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Primates

, Volume 59, Issue 2, pp 127–133 | Cite as

Reproductive success of two male morphs in a free-ranging population of Bornean orangutans

  • Tomoyuki Tajima
  • Titol P. Malim
  • Eiji Inoue
Special Feature: Original Article Research and Conservation of Orangutans (Pongo sp.) in Malaysia

Abstract

The reproductive success of male primates is not always associated with dominance status. For example, even though male orangutans exhibit intra-sexual dimorphism and clear dominance relationships exist among males, previous studies have reported that both morphs are able to sire offspring. The present study aimed to compare the reproductive success of two male morphs, and to determine whether unflanged males sired offspring in a free-ranging population of Bornean orangutans, using 12 microsatellite loci to determine the paternity of eight infants. A single flanged male sired most of the offspring from parous females, and an unflanged male sired a firstborn. This is consistent with our observation that the dominant flanged male showed little interest in nulliparous females, whereas the unflanged males frequently mated with them. This suggests that the dominant flanged male monopolizes the fertilization of parous females and that unflanged males take advantage of any mating opportunities that arise in the absence of the flanged male, even though the conception probability of nulliparous females is relatively low.

Keywords

Paternity analysis Male dominance Bimaturism Bornean orangutan Pongo pygmaeus Free-ranging population 

Introduction

In most mammals, males compete to fertilize reproductive females (Trivers 1972), and previous studies of social primates suggest that dominant males usually have more access to fertile females and sire more offspring than subordinate males (Altmann 1962; Cowlishaw and Dunbar 1991; Kutsukake and Nunn 2006). However, genetic analyses have revealed that the most dominant male is not always the most successful sire (Ellis 1995; Majolo et al. 2012) and dominant males’ monopolization of fertilization can be reduced by female estrus synchrony, the number of rival males (Kutsukake and Nunn 2006; Ostner et al. 2008), and the alternative reproductive tactics of subordinate males (Setchell 2008).

Unlike other great apes, wild orangutans lead a semi-solitary lifestyle (Delgado and van Schaik 2000). Orangutans are characterized by male bimaturism, a phenomenon in which sexually mature males exhibit intra-sexual dimorphism and that might have evolved as a result of intense male–male competition (Utami Atmoko et al. 2009a). In this system, the dominant morphs, which are called “flanged males” (FLMs), have large bodies and fully developed secondary sexual characteristics, including prominent cheek pads, long fur, and a throat sack, whereas the subordinate morphs, which are called “unflanged males” (UFMs), have skeletally mature female-sized bodies and lack secondary sexual characteristics (Delgado and van Schaik 2000). In addition to their contrasting morphology, the two male morphs also exhibit different social behavior (Utami Atmoko et al. 2009a). For example, FLMs are highly competitive, as evidenced by wounds on their faces and bodies (Utami Atmoko et al. 2009a), whereas UFMs are usually more tolerant, thereby obscuring the dominance relationships among UFMs (Utami Atmoko et al. 2009a).

Previous studies have also reported that the dominant and subordinate orangutan morphs also differ in their mating behavior. For example, FLMs primarily copulate during their consortship with females (Galdikas 1985a; Mitani 1985), whereas UFMs often perform forced copulations (Galdikas 1985b; Mitani 1985) and often do so in the absence of FLMs (Utami Atmoko et al. 2009b). These observations suggest that FLMs sire more offspring than UFMs. However, it has been reported that both male morphs can sire offspring (Utami et al. 2002; Goossens et al. 2006), and paternity studies have reported that almost half of Sumatran orangutan offspring are sired by UFMs, whereas most Bornean orangutan offspring are sired by FLMs (Utami Atmoko et al. 2009b). Banes et al. (2015), who sampled a mixed population of wild-born and ex-captive Bornean orangutans, also reported that a dominant FLM sired most of the population’s offspring.

However, orangutan paternity studies have been based on molecular genetic analyses and have generally lacked behavioral observation. In addition, Utami Atmoko et al. (2009b) pointed out that UFMs sire most firstborn offspring in Sumatra. Yet, this has never been investigated in Bornean orangutans, and the paternity studies that have been conducted in Borneo (e.g., Goossens et al. 2006; Banes et al. 2015) provide no information regarding female parity or offspring birth order.

