High incidence of supernumerary nipples and twins in Formosan macaques, Macaca cyclopis, at Mt. Longevity, Taiwan

 American Journal of Primatology 52:199-205 (2000)

High incidence of supernumerary nipples and twins in Formosan macaques,

      Macaca cyclopis, at Mt. Longevity, Taiwan

Minna J. Hsu a, Jim Moore b, Jin Fu Lin c, Govindasamy Agoramoorthy a, d

a Department of Biological Sciences, National Sun Yat-sen University, Kaohsiung, Taiwan, ROC

b Department of Anthropology, University of California at San Diego, La Jolla, CA 92093, USA

c Shi-Pu Junior High School, Kaohsiung, Taiwan, ROC

d Department of Wildlife Conservation, NPUST, Taiwan, ROC

           Abstract:

           A population of Formosan macaques at Mt. Longevity exhibits unusually high rates of both twinning (about 1% of births) and supernumerary nipples (polythelia; between 1-6 accessory nipples and/or areolae on 33% of adults).  The co-existence of these unusual traits suggests a connection, which is further supported by a tendency for mothers of twins to have accessory nipples and for twins to be born in troops with high incidence of polythelia. 

Key words: polythelia, twin, development, founder, Macaca cyclopis, Taiwan.

Introduction:

           The Formosan macaque (Macaca cyclopis) evolved from a rhesus macaque (M. mulatta) ancestor when they became isolated on the island of Taiwan (Hoelzer & Melnick, 1996).  At present they are restricted to coastal rainforests in the south, and mountainous forests in the east.  They are considered Threatened and are fully protected, though some poaching does continue (personal observations).  Although field surveys have been conducted to determine their status and distribution (Lee & Lin, 1991), little is known about their population ecology, reproductive parameters and social behavior.  Social behavior and troop size data are limited to a single troop studied in Kenting (Wu & Lin, 1992; Wu & Lin, 1993).  We have been monitoring 16 troops of Formosan macaques at Mt. Longevity, southern Taiwan since 1993 (Hsu & Agoramoorthy, 1999; Hsu et al., 2000).  In this report, we present data on the occurrence of supernumerary nipples among these monkeys and discuss them in light of the unusually high rate of twinning at this site.

           Most supernumerary nipples (polythelia) 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).  They are anecdotally linked to multiple births in humans but confirmatory data are lacking (Leung & Robson, 1989) and the connection is currently thought spurious (Grossl, 2000). 

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 paper are individually known.  Kin relations and ages were verified from genealogical records compiled by the authors [unpublished].

           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.

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 1, 2; 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.  Nipple number is asymmetric in 43.1 % of individuals.  There is no left-right bias in asymmetry (contra reports of a left-side bias in non-humans (Hartman, 1927)), but females appear more likely to be asymmetric (p <0.06, chi-square with Yates correction for continuity).

           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 67% (mean 19% ± 17%) with only one with more than 50%.  Prevalence across troops among males and females was correlated (p < 0.05).  The reason for this correlation is unclear; it seems to imply either assortative transfer by one or both sexes, or absence of transfer by either.  Neither seems likely based on the demography of other macaques and future research at the site will address this issue.

Twins

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 3; 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.

While the sample size is too small to assess significance, it is noteworthy that all six of the females who produced twins have supernumerary nipples.  This is more than twice the overall prevalence and suggestive of a link between polythelia and multiple births.

Discussion

           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.

           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.

           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 (Boussès & Réale, 1998), and the troop-specific high incidences of polythelia reported by Itani et al. (1963) and Zuckerman (1935) also suggest a matrilineal founder effect.   There is an association between incidence of polythelia in troops and presence of twinning; the five troops in which twins were born had the highest incidences of polythelia (Table 1; Mann-Whitney U-Test, U = 0, n=5, 11, p < 0.01).  Ongoing noninvasive studies of the macaques at Mt. Longevity 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

           Partial funding for the on-going field research on Formosan macaques at Mt.   Longevity has been provided by the Republic of China's National Science Council (NSC 88-2313-B- 020-023) through a research grant awarded to G Agoramoorthy and M J Hsu.

Table 1. Adult females with supernumerary nipples among free-ranging Formosan macaques at Mt. Longevity, Taiwan.

* indicates troops in which twins occurred.

Troop Name		Total no. of adult females in troop	Number of supernumerary nipples						Total of females with supernumerary
			1	2	3	4	5	6		nipples in troop (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

Table 2. Adult males with supernumerary nipples among free-ranging Formosan macaques at Mt. Longevity, Taiwan.

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
	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	10		0	1	0	0	1	10
	O	10		0	1	0	0	1	10
	Ib	3		1	1	0	0	2	66.7
Total		117		4	14	0	1	19	16.2
%		100		3.4	12.0	0.0	0.9	16.2

NEED TO CHECK; TEXT SAYS 20 of 117 BUT TABLE HAS 19

Table  3: Twin births at Mt. Longevity

Troop	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	10	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

#N : no of supernumerary nipples

* Female F.I.17 moved to Ib when this new troop formed in 1998 Oct.

　

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