Behavioral Ecology Vol. 13 No. 5: 643-652
© 2002 International Society for Behavioral Ecology
Male bimaturism and reproductive success in Sumatran orang-utans
a Ethologie & Socio-ecologie, Universiteit Utrecht, PO Box 80086, 3508 TB Utrecht, The Netherlands b Fakultas Biologi, Universitas Nasional, Jl. Sawo manila, Jakarta 12510, Indonesia c Biodiversity and Ecological Processes Group, School of Biosciences, Cardiff University, PO Box 915, Cathays Park, Cardiff CF10 3TL, UK d Evolutionary Anthropology Research Group, Department of Anthropology, University of Durham, 43 Old Elvet, Durham DH1 3HN, UK
Address correspondence to B. Goossens. E-mail: goossensbr{at}cardiff.ac.uk. S.S. Utami and B. Goossens contributed equally to this study and are joint first authors.
Received 25 July 2000; revised 31 August 2001; accepted 19 December 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Although orang-utans live solitary lives most of the time, they have a complex social structure and are characterized by extreme sexual dimorphism. However, whereas some adult male orang-utans develop full secondary sexual characteristics, such as cheek flanges, others may stay in an "arrested" unflanged condition for up to 20 years after reaching sexual maturity. The result is a marked bimaturism among adult males. Flanged males allow females to overlap with their home range and often tolerate the presence of unflanged males. However, wherever possible flanged males actively prevent unflanged males from copulating with females. Two competing hypotheses, previously untested, have been advanced to explain male reproductive behavior and bimaturism in orang-utans: (1) the "range-guardian" hypothesis, which asserts that the flanged males are postreproductive and defend a range in which they tolerate sexually active, unflanged male relatives; and (2) the "female choice" hypothesis, which asserts that flanged males tolerate unflanged males in their range because they rely on female preference to favor flanged males. We investigated these hypotheses and a third hypothesis that the two male morphs represent co-existing alternative male reproductive strategies ("sitting, calling, and waiting" for flanged males versus "going, searching, and finding" for unflanged males). Fecal samples were collected from a well-studied population in Indonesia, and eight human microsatellites were analyzed for 30 individuals that have been behaviorally monitored for up to 27 years. By carrying out paternity analysis on 11 offspring born over 15 years, we found that unflanged males fathered about half (6) of the offspring. Relatedness between successful unflanged males and resident dominant males was significantly lower than 0.5, and for some unflanged/flanged male pairs, relatedness values were negative, indicating that unflanged males are not offspring of the flanged males.
Key words: fecal analysis, mating strategies, microsatellites, non-invasive sampling, orang-utans, paternity, relatedness, Pongo pygmaeus abelii.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The causes and consequences of secondary sexual characters (SSCs) for male reproductive success in vertebrates have been a dominant and controversial issue in evolutionary ecology over the last 20 years (Andersson, 1982
;
Jones et al., 1998;
Møller, 1992). Crucial
to exploring competing hypotheses as determinants of male lifetime
reproductive success has been the impact of molecular ecological studies that
allow an individual's genetic output to be directly measured
(Jennions and Petrie, 2000;
Pemberton et al., 1992).
Although such studies have been applied successfully in wild primates (e.g.,
Altmann et al., 1996;
de Ruiter et al., 1994), they
have yet to be successfully applied in great apes, where special problems
include logistical difficulties in sampling, long generation time, and the
threatened status of many populations pertain (but see
Constable et al., 2001;
Gagneux et al., 1999;
Gerloff et al., 1999).
Orang-utans are semisolitary, but their ranges overlap to a large extent,
and they may aggregate occasionally in large fig or fruit patches
(MacKinnon, 1974;
Rijksen, 1978;
Schürmann and van Hooff,
1986). Sometimes, in the fruiting season, these aggregations
develop into bands (Sugardjito et al.,
1987; Utami et al.,
1997) in which individuals may travel together in a coordinated
fashion. The only other time adult orang-utans associate is during
reproductive consortship, when a male and female may range together for
several days, weeks, or even months and engage in sexual behavior
(Rijksen, 1978). Other
individuals (females, unflanged males, and adolescents) may also congregate
around consorting individuals
(Schürmann and van Hooff,
1986), although fully mature, flanged males never associate and
usually behave antagonistically toward each other (e.g.,
Mitani, 1985a;
Rijksen, 1978;
Rodman and Mitani, 1987).