Accordingly, the present study aimed to compare the reproductive success of the dominant and subordinate male morphs in Borneo, and to determine whether the firstborn offspring of female Bornean orangutans are sired by UFMs. The present study focused on a free-ranging population that was primarily composed of rehabilitated orangutans in Kabili Sepilok Forest Reserve, because the females of the population have been regularly monitored and their parity has been documented. To complement the paternity analyses, the behavior of the males was also observed.

Methods

Study site

Sample collection and behavioral observation were conducted by the author TT with the help of local assistants in the Kabili Sepilok Forest Reserve (KSFR), which comprises ~ 4200 ha of lowland dipterocarp forest and harbors ~ 200 orangutans (Ancrenaz et al. 2005). The Sepilok Orangutan Rehabilitation Centre (SORC; 05°51.841ʹ N, 117°57.003ʹ E), which was established in 1964, is located adjacent to KSFR and has managed a rehabilitation project in which orphaned Bornean orangutans (P. pygmaeus morio) are rescued from the state of Sabah, Malaysia and then released into the reserve (Kuze et al. 2008). The SORC has established feeding platforms (Fig. 1), which the rehabilitated orangutans visit voluntarily, and supplies the orangutans with supplemental food (mainly bananas and sugarcane) twice a day (10:00 and 15:00 h).
Fig. 1

Kabili Sepilok Forest Reserve. a Location, b feeding platform in the reserve

Animals

The present study monitored eight adult orangutans (one FLM, three UFM, and four parous females) between December 2010 and August 2012. The age-sex class of the individuals was determined based on morphology (Wich et al. 2004; Kuze et al. 2005). Reliable information about the rehabilitated orangutans was obtained from the SORC studbook (Table 1). One of the UFMs (MK) and two of the parous females (MM and BR) were rehabilitated, and the other two parous females (MR and CL) were descendants of MM and BR. The origin of the other three adult males (CD, RG, and TK) is unknown. One of the population’s UFMs (MK) and one adult female (BR), along with her offspring, were translocated to another reserve in 2012.
Table 1

Information of subject individuals (N = 26)

Category

Studbook ID

Name ID

Sex

Year of agea

Date of birthb

Originc

Focal hour

DNA analyzed

FLM

CD

M

21a

Unknown, identified in 2010

43

Yes

UFM

PP412

MK

M

18

18-Dec-1994

Rehabilitated

150

Yes

RG

M

15a

Unknown, identified in 2007

204

Yes

TK

M

15a

Unknown, identified in 2010

41

Yes

Parous

PP249

MR

F

22

03-Feb-1990

Offspring of rehabilitated mother

265

Yes

PP505

MM

F

18

28-Nov-1996

Wild-born, rehabilitated

329

Yes

PP483

CL

F

14

19-Sep-1996

Offspring of rehabilitated mother

300

Yes

PP617

BR

F

12

27-Nov-1999

Wild-born, rehabilitated

151

Yes

Offspring

PP688

RN

M

6

07-Oct-2004

Firstborn offspring of MM

Yes

PP739

SL

F

0

01-Jun-2010

Offspring of MR

Yes

PP740

CH

M

0

10-Jun-2010

Offspring of BR

Yes

PP748

MM3

F

04-Dec-2011

Offspring of MM

Yes

PP749

CL3

F

13-Mar-2012

Offspring of CL

Yes

PP753

MO

M

13-Jan-2013

Offspring of MR

Yes

PP756

AW

M

27-Jul-2013

Offspring of CL

Yes

PP758

SP

M

20-Feb-2014

Offspring of AN

Yes

Nulliparous

PP655

TP

F

10

24-May-2002

Wild-born, rehabilitated

PP660

RS

F

9

27-Nov-2002

Wild-born, rehabilitated

Yes

PP658

HP

F

9

30-Aug-2002

Wild-born, rehabilitated

Yes

PP665

AN

F

8

25-Jan-2003

Wild-born, rehabilitated

Yes

PP725

OT

F

8

16-Oct-2007

Wild-born, rehabilitated

PP663

RSL

F

7

15-Dec-2002

Offspring of rehabilitated mother

PP677

CT

F

7

16-Dec-2003

Wild-born, rehabilitated

Yes

PP691

KR

F

7

28-Feb-2005

Wild-born, rehabilitated

Yes

PP719

GN

F

7

08-May-2007

Wild-born, rehabilitated

Yes

PP689

SG

F

6

23-Jan-2005

Wild-born, rehabilitated

aAge was estimated based on the definition provided by Wich et al. (2004)

bDate of birth was estimated by SORC at the first appearance

cData was derived from the studbook of SORC

The timing of each conception was estimated from the average gestation length (245 days; Graham 1988) and each offspring’s birth date, following Knott et al. (2010). Reproductive females were defined as those that lacked dependent infants and that failed to exhibit labial swelling, which only occurs during pregnancy (Delgado and van Schaik 2000). During our study, the adult males were also observed to mate with nulliparous females (6–10 years old), some of which were potentially fertile, since the age at first parturition in the SORC is 8–15 years (Kuze et al. 2008).

