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Esterase D in Brazilian Saguinus midas nigerЧresults and comparison with previous studies in Anthropoidea.

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American Journal of Primatology 22:215-219 (1990)
Esterase D in Brazilian Saguinus midas niger-Results
and Comparison With Previous Studies in Anthropoidea
CARMEM M.L. BARROSO', MARIA P.C. SCHNEIDERl, MARIA I.C. SAMPAIOl, AND
FRANCISCO M. SALZAN02
'Departamento de Genktica, Centro de Cisncias Biologicas, Universidade Federal do Para,
Campus Universitario do Guama, Belim, PA, and 'Departamento de Genktica, Instituto de
Bioci&cias, Universidade Federal do RW Grande do Sul, Porto Alegre, RS, Brazil
Four esterase D (ESD)phenotypes, presumably resulting from the segregation of three alleles with moderate polymorphic frequencies, were observed in a sample of the black handed tamarin, Saguinus midas niger,
from the northern Amazonian region (Brazil). Previous surveys in the
non-human Anthropoidea indicate that the ESD locus is polymorphic in at
least 4 of the 19 taxonomic entities listed.
Key words: polymorphism, black handed tamarins, Callithrichidae
INTRODUCTION
The esterase D (ESD) polymorphism was first described in humans more than
a decade ago [Hopkinson et al., 19731,and since then studies of this locus have been
made both in humans and in other primates. As part of a long-term project of
genetic investigation of New World primates [Schneider et al., 1982, 1983, 1985;
Sampaio et al., 1986; Sampaio & Schneider, 19861we added the study of this locus
to our testing battery. In a previous investigation one heterozygous animal for the
ESD locus was detected in 8 captive specimens of Saguinus midas niger [Schneider
et al., 19831. We now report the presence of three alleles at the ESD locus in a
natural population of black handed tamarins (S. m. niger) from the Brazilian
Amazonian region and compare this information with previous data on this system
in Platyrrhines and Catarrhines.
METHODS
The genus Saguinus has a widespread geographical distribution, extending
from Central America (Costa Rica and Panama) to northern South America, including the Guianas, Colombia, Ecuador, Peru, Bolivia, and Brazil. Hershkovitz
119771 proposed 10 species and 29 subspecies for this genus. Saguinus midas has
been subdivided in two subspecies: S . m. midas and S . m. niger, the latter having
a very restricted geographical distribution. It is found only between the Xingu and
Gurupi rivers, south of the Amazon.
Blood samples were obtained from 73 males and 50 females belonging to a
Received for publication July 31, 1989; accepted November 13, 1989.
Address reprint requests to Prof. Francisco M. Salzano, Departmento de Genbtica, Instituto de Biocihcias, UFRGS, Caixa Postal 1953, 90001 Porto Alegre, RS, Brazil.
0 1990 Wiley-Liss,Inc.
216 / Barroso et al.
Fig. 1. Esterase D electrophoretic patterns in S . m. niger, compared with the ESD 2-1 heterozygous pattern
of Cebus apella (Ca). The faint second band shown in the 1 pattern is most probably secondary, due to posttranslational changes.
natural population of Saguinus midas niger living a t the west margin of the Tocantins river (4“5’-4”38’S;49”5’-49”50’W).These animals were captured before the
formation of a large water reservoir for the Tucurui Hydroelectric Power Station.
Following capture, they were transported to a field base, where they were bled and
later released in an area away from flooding.
For the blood collections the animals were anesthetized with Ketalar (ketamine chloride, Park Davis) at a dose equivalent to 10 mg/kg of weight, and the
samples were processed as previously reported [Sampaio & Schneider, 19861. Detection of ESD phenotypes was performed with horizontal electrophoresis using 1%
agarose gel (Sigma’stype I) with the citrate-phosphate buffer. Running buffer was
0.015 M trisodium citrate, 0.022 M monobasic sodium phosphate, and 0.0005 M
EDTA, adjusted to pH 6.9 with 10 N NaOH (this solution was diluted 1:4 to make
the gel buffer). Staining was as described by Hopkinson et al. [1973], using a
solution of 4-methylumbeliferil acetate (10 mg) in acetone (0.5 ml) and acetate
buffer 0.05 M (pH 5.21, which was spilled on the gel. After 10 minutes, ESD-bands
were observed under UV light and photographed with Kodak Tri-X 400 ASA film
through an orange filter. The gene frequencies and standard deviations were estimated by the maximum likelihood method using the MAXLIK program of Reed
and Schull [19681.
RESULTS
Four different electrophoretic ESD phenotypes were observed (Fig. 1). The
ESD 2 band of S. m. niger shows an electrophoretic mobility similar to human ESD
1 [Hopkinson et al., 19731, to Cebus upella ESD 1 [Schneider et al., 1982, 1983;
Sampaio et al., 19861 and to Chiropotes satanus ESD 2 [Sampaio & Schneider,
19861. The putative heterozygotes show a three-banded pattern, consistent with
the dimeric molecular structure proposed for this enzyme.
Esterase D in Tamarin Monkeys / 217
TABLE I. Esterase D Phenotype and Allele Frequencies in Two
Samples of Saguinus midus niger
Phenotype and
allele frequencies
Phenotypes
1
2-1
2
3-2
Total
X2
df
P
Alleles
ESD*l
ESD*2
ESD*3
Captives"
Natural populationb
0
0
7
1
8
0.00
1
-
2
36
84
1
123
0.30
3
0.92
Frequency
SD
0.168
,024
0.828
0.24
0.004
.004
Frequency
0.94
0.06
SD
0.06
0.06
"Obtained at the Animal Rearing Division of the Federal University of Parit
[Schneider et al., 19831.
bLiving at the west bank of the Tocantins river (present communication).