Orang-utans exhibit extreme sexual dimorphism in male SSCs such as flanged
cheeks and a throat sac, which enables them to produce loud calls to advertise
their presence (Galdikas,
1985b; MacKinnon,
1974; Rijksen,
1978; Rodman,
1984). These characteristics are hypothesized to have arisen as a
result of sexual selection in which female choice or male—male
competition has played an important role
(Rodman and Mitani, 1987;
Schürmann and van Hooff,
1986). In addition, there is remarkable bimaturism among adult
males, who vary considerably in the age at which their SSCs develop. In some
males this transition may be delayed until around the age of 30 (see below).
Although these unflanged or "arrested" males lack SSCs, they are
fertile, sexually active, and can sire offspring
(Kingsley, 1982;
Maggioncalda, 1995). Social
factors, such as the presence of a dominant adult male, are thought to
influence the delay of SSC development in such males (Maggioncalda, 1999;
Schürmann and van Hooff,
1986).
Bimaturism has been studied in apes by Leigh
(1995) and Leigh and Shea
(1995), who attributed adult
dimorphism in orang-utans to sexual selection for indeterminate male growth.
To date, the most comprehensive study that has found evidence, from both
behavioral and genetic data, of a clearcut relationship among male secondary
sexual development, social dominance, copulatory behavior, and reproductive
success was carried out in mandrills (Mandrillus sphinx;
Wickings et al., 1993). The
authors identified two morphological variants of adult male;
"fatted" males (with maximum secondary sexual coloration and which
occupy dominant positions in the social group) and "non-fatted"
males (with muted secondary sexual adornments, smaller testes, and which live
as peripheral/solitary individuals). DNA fingerprinting analyses showed that
only the two most dominant fatted males in the group fathered offspring. Male
rank and mating success were strongly correlated and the alpha male sired
80-100% of the resulting offspring during 3 consecutive years.
Flanged and unflanged males also differ in their mating strategies. Flanged
males, and especially dominant individuals, often establish consortships with
potentially reproductive females and are usually preferred by females
(Utami, 2000). Unflanged males
engage in consortships comparatively rarely, but often try to copulate with
females, even when they resist (Galdikas,
1985b; MacKinnon,
1974; Mitani,
1985a; Rijksen,
1978; Schürmann and van
Hooff, 1986). Two hypotheses have been put forward to explain
these mating patterns and to understand how two different adult male morphs
can co-exist in an evolutionarily stable situation and here we posit a
supplementary hypothesis related to the second.
The range-guardian hypothesis
The range-guardian hypothesis asserts that flanged males are
postreproductive and defend a range in which they tolerate sexually active,
unflanged males who are related to them. MacKinnon
(1974) first reported sexual
interactions among orang-utans. However, he never observed sexual behavior by
a flanged male, but repeatedly observed both forced and unforced matings by
unflanged males. A model where flanged males are postreproductive and defend a
range in which they tolerate sexually active, unflanged males is only
sustainable in an inclusive fitness context (e.g., if flanged males
selectively tolerate sons or other male relatives). However, a number of more
recent studies have shown that flanged males can be sexually active, mostly
while engaged in a consortship (Mitani,
1985a; Schürmann,
1982; Schürmann and van
Hooff, 1986). Therefore, a model implying a totally
nonreproductive role for flanged males is questionable. However, selective
tolerance of unflanged male relatives based on inclusive fitness benefits
cannot be rejected based on these observations. The evolutionary predictions
of this hypothesis are that unflanged males have a share in reproduction and
that flanged and unflanged males in an overlapping range are related.
The female choice hypothesis
The female choice hypothesis asserts that flanged males tolerate unflanged
males in their range because they rely on female preference to favor flanged
males. Schürmann and van Hooff
(1986) and van Hooff
(1995) have argued that the
co-existence of two sexually mature male morphs could only have evolved as
stable alternative strategies if it is assumed that female choice plays a
pivotal role. This contrasts with the view of Rodman and Mitani
(1987), who proposed that the
extreme sexual dimorphism of orang-utans and their bimaturism rests solely on
strong male—male competition and that female choice plays no role in the
evolution of bimaturism. However, because fertile female orang-utans are
usually widely dispersed spatially
(Galdikas, 1985b;
Rijksen, 1978;
Rodman and Mitani, 1987;
Schürmann and van Hooff,
1986; van Schaik and van
Hooff, 1996), and given the dense character of the forest habitat
and the large size of orang-utan home ranges, it is difficult to envisage how
a dominant flanged male could permanently control access to all the females in
his range (van Hooff and van Schaik,
1992). Thus, other males might still have the opportunity to gain
access to females, especially unflanged males who are less conspicuous and do
not advertise their presence. Moreover, it would seem evolutionary feasible
for flanged males to invest in growth and in defending a territory against
other flanged males, while tolerating unflanged males to some extent, if
females had a preference for flanged males when it really mattered (i.e., when
they are fertile; van Hooff,
1995). Consequently, the prediction would be that flanged males
fertilize the females.
