Hsu, M. J., Moore, J., Lin, J. F. & Agoramoorthy, G. (2000). High
incidence of supernumerary nipples and twins in Formosan macaques
(Macaca cyclopis) at Mt. Longevity, Taiwan. Am. J. Primatol.
52: 199-205.
High incidence of supernumerary nipples and twins in Formosan macaques, Macaca cyclopis, at Mt. Longevity, Taiwan
| Fig. 1. Adult female Formosan macaque at Mt. Longevity with two symmetric pairs of supernumerary nipples/areolae. |
Key words: polythelia, twin, development, founder, Macaca cyclopis, Taiwan.
Methods
The study population of about 790 monkeys occupies Mt. Longevity, a 1,116
ha protected area covered with tropical lowland rainforest, located within the
city limits of Kaohsiung. Observations began in January 1995 and currently
16 troops are monitored on a regular basis. Subjects mentioned in this work
are individually known. Kin relations and ages were verified from
genealogical records compiled by the authors [unpublished]. Troop
compositions and polythelia prevalences reported here are from July 1999.
Troops are monitored at least three times per week during the birth season and twin births were inferred by the presence of two neonates nursing from a single female who continues to care for both. It is possible but highly unlikely that some "twins" could represent permanent neonatal adoptions; it is somewhat more likely that perinatal death of a twin might not be detected. Because observation conditions are good, and these potential problems bias results in opposite directions, we believe our reported twinning rate is very close to the actual one.
The term polythelia covers a range of eight types, from morphologically and functionally normal extra breasts (type 1) to "polythelia pilosa", a patch of hair only (Leung & Robson, 1989); all are associated with histologically identifiable glandular tissue (Camacho & Gonzalez-Campora, 1998). Animals were visually inspected without restraint for presence of supernumerary nipples or areolae (types 5-7). Without capture, distinguishing small nipples from areolae is difficult and they are not differentiated here. Polythelia can be difficult to detect within the fur (especially on males) and we included only individuals for whom we were confident supernumerary nipples/areolae would have been detected if present. Both the color and prominence of supernumerary nipples/areolae are hormone-dependent and they may not appear prior to puberty (Grossl, 2000; Zuckerman, 1935). Because of this the sample is restricted to adults.
Statistical analyses were performed using StatView (version 4.5).
Results
Supernumerary nipples
Eighty-nine of 211 females (42.2%) and 20 of 117 males (17.1%) possess
between 1-6 accessory nipples or areolae (Tables I, II; Fig.1). Nursing from
accessory nipples has never been observed. Since polythelia is less visible on
males, the sex difference may be partially artifactual, though we were aware of
this possible bias and attempted to avoid it (see Methods). Among humans, the
commonest form is a single accessory nipple but here 63.9 % of cases exhibit
two or more; the commonest pattern is two bilaterally symmetric nipples above
the normal pair (52.3% of cases). All extra nipples observed occur roughly
along the mammary line(s). Nipple/areola number is asymmetric in 43.1 % of
individuals. There is no left-right bias in asymmetry (right side with more
nipples than left, 23; left > right, 22; contra reports of a left-side bias in non-
humans (Hartman, 1927)), but females appear more likely to be asymmetric
(females: 48 symmetric, 41 asymmetric; males 16 and 4 respectively; p <0.06, chi-
square with Yates correction for continuity).