Table I shows the phenotype and allele frequencies observed in this sample,
comparing them with previous data obtained from a smaller group of animals from
the same species. The genotype distribution is in Hardy-Weinberg equilibrium,
under the assumption that phenotypes are determined by three different alleles.
Since the frequencies showed no differences between sexes, data from males and
females were pooled. The most frequent allele (ESD*2)occurs with a prevalence of
83% in the Tocantins sample; another fairly frequent form (ESD*l, 16%) and a
rare variant (ESD*3, 0.4%) were also found. These findings confirm our previous
report and further extend it, allowing us to estimate gene frequencies.
DISCUSSION
A comparison of these data with 19 other taxa of Anthropoidea is summarized
in Table 11. Although a straightforward comparison is not possible due to sampling
or the lack of data on geographic variation, Homo sapiens appears as the most
polymorphic species. One species, Cebus apella, presents a high degree of polymorphism, while two others (Chiropotes satanas and Saguinus midas niger) exhibit
moderate variation. An added complication is the fact that all Callithrichids are
blood chimeras. This could lead to a spurious increase in the frequency of heterozygotes in heterozygous x heterozygous or heterozygous x homozygous matings.
However, this was not observed in our sample, in which we found one 3-2 and 36
2-1 heterozygotes, while the numbers expected by the calculated gene frequencies
would be, respectively, 1 and 34.
Interestingly, while the majority of the taxa (Cebus apella, Cebus albifrons,
Saimiri sciureus, Aotus triuirgatus) show bands with mobility similar to human
ESD 1[Schneider et al., 19821,the variability present in C . satanas and S. m. niger
leads to fractions of lower mobility (their ESD 1 band presenting a migration
slower than that of the ESD 1of Cebus apella, humans, and other members of the
first group). On the other hand, the single band observed in the two specimens of
Lagothrix lagothricha had a mobility equivalent to that of s. m. niger's ESD 3,
which may be similar to the human ESD 2 [Schneider et al., 19831.
218 I Barroso et al.
TABLE 11. Esterase D Studies Performed Among the Anthropoidea
Degree of
polymorphism"
Taxonomic category
and sDecies
No.
studied
Monomoruhic
No.
Alleles
High
8
X
Moderate
Low
Referencesb
~~
Anthropoidea
Catarrhini
Hominidae
Homo sapiens
Pongidae
Pan troglodytes
Cercopithecidae
Cercopithecus aethiops
Papio anubis
Papio hamadryas
Macaca sinica
M. fuscata
M . fascicularis
M . nemestrina
M. silenus
Platyrrhini
Cebidae
Cebus apella
C. a1bifrons
Saimiri sciureus
Aotus triuirgatus
Chiropotes satanas
Lagothrix lagothricha
Callithrichidae
Saguinus midas niger
S . mistax
S. labiatus
S. oedivus
thousands
19
125
68
438
131
1,655
231
8
2
241
2
15
2
X
130
21
29
21
2
1
X
X
X
X
X"
X
X"
X
X
2
X
X
X
89
2
1
X
1
1
1
2
1
X
X
X
X
X
X
3
4
4
5
6,9
7
8
9
10,11,12
11
11
11
13
11
11,14
15
15
15
"Classified according to the frequency of the second most common allele as follows: high = 0.31-0.50; moderate
= 0.11-0.30; low = 0.01-0.10.
bl)Hopkinson e t al. 119731; Papiha & Nahar [19771; Nishigaki & Itoh [19841. 2) Nozawa e t al. [1982al. 3)
Palmour et al. [19801.4) Shotake t19811.5) Shotake & Santiapillai 119821.6) Nozawa et al. [1982b]. 7) Kawamoto
& Ischak [1980]. 8) Anderson & Giblett (1975). 9) Scheffrahn & Ziggioti [19811. 10) Schneider e t al. 119821. 11)
Schneider e t al. [1983]. 12) Sampaio et al. [19861. 14) Present communication. 15) Nagai e t al. [1986).
'Polymorphic variation in one troop only.
CONCLUSIONS
1. Saguinus midas niger exhibits polymorphism for the ESD locus.
2. The occurrence of ESD intrapopulacional variation in four other nonhuman primate taxa, plus the already observed interspecific differences in electrophoretic mobility found in the isozymes of this system subjected to the same
testing conditions, indicates that this enzyme may usefully contribute to the understanding of the evolutionary relationships in the Anthropoidea.
ACKNOWLEDGMENTS
This work was supported by UFPA (Universidade Federal do Para), FINEP
(Financiadora de Estudos e Projetos), CNPq (Conselho Nacional de Desenvolvimento Cientifico e Tecnologico), FADESP (Fundacao de Amparo e Desenvolvi-
Esterase D in Tamarin Monkeys / 219
mento da Pesquisa), ELETRONORTE (Centrais Eletricas do Norte do Brasil, S.A.)
and Schultz Foundation, Switzerland. Special thanks are due to Miss Maria Ilma
da Silva Mera for technical help, and to Dr. Horacio Schneider and Mr. Domingos
Nunes, for field assistance.
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