The sit-and-wait versus go-and-search hypothesis
The sit-and-wait versus go-and-search hypothesis asserts that flanged males
and unflanged males represent alternative reproductive strategies. This
hypothesis (a variant to the female choice hypothesis) posits that unflanged
males are also reproductively successful because the two male reproductive
strategies are at an evolutionary stable equilibrium. Flanged males are
reproductively successful because they are preferred by females in most cases.
Flanged males sit and wait for fertile females that are attracted by their
long calls and subsequently consort with them. Flanged males would have to
tolerate unflanged males because of the difficulty of excluding them
effectively. This allows unflanged males to go and search for females in a
less conspicuous and therefore less provocative manner. Under this scenario it
could be possible that the presence of unflanged males would attract more
females, as has been suggested for satellite males who are tolerated by male
lek winners in the ruff Philomachus pugnax
(van Rhijn, 1973). The
prediction would be relatively low reproductive success for unflanged males,
as has been observed in a recent study of reproductive success in ruff (Burke
T, personal communication) and in Bullock's orioles, which demonstrate
age-specific plumage characteristics
(Richardson and Burke,
1999).
Microsatellites are now used routinely in primates for paternity and
relatedness analyses (Altmann et al.,
1996; Gagneux et al.,
1999; Gerloff et al.,
1999; Keane et al.,
1997; Morin et al.,
1994; Nievergelt et al.,
2000), and many human-derived microsatellite loci have been
described as suitable in a large number of primates (e.g.,
Coote and Bruford, 1996),
especially in the apes (e.g., Clifford et
al., 1999; Field et al.,
1998; Goossens et al.,
2000b). Recent technical developments in the use of noninvasively
collected samples (Taberlet et al.,
1999) such as hair (e.g.,
Gagneux et al., 1999) and
feces (e.g., Kohn and Wayne,
1997) now provide the possibility of studying endangered species
such as orang-utans.
To test the hypotheses described above, we compared mating pattern data collected during a 30-year field study in Ketambe, Gunung Leuser, Sumatra, Indonesia, with genetic data derived from polymorphic human-derived microsatellites and DNA extracted from fecal samples.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Behavioral observations
The study was carried out at the Ketambe Research Station, Gunung Leuser National Park, southeast Aceh, northern Sumatra, Indonesia. The site is approximately 450 ha large and is bordered on two sides by the Alas River and the Ketambe River. The area mainly consists of undisturbed, primary low-land rainforest (Rijksen, 1978
;
van Schaik and Mirmanto,
1985). Orang-utans have been studied at Ketambe since 1971
(Rijksen, 1978) and were
habituated by previous researchers. They are recognized individually, and the
life history of most animals has been well documented.
Most of the behavioral data were collected between January 1993 and October
1995 and consist of 8918 h of focal animal sampling
(Altmann, 1974). In addition,
data from previous studies on this same population have been used
(Rijksen, 1978;
Schürmann, 1982;
Schürmann and van Hooff,
1986; te Boekhorst et al.,
1990; Utami and Mitrasetia,
1995; Utami et al.,
1997) and cover 11 adult males who were observed to have been in
contact with females. Different individuals were followed simultaneously where
possible by different observers, and observation methods were
standardized.
We distinguished the following categories of flanged males: resident males
(seen regularly in the area, but not always as a dominant); dominant males
(were able to displace all other males in the area and were usually, but not
necessarily, resident); and nonresident males. The dominance status was
determined on the basis of interactions between males. Interactions can be
agonistic (avoidance, threat, chase, and fighting) and nonagonistic
(Utami et al., 1997). The
status of the males (unflanged and flanged) which were not excluded and their
sexual contacts with the females in our population are described in detail in
Utami (2000).
Figure 1 presents a summary of
male careers and offspring sired.
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We defined copulations as interactions between males and females that included at least one intromission. Forced copulations were initiated by a male and resisted by struggling, biting and/or screaming. Cooperative copulations involved nonresisting females and were initiated by either the male or the female.