Sample and data collection

The behavior of the four adult males and four parous females was monitored during July–August 2010, December 2010–April 2011, and July 2011–August 2012. These periods encompassed three conceptions (MM3, CL3, and MO). Whenever possible, we followed the same animal from the morning to the night nest for a maximum of three consecutive days, in order to record sexual and agonistic interactions with other individuals. The behavior of the individuals was observed for a total of 1557 h (males: 438 h; females: 1045 h). During these observations, copulation was recorded when penile intromission was observed.

Genotyping and paternity analyses

We analyzed the paternity of 22 individuals, but we failed to collect DNA samples from four nulliparous females (TP, RSL, SG, and OT). From 2010 to 2014, 73 fresh fecal samples were collected from 19 individuals, which included eight mother–infant units (Table S1). However, three infants (CL3, MM3, and MO) had died before the non-invasive samples were taken. Therefore, we collected muscle and liver tissues from the postmortem specimens, with appropriate permissions from the SORC and Sabah Wildlife Department. Four adult males were genotyped as paternal candidates, although we were unable to collect samples from an FLM that had been occasionally observed in 2009. Following Wich et al. (2004), we estimated that the five young males were less than 14 years old at the time of each conception and thereby regarded them as adolescent and excluded them from the paternal analysis. To obtain DNA through non-invasive means, we swabbed the surface of feces from the individuals and then soaked the swabs in tubes that contained lysis buffer (Longmire et al. 1997). The DNA of fecal and post-mortem tissue samples was then extracted using the QIAamp DNA Stool Mini Kit (Qiagen, Valencia, CA, USA) and DNeasy Blood & Tissue Kit (Qiagen), respectively. Multiplex polymerase chain reaction (PCR) was performed as described in Inoue et al. (2007), using the QIAGEN multiplex PCR Kit (Qiagen). We then amplified 12 microsatellite loci (Goossens et al. 2006) from each of the DNA samples using two multiplex primer sets: multi1 (D2s1326, D3s2459, D5s1457, D12s375, D16s420, and D1s2130) and multi2 (D1s550, D4s1627, D5s1505, D6s501, D2s141, and D13s765). Because the non-invasive samples had low DNA contents, we needing to account for the low rate of DNA amplification and the resulting genotyping errors (Lampa et al. 2013). For accurate genotyping, homozygous and heterozygous alleles were scored after amplification in three and two independent PCRs, respectively (Lampa et al. 2013). Genotypes for all 12 microsatellite loci were obtained for 22 individuals (Table S1). We estimated the paternity of the offspring using CERVUS 3.0 (Kalinowski et al. 2007), with 10,000 simulations and confidence levels of 95% (relaxed) and 99% (strict).

Results

Paternity

Genotypes for all 12 microsatellite loci were generated for 22 individuals (Table S1), and paternity was determined for six of the eight offspring born during the study period (Table 2). No mismatches were observed between the offspring and expected sires at any locus. One FLM (CD) sired five non-firstborn offspring, whereas a UFM (RG) sired a firstborn offspring (SP). Another firstborn (RN) was sired by CD, who has been an FLM since 2010; no information regarding its morph and status in 2004 is available. We could not determine the paternity of two offspring (SL and CH) that were born in June 2010, and we failed to collect DNA samples from an FLM that was occasionally observed at the feeding platforms around the estimated timing of these two conceptions (i.e., October 2009).
Table 2

Results of paternity assignment at 12 microsatellite loci (N = 8)

Offspring

Date of birth

Birth order

Mother

Father

Morph

Number of mismatches with the next best male

Level of confidence (%)

Number of paternal candidates (number of sampled males)

FLM

UFM

RN

07-Oct-04

1st

MM

CD

unknown

4

99

1 (0)a

2 (0)b

SL

01-Jun-10

3rd

MR

unknown

3

1 (0)b

2 (2)

CH

10-Jun-10

2nd

BR

unknown

2

1 (0)b

2 (2)