Troop name | Total no. of adult females in troop | Number of supernumerary nipples | Total of females with supernumerary nipples in troop (N, %) |
1 | 2 | 3 | 4 | 5 | 6 | N | % | ||
A | 10 | 1 | 2 | 0 | 0 | 0 | 0 | 3 | 30.0% |
B* | 17 | 7 | 0 | 1 | 2 | 0 | 0 | 10 | 58.8% |
C | 17 | 1 | 7 | 0 | 0 | 0 | 0 | 8 | 47.1% |
D* | 10 | 2 | 3 | 0 | 0 | 0 | 0 | 5 | 50.0% |
E | 10 | 0 | 2 | 0 | 1 | 0 | 0 | 3 | 30.0% |
F* | 17 | 2 | 3 | 1 | 0 | 0 | 0 | 6 | 35.3% |
G | 17 | 3 | 4 | 0 | 0 | 0 | 0 | 7 | 41.2% |
Aa | 5 | 0 | 1 | 0 | 0 | 0 | 0 | 1 | 20.0% |
I* | 15 | 4 | 4 | 0 | 0 | 0 | 0 | 8 | 53.3% |
J | 14 | 2 | 1 | 0 | 0 | 0 | 0 | 3 | 21.4% |
K* | 26 | 8 | 7 | 2 | 0 | 0 | 0 | 17 | 65.4% |
Ia | 8 | 0 | 1 | 0 | 0 | 0 | 0 | 1 | 12.5% |
M | 10 | 1 | 1 | 1 | 0 | 0 | 0 | 3 | 30.0% |
N | 11 | 1 | 1 | 0 | 1 | 0 | 0 | 3 | 27.3% |
O | 13 | 0 | 1 | 0 | 0 | 0 | 0 | 1 | 7.7% |
Ib* | 11 | 3 | 6 | 0 | 0 | 0 | 1 | 10 | 90.9% |
Total | 211 | 35 | 44 | 5 | 4 | 0 | 1 | 89 | 42.2% |
% | 100.00 | 16.6 | 20.9 | 2.4 | 1.9 | 0.0 | 0.5 | 42.2 |
Troop Name |
Total no.
of adult males in troop | Number of supernumerary nipples |
Total of males with supernumerary nipples in troop (N, %) |
1 | 2 | 3 | 4 | N | % | ||
A | 7 | 0 | 0 | 0 | 0 | 0 | 0 |
B | 11 | 0 | 3 | 0 | 1 | 4 | 36.4 |
C | 10 | 2 | 0 | 0 | 0 | 2 | 20 |
D | 8 | 0 | 1 | 0 | 0 | 1 | 12.5 |
E | 3 | 0 | 0 | 0 | 0 | 0 | 0 |
F | 11 | 1 | 1 | 0 | 0 | 2 | 18.2 |
G | 9 | 0 | 0 | 0 | 0 | 0 | 0 |
Aa | 4 | 0 | 1 | 0 | 0 | 1 | 25 |
I | 6 | 0 | 1 | 0 | 0 | 1 | 16.7 |
J | 9 | 0 | 1 | 0 | 0 | 1 | 11.1 |
K | 10 | 0 | 1 | 0 | 0 | 1 | 10 |
Ia | 3 | 0 | 1 | 0 | 0 | 1 | 33.3 |
M | 3 | 0 | 1 | 0 | 0 | 1 | 33.3 |
N | 9 | 0 | 1 | 0 | 0 | 1 | 11.1 |
O | 10 | 0 | 1 | 0 | 0 | 1 | 10 |
Ib | 4 | 1 | 1 | 1 | 0 | 3 | 75 |
Total | 117 | 4 | 14 | 1 | 1 | 20 | 17.1 |
% | 100 | 3.4 | 12.0 | 0.9 | 0.9 | 17.1 |
The prevalence of polythelia among adult females varied from
8% to 90% across troops (mean 39% ± 21%, N=16 troops); in only
four was the prevalence over 50%. For males, prevalence ranged
from 0 to 75% (mean 20% ± 19%) with only one troop with more
than 50%. Prevalence across troops among males and females was
correlated (p < 0.05) but this was due almost entirely to high
prevalence in Troop Ib (10 of 11 females, 3 of 4 males) and may be
spurious. Future research at the site will address this issue.
Twins
Co-occurrence of polythelia and twinning
Discussion
Most supernumerary nipples result from a failure to terminate mammary
bud development, consistent with over- or under-expression of Hox genes
(Schmidt, 1998). They occur in 1 - 5% of humans, are usually asymmetrically
expressed, and are associated with increased risk for urogenital malignancies.
The nature of possible causal relationships between gene defects, polythelia,
and urogenital disease is unknown (Casey et al., 1996; Urbani & Betti, 1996). It
is hoped that ongoing studies at Mt. Longevity can elucidate such possible
biomedically relevant associations in Taiwanese macaques.
