3). The root was located by assuming the Rhlike protein of sponge as an outgroup. There are 3
clusters in this tree: Rh50 genes of mammals, Rh
genes of mammals, and 2 genes of C. elegans. The
branch lengths of Rh50 genes are much shorter thanthose of Rh genes, indicating a lower evolutionaryrate in the Rh50 gene than in the Rh gene. It is interesting that after the gene duplication (indicated by aclosed diamond) which produced Rh and Rh50
genes, the Rh gene lineage started to evolve more
rapidly than the Rh50 lineage. Kitano et al. (1998)
obtained essentially the same tree by using theneighbor-joining method (Saitou and Nei 1987).
To examine the effects of numbers of sequences for estimation of the divergence time, wereconstructed 4 trees (Fig. 5) for Rh and Rh50 genesof primates and rodents by using the go/0 program of
OOta and Saitou (1997), and estimated the divergence time between Rh and Rh50 genes. The 223
amino acid sites for membrane-spanning regions(Fig. 3) were used for construction of trees. The root
for each tree was located by assuming the Rh-likeprotein of sponge (Seack et al. 1997) as an outgroup.
Numbers of amino acid substitutions of single lineage were obtained by applying the method of Ishida
et al. (1995) to each tree (Table 2). Because numbers of amino acid substitutions for Rh were consis-

Fig. 4. The phylogenetic tree of the Rh blood group genes andtheir related genes. Only amino acid sequences of membranespanning regions (223 sites; see Fig. 3) are used. The root was
located by assuming the Rh-like protein of sponge as an
outgroup. Diamonds on interior nodes indicate gene duplication.
The closed diamond indicates the gene duplication which produced between Rh and Rh50 genes.

383

tently 2-3 times higher than those for Rh50, a roughmolecular clock exists for both genes. Therefore, weestimated evolutionary rates of Rh and Rh50 genes
by using regression through the origin. Divergencetimes between human and crab-eating macaque,between mouse and rat, and between primates androdents were assumed to be 23 (Kumar and Hedges
1998), 30 (estimated in this study), and 122 (Easteal
et al. 1995) mya, respectively, and they were used
for calibration of the molecular clock.
In the case of tree A, the divergence time between Rh and Rh50 genes is estimated to be 130170 mya. This period roughly corresponds to theFig. 5. Four trees examining the effects of numbers of OTUs for
estimation of the divergence time between Rh and Rh50 genes.
Numbers on branches show numbers of amino acid substitutions
estimated from the maximum likelihood method. The root of
each tree was located by assuming the Rh-like gene of sponge
as an outgroup. (A) Rh and Rh50 genes for human and crabeating macaque were used. (B) Rh and Rh50 genes for mouseand rat were used. (C) Rh and Rh50 genes for human andmouse were used. (D) Rh and Rh50 genes for human, crabeating macaque, mouse, and rat were used.

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Zoological Studies 38(4): 379-386 (1999)

early Mesozoic before the mammalian radiation. Because these values are close to the divergence time
between primates and rodents, these are probably
underestimations. Acceleration of evolutionary rate
for the primate lineage by positive selection may
have affected these values. In the case of tree B, thedivergence time is estimated to be 290-320 mya.
This period roughly corresponds to the latePaleozoic. These values are about 2 times higher
than those of tree A. In the case of tree C, the divergence time is estimated to be 370-450 mya. In thecase of tree D, the divergence time is estimated to be340-380 mya. This period roughly corresponds tothe middle Paleozoic, and the divergence between
land vertebrates and amphibian lineage occurred
around that period. The ranges of these values are
smaller than those of tree C. It is clear from thesecomparisons that many calibration points for the molecular clock are needed to obtain a better estimationof divergence times. Figure 6 shows comparisons
between amino acid substitutions and divergencetimes from tree D of figure 5. It indicates evolutionary
constancy of Rh and Rh50 genes except in primates.
It is interesting that evolutionary rates of Rh andRh50 genes are accelerated on the primate lineage.
In any case, one should be very careful when estimating the divergence time of genes.
In conclusion, we performed evolutionary analyses of the Rh blood group genes and its homologous
Rh50 genes in the present study. First, we compared synonymous substitutions of Rh and Rh50
genes in primates and rodents. As a result, we obtained the result that the mutation rate in rodents isabout 3 times higher than that in primates, and we
could estimate the divergence time of mouse and rat.
Second, we compared amino acid changes of outer-,inner-, and trans-membrane regions of the Rh andRh50 proteins. Amino acid changes of outer-membrane regions were more frequent than others ex-

cept for primate Rh genes. Finally, we made themultiple alignment for these genes and constructed
the phylogenetic tree. The time of the gene duplication that produced the Rh and Rh50 genes was estimated to be about 340-380 mya. To obtain a moreaccurate estimation of divergence time, it is better tohave multiple calibration points for the molecular
clock.

Fig. 6. Comparisons between amino acid substitutions and divergence times from tree D of figure 5. Closed circles and closed
squares show points for Rh and Rh50 genes, respectively. Divergence times between Rh (open circle) and Rh50 (open square)genes are estimated by using regression through the origin.

Table 2. Numbers of amino acid substitutions and divergence times
Diverging node:
Divergence time (mya):

human/macaque(23)

mouse/rat(30)

primates/rodents(122)

Rh/Rh50

Rh (Tree A)
Rh (Tree B)
Rh (Tree C)
Rh (Tree D)

13.73
–
–
13.66

–
7.29
–
7.38

–
–
22.46
24.68

79.44
78.10
82.07
82.79

133
321
446
381

Rh50 (Tree A)
Rh50 (Tree B)
Rh50 (Tree C)
Rh50 (Tree D)

3.99
–
–
4.06

–
2.78
–
2.79

–
–
8.43
9.94

28.71
26.83
25.33
29.15

165
290
366
342

a

timea

Divergence time (mya) between Rh and Rh50 genes estimated from numbers of amino acid substitutions ofeach tree of figure 5.

Kitano et al. − Evolution of Rh Blood Group Genes

Acknowledgments: This study was partially supported by grants-in-aid for scientific studies from the
Ministry of Education, Science, Sport, and Culture,
Japan to N. S.

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Laboratory of Evolutionary Genetics, National Institute of Genetics, Mishima 411-8540, Japan