MM3

04-Dec-11

3rd

MM

CD

FLM

3

99

1 (1)

3 (3)

CL3

13-Mar-12

3rd

CL

CD

FLM

2

99

1 (1)

3 (3)

MO

13-Jan-13

4th

MR

CD

FLM

5

99

1 (1)

2 (2)

AW

27-Jul-13

4th

CL

CD

FLM

5

99

1 (1)

2 (2)

SP

20-Feb-14

1st

AN

RG

UFM

4

99

1 (1)

2 (2)

aOne FLM and two UFMs were observed but samples could not be collected in 2004 (Kuze 2005)

bOne FLM occasionally appeared but samples could not be collected in 2009

Male agonistic interaction

We observed 22 cases of agonistic interactions among the four adult males. All of these interactions occurred in the presence of females, and male dominance relations were established on the basis of these dyadic interactions (Table 3). The FLM (CD) was always dominant over the UFMs, and linear dominance was observed among the UFMs. The FLM only exhibited aggression in the presence of reproductive parous females, whereas the UFMs competed for access to both reproductive parous and nulliparous females (Table 4).
Table 3

Results of agonistic interactions among males

Looser

 

CD

MK

RG

TK

Total

Winner

 CD (FLM)

5

3

3

11

 MK (UFM)

 

4

2

6

 RG (UFM)

  

5

5

 TK (UFM)

   

0

 Total

0

5

7

10

22

Table 4

Number of male–male aggression by reproductive status of females in proximity

Opponents

Status of females in proximity

Reproductive parous

Nulliparousa

FLM–UFM (10)

10

0

UFM–UFM (12)

10

2

aNo reproductive parous female was observed

Mating interaction

Forty-four copulations were documented during the study period (37 and seven in the male- and female-focal observations, respectively). The FLM copulated with parous females in two cases, and the UFMs also copulated with parous females in 21 cases, always in the absence of the FLM. However, the FLM was not observed to make any attempts to copulate with or inspect the genitals of nulliparous females, whereas the UFMs were observed to copulate with the nulliparous females in 21 cases, and all of the UFMs were observed to copulate with both reproductive parous and nulliparous females (Table 5). We also observed 136 cases of males inspecting female genitals, either by hand or mouth, and subsequent copulation occurred in 34 (25.0%) of these cases. The UFMs inspected nine nulliparous females and copulated with four of them, only one of which (AN) become pregnant during the study period.
Table 5

Number of successful copulations for each male and the partners’ parity

Male ID

Focal hour

Female parity

Parous

Nulliparous

CD (FLM)

43

2 (1)

0 (0)

MK (UFM)

150

4 (3)

7 (4)

RG (UFM)

204

14 (11)

13 (9)

TK (UFM)

41

3 (1)

1 (1)

Number in parentheses indicates forced copulation

Discussion

The purpose of the present study was to compare the reproductive success of Bornean FLMs and UFMs, and determine whether UFMs sired firstborn offspring. The paternity results of the present study are basically consistent with those of previous paternity studies in Borneo (Table 6) and suggest that dominant FLMs might be able to monopolize the fertilization of females within certain areas (Goossens et al. 2006; Banes et al. 2015). Even though it is possible that the rehabilitation project influenced the reproductivity of the animals through interactions with the human staff and with other rehabilitant orangutans, our paternity results are not different from those of previous studies. Our observations that all UFMs copulated with parous females when the FLM was absent and that only the UFMs mated with nulliparous females are also consistent with the observations of previous behavioral studies (Mitani 1985; Galdikas 1985a, b; Utami Atmoko et al. 2009b), which again suggests the rehabilitation project at the SORC has little impact on the mating interactions or offspring paternity of the studied orangutans.
Table 6

Comparison with previous paternity studies

Site

Species

Number of analyzed offspringa

Morph of father

References

FLM

UFM

Unknownb

Ketambe

P. abelii

10

4

6

Utami et al. 2002

Kinabatangan

P. pygmaeus morio

6

5

1

Goossens et al. 2006

Tanjung Puting

P. pygmaeus wurmbii

14

10

3

1

Banes et al. 2015

Sepilok

P. pygmaeus morio

6

4

1

1

This study

aCriterion for paternity assignment is different among studies

bPaternity could be assigned, but morph at the time of the offspring’s conception was unknown

As in Sumatra (Utami Atmoko et al. 2009b), the UFMs at the SORC sired none of the offspring born to parous females, even though we observed copulation between the two. A previous hormone study suggested that female Bornean orangutans might copulate with the most dominant male near the time of ovulation, thereby resulting in more conceptions when mating with the FLM (Knott et al. 2010). We observed that males at SORC performed frequent genital inspection, which might help to estimate the reproductive state of females (Knott et al. 2010). Furthermore, orangutan sperm cells have better-developed acrosomes than either chimpanzee or gorilla sperm cells, which facilitates conception (Fujii-Hanamoto et al. 2011). These studies may explain why the dominant FLM had the highest reproductive success and the UFMs did not.