We assume that the reproductive status of a female most directly influenced
her sexual activity as well as her preference for a specific partner.
Orang-utan females do not display patterns of sexual swelling, and it is
difficult to estimate time of ovulation. It is only a few weeks after
conception that a pregnancy-related swelling of the labia is observed
(Schürmann and van Hooff,
1986). The nearest approximation to the reproductive stage, in our
case, is the presence and age of offspring. Because we know that the
interbirth interval is approximately 8 years
(Galdikas and Wood, 1990), we
assume that from 6 years after having given birth to a surviving offspring,
the females are potentially reproductively active again.
Sampling
Forty individuals were observed in Ketambe between 1972 and 1998: 16 males,
9 females, and 15 offspring. Between 1993 and 1998, a total of 90 fecal
samples were collected for 11 males (69% of those observed during this
period), 6 adult females (67%), and 11 offspring (73%), shortly after
defecation. The samples were stored in 90% ethanol. Precautions were taken to
avoid human contamination by using sterile gloves and implements.
DNA extraction
Fecal extractions were carried out in a class I microbiological safety
hood, using the QIAamp DNA Stool Mini Kit provided by Qiagen GMBH (Hilden,
Germany, catalogue no. 51504; Goossens et
al., 2000a). For each fecal sample, three DNA extractions were
carried out. The protocol is described in Goossens et al.
(2000a).
Microsatellite analysis
Eight human microsatellite loci tested on blood and tissue samples from
captive orangutans (Zoological Society of London Blood and Tissue Bank) were
used and shown to be polymorphic: two dinucleotide loci D2S141 and D17S791,
and six tetranucleotide loci D1S550, D3S1766, D4S243, D5S1457, D5S1470 and
D12S375 (Table 1; see also
Coote and Bruford, 1996;
Gerloff et al., 1999;
Goossens et al., 2000b;
Launhardt et al., 1998). All
forward primers were fluorescently labeled. All polymerase chain reactions
(PCRs) were carried out in a total volume of 12.5 µl reaction mix
containing 2.5 µl DNA extract. We conducted a multiple-tube procedure for
each fecal extract according to Taberlet et al.
(1996; see also
Constable et al., 2001;
Gerloff et al., 1999;
Kohn et al., 1999;
Launhardt et al., 1998). For
each extract and each locus, three amplifications were performed
(Goossens et al., 2000a).
After that, the most successful extract (three positive PCRs) for each sample
was reamplified seven times to confirm genotypes and avoid typing errors (see
Taberlet et al., 1999, for a
review), even if three heterozygotes were obtained after three PCRs. This
procedure gives a 99% genotype confidence level (10 independent PCRs;
Taberlet et al., 1996).
Amplifications were carried out in a solution of 12.5 µl 10 mM Tris-HCl (pH
9.0), 200 mM (NH4)2SO4, 50 µM each dNTP,
1.5 mM MgCl2, 5 ng of bovine serum albumin, 0.1 U Amplitaq®
Gold DNA polymerase (Perkin Elmer), 0.5 µM nonfluorescent reverse primer,
0.5 µM fluorescent (TET, FAM or HEX) forward primer, and 2.5 µl of DNA
extract. A PCR amplification of 50 cycles was carried out (initial
denaturation 94°C for 10 min, 94°C for 15 s, 45°C to 52°C for
15 to 30 s, 72°C for 30-60 s). The annealing temperature was optimized for
each locus (Table 1). All PCR
products were separated on an acrylamide gel using an ABI PRISM 377 DNA
sequencer. We analyzed gels using GeneScan Analysis 2.0 and Genotyper 1.1
software.
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Data analysis
We analyzed paternity in two different ways. First, using the exclusion
method, potential fathers (males that were present in the study area during
the period of conception and from whom a genetic sample was obtained) were
excluded if they did not possess an allele in the offspring which it could not
have inherited from its mother. If all potential fathers are tested and if
sufficient markers have been included, all but one male, the father, can be
excluded. The probability of exclusion was calculated using the method of
Chakraborty et al. (1988) and
was implemented using POPASSIGN 3.8 (Funk SM, Zoological Society of
London).