Polythelia is anecdotally linked to multiple births in humans but
confirmatory data are lacking (Leung & Robson, 1989), however, and the
connection is currently thought spurious (Grossl, 2000). Our data suggest that
the connection merits reevaluation. Twins appear to be rare among
macaques. At Cayo Santiago the rate is under 0.1% (Koford et al., 1966; Rawlins
& Kessler, 1986). Hendrickx & Nelson (1971) give rates ranging from about 0.2
- 1% for several macaque and baboon colonies; the higher rates either include
abortions and stillbirths or have N < 100. In their largest sample, two twin
live-births were recorded among 838 rhesus (0.2%). Schultz (1956) has argued
that the rate of twinning is similar in humans and nonhuman primates (about
1%), but this is based on aggregating nonhuman taxa and the rate for
macaques in his data is about 0.3%. The rate at Mt. Longevity is apparently
between 3-10+ times greater than that of other macaques.
The cause[s] of the high incidences of twinning and polythelia at this site
is unknown, but founder effect and/or inbreeding in an isolated population
are obvious possibilities. A high rate of twinning is reported for an island
population of mouflon founded by a single pair (BoussŹs & RŽale, 1998), and
the troop-specific high incidences of polythelia reported by Itani et al. (1963)
and Zuckerman (1935) also suggest a matrilineal founder effect. This is the
first report in any nonhuman showing a clear association between the
phenomena. Ongoing noninvasive studies of the Mt. Longevity macaques
should help to elucidate the population genetics and fitness consequences of
both phenomena, as well as to study the relationship amongst multiple births,
polythelia, and (potentially) urogenital abnormalities.
Acknowledgments
Six pairs of twins (11 live births) have been observed since 1996, out of
596 births (1.01%, or 0.84% for 5 sets of live births only) (Table III; Hsu et al.,
2000). Both twins survived past 36 months in two cases and both died within
one week in one case. One of the infants (female 6) died after being carried
for three days by a juvenile aunt and presumably died of starvation. The
cause of death is unknown in the other cases.
All six of the females who produced twins have supernumerary nipples.
This is more than twice the overall prevalence (Fisher exact probability
P=0.005) and suggests a link between polythelia and multiple births. This is
further supported by an association between incidence of polythelia in troops
and presence of twinning; the six troops in which twins were born had the
highest incidences of polythelia (Table I; Mann-Whitney U-Test, U = 2.0, n=6,
10, p < 0.01).
Table III: Twin births at Mt. Longevity
#N : no of supernumerary nipplesTroop
ID
#N
Birthdate
Sex
Outcome
Other births
I
8
2
5/11/96
F, F
Survive
97F, 98M, 99M
I*
17
2
5/11/96
F, M
Survive
97-, 98M died < 2 mos, 99M
D
6
1
4/5/98
F, F
1 died < 1
month
96F, 97M, 99F
K
11
1
5/4/98
M, M
1 died < 1
month
96M, 97M died < 1 day,
99M
B
2
2
5/15/99 &
5/24/99
F
M
F dead < 1
day, M dead <
1 week
96F, 97M, 98M stillbirth
F
8
1
3/17/00 &
5/11/00
?
M
abortion
96F, 97F, 98F died at 2
mos (accidental), 99F
died < 3 mos
* Female F.I.17 moved to Ib when this new troop formed in October, 1998.
Polythelia among monkeys and apes is occasionally commented upon (e.g.,
"Several [of > 1,000 rhesus] have one or two non-functional supernumerary
nipples" ([Koford et al., 1966]) but there has been little quantitative work on
patterns and incidence (see Buss & Hamner III, 1971; Schultz, 1956). With
three exceptions, previous reports of incidence have been in the range of
about 1-5%, similar to that reported for humans (Grossl, 2000; Schultz, 1948).
The exceptions are a report by Thorington et al. (1979) who found
supernumerary nipples on five of 13 immobilized male red howlers (Alouatta
seniculus); a statement by Itani et al. (1963) that among Japanese macaques
"[i]n T-troop of Shodoshima ... nearly half of females there had extra nipples
(Itani and others, unpublished)"; and a report by Zuckerman (1935) that three
of 12 adult female chacma baboons he shot had extra nipples. The Mt.
Longevity Formosan macaque population has more individuals with polythelia
than have to date been reported for all non-human primates combined.
Partial funding for the ongoing field research on Formosan macaques at
Mt. Longevity has been provided by the Republic of China's National Science
Council through a research grant (NSC 88-2313-B- 020-023) awarded to G
Agoramoorthy and M J Hsu. Thanks to Jasmine Tan for her assistance.
REFERENCES