The present study also provides new evidence for the siring of firstborn offspring (e.g., SP) by UFMs, as previously reported from Sumatra (Utami Atmoko et al. 2009b). Several researchers have reported that FLMs show little interest in nulliparous females (Schürmann 1981; Galdikas 1985a). Indeed, in the present study, the FLM did not attempt to either copulate with or inspect the genitals of any nulliparous female, whereas all of the UFMs copulated with nulliparous females, and some of them competed with one another for access in front of nulliparous females. In orangutans, nulliparous females are regarded as less fertile than parous females, owing to adolescent sterility (Galdikas 1995; Knott and Kahlenberg 2007), so the FLMs might focus their efforts on mating with parous females, whereas UFMs mate with all potentially reproductive females, including nulliparous ones (Utami Atmoko et al. 2009b). The latter conclusion is also supported by our observations that only the UFMs exhibited agonistic interactions in proximity to nulliparous females.

The tendency of subordinate males to mate with nulliparous females has also been reported in other African great apes. In eastern chimpanzees (Pan troglodytes schweinfurthii), for example, high-ranking males prefer to mate with older parous females (Muller et al. 2006), whereas low-ranking adult and adolescent males copulate more with nulliparous females (Watts 2015), which are regarded as less desirable mates (Wroblewski et al. 2009). In the multi-male groups of mountain gorilla (Gorilla beringei beringei), the most dominant males copulate more with parous females, whereas the subordinate males copulate more with nulliparous females (6–8 years old; Stoinski et al. 2009), which subsequently bear offspring (Nsubuga et al. 2008). Therefore, mating with nulliparous females is probably an alternative reproductive tactic.

Our observations of male agonistic interactions suggest that clear dominance relationships occur among the three UFMs, a finding which has not been reported by previous studies (e.g., Utami Atmoko et al. 2009a). It is possible that long-term interactions between ex-rehabilitants might influence the relationships among UFMs. However, owing to our study’s small sample size, we were unable to determine whether dominance rank affected the siring of firstborn offspring. Therefore, future studies should focus on the dominance relationships of UFMs, as well as the possible effects of such relationships on reproductive success.

Notes

Acknowledgements

We are grateful to Sabah Biodiversity Centre, Sabah Wildlife Department, and Economic Planning Unit of Malaysia Federal Government for permitting this study. We are also grateful to Dr. Noko Kuze, Dr. Henry Bernard, Dr. Vijay Kumar, Ms. Sylvia Alsisto, Mr. Sailun Aris, and all the staff of the Sepilok Orangutan Rehabilitation Centre for their kind support of our research activity in Sabah, Malaysia, and to Dr. Naofumi Nakagawa for helpful comments on our manuscript. The present study was supported by Grants-in-Aid for Japan Society for the Promotion of Science (JSPS) Research Fellow (Grant no. 10J01218 to Tomoyuki Tajima); JSPS Core-to-Core Program, Advanced Research Networks “Tropical Biodiversity Conservation” Wildlife Research Center, Kyoto University, Japan, and by the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Leading Graduate School Program in Primatology and Wildlife Science, Kyoto University, Japan. We obtained appropriate permission from the Sabah Wildlife Department and Sabah Biodiversity Council before conducting our research, and the study complies with current Malaysian laws, as well as with the “Guidelines for Care and Use of Nonhuman Primates” and “Guideline for field research of non-human primates” provided by the Primate Research Institute of Kyoto University, Japan.

Supplementary material

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Supplementary material 1 (DOCX 17 kb)

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Copyright information

© Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Human Evolution Studies, Graduate School of ScienceKyoto UniversityKyotoJapan
  2. 2.Sabah Wildlife DepartmentKota KinabaluMalaysia
  3. 3.Department of Biology, Faculty of ScienceToho UniversityChibaJapan

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