The second paternity assessment method was inclusion. For this analysis, we
used the program CERVUS 1.0 (Marshall et
al., 1998), which was also used to assess the possible occurrence
of null (nonamplifying) alleles that could result in false paternal
discrepancies. This program identifies the most likely father from a panel of
potential fathers by correlating the genotypes of the males to the most likely
genotype of the father (see, e.g., Coltman
et al., 1998; Constable et
al., 2001; Gerloff et al.,
1999; Kohn et al.,
1999; Nesje et al.,
2000; Rossiter et al.,
2000). With this method a potential father can also be implicated
if not all potential fathers have been sampled or if the number of loci is not
sufficient to exclude all males who are not the father. We assessed males that
were candidates for paternity of each offspring from frequency of sightings
during the period when each offspring was conceived and averaged six males per
offspring. Estimations from field observations suggest that approximately 70%
of males were sampled. The proportion of loci typed (0.95) and the loci
mistyped (0.01) are average values across eight loci. We estimated the rate of
typing error from mother—offspring mismatches. Paternities were assigned
using CERVUS 1.0 at levels of 95% confidence, and 10,000 paternity simulations
were generated.
Relatedness between flanged males and unflanged males living in the same
area were calculated using the program Kinship 1.3
(Queller and Goodnight, 1989).
Relatedness values may vary from +1 (identical twins) through 0 (average
relatedness in the population) to -1 (originating from another gene pool). We
tested the hypothesis that the unflanged males were unrelated to the flanged
male by comparing their relatedness against the hypothesis that the unflanged
males were sons of the flanged males (r = 0.5). We also calculated
relatedness between non-excluded father—offspring,
one-locus—excluded father—offspring, mother—offspring,
father—mother, all mature males, adult females, and all individuals.
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RESULTS |
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Genetic analysis
We genotyped 11 potential mother—offspring pairs and 11 potential fathers. The number of alleles per locus ranged from 4 (D5S1457) to 8 (D2S141), and expected heterozygosities ranged from a minimum of 0.58 (D5S1457) to a maximum of 0.78 (D5S1470; Table 1). The estimated frequency of null alleles was 0.021. Allelic dropout and false alleles (Taberlet et al., 1996
,
1999) were identified in two
individuals, and additional PCRs on two other extracts were performed to
assess the true genotype for a heterozygous individual. Homozygous individuals
for a locus were assessed only if seven independent PCRs detected the same
allele for a particular extract. All 11 offspring analyzed contained fully
compatible multilocus genotypes with their known mother. The results are summarized in Table 2. Each offspring is compared with each male in terms of the number of loci at which the male is excluded, and the paternal exclusion probability is given for the non-excluded father and the one-locus—excluded males. The log likelihood inference (LOD score) of paternity is also given in Table 2. The LOD score value is the highest for 7 of the 10 included fathers. We found the following mean pairwise relatedness estimates and standard errors: mother—offspring, 0.613 ± 0.051; father—offspring, 0.521 ± 0.061; one-locus—excluded father—offspring, 0.221 ± 0.072; included father—mother, 0.080 ± 0.081; all potential fathers, -0.09 5 ± 0.081; all males (flanged and unflanged), -0.091 ± 0.030; adult females, -0.108 ± 0.070. Relatedness values between the two dominant/resident flanged males "Jon" and "Nur" and the unflanged males are also indicated in Table 2.
Paternity and relatedness
Paternity analysis implicated a single male in 10 out of 11 cases. In six
of these cases an unflanged male was implicated as the father, and in four
cases a flanged male was implicated. Of the seven cases where consorting males
were observed, in four cases the consorting male was indicated as the father,
and in three out of these four cases the father was an unflanged male (see
behavioral data in Table 2). It
was not possible to include all males that might have had sexual interactions
with the females (some males who were present at the time of the conceptions
were no longer present at the time of genetic sampling and, moreover, females
may have ranged outside of the monitored area and mated with unknown males).
Jon was the resident/dominant flanged male at the time of the conception for
four of the sampled offspring. However, he was excluded as father for three of
the offspring by at least two loci. Of the 11 potential fathers in our study,
three were flanged males, and two of these fathered offspring during their
tenure (Jon dominant > 15 years; Nur dominant < 5 years). In the four
cases of conception that occurred when the male dominance relationships
appeared to be unstable, unflanged males fathered all offspring.
In Table 2, the Queller-Goodnight relatedness values are given between the two dominant/resident flanged males Jon and Nur and the unflanged males. Relatedness between Jon and all the unflanged males found in the study area and between Nur and Aldo (flanged and unflanged males, respectively, from the same territory) were significantly lower than 0.5; and for some unflanged/flanged male pairs, relatedness values were strongly negative (Jon/Aldo, r = -0.160; Jon/Boris, r = -0.177; Boris/X, r = -0.292). None of the values were significantly different from unrelated (r = 0; Table 2). Mean relatedness values for all adult males (-0.095) and all adult females (-0.108) are negative, showing that both adult males and adult females are mostly unrelated in our population.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Six out of 10 tested offspring could be attributed to three of the unflanged males and just four offspring to three flanged males. How do these results correspond to the predictions of the three hypotheses?
First, the hypothesis that resident flanged males are postreproductive
guardians of a territory inhabited by male relatives can be rejected because
flanged males are the most likely fathers of about half of the offspring.
Furthermore, the relatedness between the flanged males and the unflanged males
present in the area at the time of conception of the offspring does not
support this hypothesis. Boris, an unflanged male, fathered three offspring
during Jon's tenure (a flanged male). The estimated relatedness value between
Jon and Boris was -0.177, a value significantly lower than 0.5, but not
significantly different from 0. Thus we may conclude that Jon and Boris are
not closely related. The range-guardian hypothesis also implies that males
must be comparatively philopatric, or, when migrating between habitats, that
certain unflanged males migrate in coordination with an adult male
(van Hooff, 1995). The mean
pairwise relatedness values for all adult males (-0.091 ± 0.030) and
for all adult females (-0.108 ± 0.070) suggest that females may be more
unrelated than males are, although the difference is not significant. This
finding does not support the hypothesis that maturing females tend to remain
in their natal area, whereas males disperse
(Rodman, 1973). These
relatedness values for both sexes do, however, reflect records for Ketambe
that suggest dispersal by both sexes.
Second, the female choice model in which fertile females have an exclusive
preference for flanged males, and therefore unflanged males never father
offspring, can also be refuted. The finding that unflanged males are
responsible for about half of the tested offspring shows that flanged males do
not have a reproductive monopoly. The female choice model cannot be maintained
in its most strict form; however, the role of female choice cannot be
rejected. This model was based on the consideration that a dominant flanged
male could never fully control access to the females, given the large size of
home ranges, the dense character of the forest habitat, and the cryptic
fertility of females. Thus, other males would still have an opportunity to
gain access to a female. This applies particularly to unflanged males, who
refrain from making their whereabouts known by producing long calls
(Mitani, 1985b) and who are
able to roam, often without provoking aggression from flanged males. However,
if females did not exert a preference for flanged males, it would be difficult
to see how flanged males could obtain the reproductive advantage required to
maintain such costly traits.
Alternative male mating strategies have been demonstrated for mammals,
birds, and fish. In Antarctic fur seals (Arctocephalus gazella),
holding a land-based territory was expected to confer a reproductive advantage
to males. However, a recent study has shown that at least 70% of the pups born
in the study site in a given year are not fathered by males who held a
territory or were observed copulating with females in the previous year
(Gemmell et al., 2001). This
implies that a pool of males exists that seldom venture ashore at this site.
The authors suggested that female choice is an integral component of the
Antarctic fur seal mating system and that aquatic mating may be an alternative
mating strategy in this species.
In the ruff, two different adult male morphs coexist
(van Rhijn, 1983). Hugie and
Lank (1997) have presented a
model in which female choice favors the evolution and maintenance of
alternative mating strategies. Resident males establish and defend courts on
leks against other residents, while nonterritorial satellite males move
between leks and among courts on a lek. The analysis suggested that the
resident—satellite relationship is fundamentally a cooperative
association favored by female choice, and in this polyandrous system
territorial males have been shown to gain the majority of paternities (Burke
T, personal communication).
In the long-tailed manakin (Chiroxiphia linearis), Trainer and
McDonald (1995) highlighted a
relationship between song performance and courtship success in this lek-mating
species. Teams of male manakins form cooperative partnerships consisting of a
dominant alpha male and a beta male partner with a variable number of
subordinate affiliates. The song performance of each male may provide
information useful to females in assessing a potential mate's ability to form
a cooperative, long-term partnership. The alpha male is responsible for
virtually all mating, whereas the beta male assists in the courtship displays.
McDonald and Potts (1994)
showed that alpha and beta partners are not relatives. Long-delayed benefits
to beta males are demonstrated including rare copulations, ascension to alpha
status, and female lek fidelity (McDonald
and Potts, 1994).
The bluegill sunfish (Lepomis macrochirus) shows two male
alternative reproductive strategies, wherein heteromorphic males specialized
for parasitism or for parental care coexist
(Gross, 1991). All these
examples highlight that female choice and cooperative breeding may have
influenced the evolution of bimaturism or dimorphism and alternative
reproductive strategies in some animal species, and still may give the
opportunity for beta males to access females.
The alternative mating strategies of unflanged males may confound the
effects of direct male—male competition. Peripheral, young, or
subordinate males of other primate species are also known to engage in
alternative mating strategies. In Japanese macaques (Macaca fuscata
fuscata), Soltis et al.
(1997) showed quantitative
evidence that (1) female choice can weaken the observed effects of
male—male competition, and (2) when in conflict with male—male
competition, female choice can be the stronger predictor of male reproductive
success. In Japanese and rhesus macaques, dominant males form long-term mating
series with females, but subordinate males form short-term, sometimes furtive,
mating series with females (Berard et al.,
1994; Huffman,
1992; Manson,
1996).
In wild patas monkeys (Erythrocebus patas), direct observation
showed that only 31% of matings were performed by the resident male in a
multi-male situation with three subordinate males in the group. In a one-male
group (harem), the tenured male accounted for all matings. Paternity
discrimination by DNA typing revealed that 50% of infants were sired by
outsider males in a one-male situation, and that 20% of the infants were sired
by intruder males directly after following take-over of a group by a new
resident male. Finally, sneaky mating by females with outsider males or
subordinate males was initiated by the females
(Ohsawa et al., 1993).
Gerloff et al. (1999)
demonstrated that in bonobos, reproductive success is biased in favor of
high-ranking males, even though these do not necessarily show the highest
copulation rates, but several studies suggest the existence of alternative
male competitive tactics also in great ape species (see
Smuts, 1987, for a review). In
chimpanzees, alpha males monopolize estrous females through possessive
behavior within groups, and non-alpha males mate opportunistically within
groups and form prolonged sexual consortships away from other males
(Hasegawa and Hiraiwa-Hasegawa,
1983; Tutin,
1979). However, Gagneux et al.
(1997) showed that half of the
infants born in a chimpanzee community were sired by males from outside the
group, even though extra-community copulations had not been observed. In
mountain gorillas, Robbins
(1999) showed that although
the dominant males in two studied groups participated in the largest
proportion of matings, they did not monopolize mating behavior.
In orang-utans, behavioral observations show that females consort with
flanged males and engage in cooperative copulations, especially with the
dominant or resident male, whereas they often resist the forced copulations of
unflanged males (Galdikas,
1985b; Schürmann and van
Hooff, 1986). We observed that in the Ketambe population,
reproductive females prefer flanged males. They do so especially during phases
of stability in the male hierarchy (Utami,
2000). However, in this population, unlike the one studied by
Galdikas (1985b), some females
occasionally also choose unflanged males. During periods of male rank
instability such mating became more common. During such periods, in fact, both
flanged and unflanged males engaged in matings with reproductive and
nonreproductive females. Matings with unflanged males were not only more
common, but also they were often not resisted by females. In our results, four
out of six offspring sired by unflanged males were conceived during such
periods of instability in male rank when dominant males were not present (see
Figure 1). It is possible that
only certain unflanged males may be successful. Although numbers are
necessarily small, our results suggest that all reproductively successful
males except for one were residents and not part of the considerable
population of "floating" males
(te Boekhorst et al., 1990).
This lends support to the suggestion by van Schaik and van Hooff
(1996) that individual pair
bonds might exist.
Recent studies suggest that male dominance is not always attractive to
females and that it does not necessarily predict superior parental quality,
good genes, or other forms of benefit to females (in birds such as the
pheasant, the pintail duck, the house sparrow; insects such as the field
cricket; amphibians such as the tiger salamander; and fish such as the sand
goby and the three-spined stickleback; for a review see
Qvarnström and Forsgren,
1998). When traits selected by male—male competition do not
reflect overall mate quality, females are expected to use other choice
criteria and might occasionally prefer subordinate males
(Qvarnström and Forsgren,
1998). Thus females may engage in durable relationships with
certain familiar unflanged males, possibly as an investment for when these
become dominant flanged males
(Schürmann and van Hooff,
1986).
Whether females find the full secondary sexual characters of flanged males
more attractive is currently unknown. Utami
(2000) demonstrated that
relationships between males depend on the presence of potentially reproductive
females, and an absolute intolerance between flanged males has been observed.
This reflects the strong contest competition between flanged males for access
to females (Mitani, 1985a; van
Hooff and van Schaik, 1995). This is in contrast with the comparatively
peaceful relationships observed between flanged and unflanged males (Utami et
al., in press). This means that flanged males are unable to prevent unflanged
males from contacting females, even though unflanged males appear to engage in
sexual interactions with the females regularly. Such tolerance would be
understandable if unflanged males were reproductively less successful, which
is not the case in our study, or if female choice for unflanged males under
certain circumstances would make intolerance less effective. The genetic
results and observations suggest that the unflanged phase represents a
specific, alternative male strategy which is extended when a dominant flanged
male is in the area (van Hooff,
1995). A similar dimorphism within males has been described for
another solitary primate, the lesser bushbaby (Galago senegalensis).
Older and heavier "A-males" have territories and preferential
social contacts with the females living in their territories and are highly
intolerant of other A-males. A-males are much more tolerant toward the lighter
B-males, which roam their territories. A high-ranking B-male can quickly
become an A-male once a territory becomes available
(Bearder, 1987).
Seemingly in contrast to our present findings in orangutans, but in a
group-living species, mandrills (Mandrillus sphinx), which also
exhibit adult male bimaturism, Wickings et al.
(1993) demonstrated, in a
semi—free-ranging group, a strong relationship among adult male
secondary sexual development, social dominance, and reproductive success. This
result is more in accordance with other studies, such as on wild long-tailed
macaques (Macaca fascicularis), where the high-ranking males father
the majority of offspring (de Ruiter et
al., 1994). It is also more in accord with a study on Sulawesi
crested black macaques (Macaca nigra), where adult females sexually
solicit high-ranking males more often than low-ranking males, but frequency of
copulation is not correlated with dominance rank
(Reed et al., 1997). All these
studies concern social species, which live in uni- or multi-male groups.
Orangutans, however, are solitary, and in that situation, two alternative
strategies, maintained by frequency-dependent selection (e.g.,
Brockman et al., 1979), may be
more feasible because monopolization of females by males is more difficult.
These could be (1) a sitting, calling, and waiting strategy of flanged males
who would rely on female choice in relation with their SSCs and long calls and
(2) a going, searching, and finding strategy of unflanged males with low costs
from aggression but higher costs of finding and persuading females (Galdikas,
1985a,b;
Utami, 2000). That the going,
searching, and finding strategy might be successful as an alternative is
suggested by the fact that a resident unflanged male had three offspring, the
first of which was conceived more than 20 years before he finally became a
flanged male (see Figure 1).
Some males may never reach this stage, yet may be reproductively
successful.
One possible complicating factor associated with these data is that in the early 1970s Ketambe was used as a rehabilitation station. When it was determined that it was problematic to introduce rehabilitants into a healthy population, these rehabilitants were recaptured and translocated. However, two of the rehabilitants, the females Binjei and Getti, could not be recaptured. Two of the six offspring assigned to an unflanged male have an ex-rehabilitant female as a mother and two have the daughter of a rehabilitant female as a mother (Kelly and Chris). There remains, therefore, the possibility that these unexpected paternities result from unusual sexual behavior of these females. However, two offspring (Eibert and Puji) fathered by unflanged males, Boris and X, respectively, have non-rehabilitant females as mothers, Pluis and Elisa, respectively.
Finally, although the data in this study concern a population that has been studied for many years, they involve a species with extremely slow demographic dynamics, and as a result sample sizes are always likely to be small. A caveat, therefore, is that an element of demographic stochasticity may bias these data, which should be regarded as information which ultimately needs to be augmented with data from continued study and from comparable sites.
|
ACKNOWLEDGEMENTS |
|---|
We thank T. Burland and M. Bayes for discussions during the development of the fecal extraction protocol and S. M. Funk for providing his program POPASSIGN 3.8. We are grateful to the Indonesian Institute of Science (LIPI) for granting permission to do research in Indonesia and to Universitas Nasional and Leuser Management Unit for sponsoring the project. The directorate general of Nature Conservation and Forest Protection (PHPA) gave permission to do the work in Gunung Leuser National Park. This study was supported by Leverhulme Trust (grant no. F/390/U), by the Royal Society of London (grant no. 20106), by the Zoological Society of London, by Cardiff University, and by a grant from the Universiteit Utrecht and the Lucie Burgers Foundation, Arnhem.
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