1195
The mating system of polar bears: a genetic
approach
E. Zeyl, J. Aars, D. Ehrich, L. Bachmann, and Ø. Wiig
Abstract: Parentage analysis data for 583 individuals genotyped at 27 microsatellite loci were used to study the mating
system of polar bears (Ursus maritimus Phipps, 1774) in the Barents Sea area. We discriminated statistically between full
and half-siblings identified through only one common parent. We document for the first time multiple paternity in polar
bears. We demonstrated for both sexes low fidelity to mating partners over time. We did not detect any significant difference between the age distribution of adult males at capture and the age distribution of males siring cubs. This might indicate that the male’s age and size are less indicative of the reproductive success than previously thought. This is further
supported by a rather long mean litter interval of 3.9 years for males siring several litters. The mating system of polar
bears in the Barents Sea appears to be promiscuous, usually with a single successful father siring full siblings within a
year, but with consecutive litters of a mother being fathered by different males. We discuss how population density, landscape characteristics, and adult sex ratio might influence the mating system of polar bears. This is of particular importance
for management decisions such as, e.g., implementing sex ratios in hunting quotas.
Résumé : Nous utilisons les résultats d’analyses de filiation portant sur 583 individus génotypés à 27 loci microsatellites,
afin d’étudier le système de reproduction des ours blancs (Ursus maritimus Phipps, 1774) de la région de la Mer de
Barents. Nous avons statistiquement discriminé entre les vrais-frères et sœurs et les demi-frères et sœurs identifiés par un
seul parent commun. Nous documentons, pour la première fois chez les ours blancs, un cas de parenté multiple dans une
même portée. Nous avons démontré une faible fidélité entre partenaires sexuels, lors de différentes reproductions, quel que
soit le sexe. Nous n’avons pas détecté de différence entre la distribution des âges des mâles adultes à la capture et la distribution des âges des mâles au moment où ils sont pères. Cela pourrait indiquer que l’âge des mâles et leur taille sont une
moindre indication du succès de leur reproduction qu’on ne le croyait. Cela est supporté par un intervalle moyen assez
long (3,9 ans) entre les portées pour les pères ayant engendré plusieurs portées. Nos résultats indiquent que le système de
reproduction des ours blancs de la mer de Barents semble lié à la promiscuité; ainsi, de manière générale, un mâle est le
père de tous les petits d’une portée, mais les portées successives d’une femelle ont des pères différents. Nous discutons
comment les variations de densité des populations et des caractéristiques du paysage, ainsi que le rapport des sexes des
adultes peuvent influencer le système de reproduction des ours blancs. Ceci est important pour les décisions de gestion des
populations, par ex. la fixation du rapport des sexes dans les quotas de chasse.
Introduction
Information about the mating system and the reproductive
biology of both sexes is important for wildlife conservation
and management. Mating systems can be viewed as different
degrees of female monopolization by males (Le Boeuf
1991). In species where males do not contribute to parental
care the main factor influencing the ability of males to monopolize receptive females, and hence the male reproductive
success, is the temporal distribution of receptive females.
The operational sex ratio (i.e., number of adult males per receptive female; OSR) and female spatial distribution are important factors when there is little estrous synchronization
(Ims 1988). In general, the spatial distribution of females is
Received 21 April 2009. Accepted 3 September 2009. Published
on the NRC Research Press Web site at cjz.nrc.ca on
4 December 2009.
E. Zeyl,1 L. Bachmann, and Ø. Wiig. Natural History
Museum, National Centre for Biosystematics, University of
Oslo, P.O. Box 1172 Blindern, NO-0318 Oslo, Norway.
J. Aars. Norwegian Polar Institute, NO-9296 Tromsø, Norway.
D. Ehrich. University of Tromsø, Department of Biology,
NO-9037 Tromsø, Norway.
1Corresponding
author (e-mail: eve.zeyl@nhm.uio.no).
Can. J. Zool. 87: 1195–1209 (2009)
closely associated with resources necessary for producing
and rearing the young (Davies and Lundberg 1984; Gehrt
and Fritzell 1998). Among marine mammals such as pinnipeds, the spatial and temporal distribution of females determine the mating system in that the degree of polygyny
(where males mate with the same restricted group of females in successive mating attempts; Clutton-Brock 1989)
varies with female clumping and estrous synchrony (Boness
1991). In land-breeding pinnipeds such as northern elephant
seals (Mirounga angustirostris (Gill, 1866)), the females are
spatially clumped. Accordingly, the mating system is highly
polygynous and the variance of lifetime reproductive success is estimated to be four times greater among males than
females (Le Boeuf and Reiter 1988; Le Boeuf 1991). The
mating systems of ice-breeding seals with spatially scattered
distribution of females are less well known (Le Boeuf
1991). Promiscuity such as in harp seals (Pagophilus groenlandicus (Erxleben, 1777); Kovacs 1995 in Kovacs et al.
1997) and slight polygyny or serial monogamy (where females (or males) usually mate with a single partner in successive breeding attempts during a single breeding season
but mate with several different partners during their lifetime;
Clutton-Brock 1989) such as in hooded seals (Cystophora
cristata (Erxleben, 1777); Boness et al. 1988; McRae and
Kovacs 1994) has been reported.
doi:10.1139/Z09-107
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1196
In many species, females may mate with several males
during a mating season (polyandry, where females mate
with the same restricted group of males in successive breeding attempts; Clutton-Brock 1989). In mammals, various
benefits have been hypothesized for such behavior, e.g., improvement of fecundity by confusing paternity and thus reduction of the risk of infanticide from the mating males
(Hosken and Stockley 2003), or avoidance of inbreeding
(Stockley et al. 1993). In pinnipeds, the multiple copulations
by females have been interpreted as an avoidance strategy
toward male harassment in periods when females are spatially clumped (Cassini 1999).
Mating with more than one male during an oestrus may
result in multiple paternity within a litter. Multiple paternity
is common in mammals (Baker et al. 1999; Burton 2002;
DeYoung et al. 2002; Crawford et al. 2008) and has also
been documented in several bear species, such as in American black bears (Ursus americanus Pallas, 1780; (Schenk
and Kovacs 1995; Sinclair et al. 2003). In Swedish brown
bears (Ursus arctos L., 1758), a minimum of 10 out of 69
litters (14.5%) were fathered by several males (Bellemain et
al. 2006a). However, the frequency of multiple paternity
may vary between (Baker et al. 1999; Burton 2002) and
within species, and may depend on population density (Say
et al. 1999). Multiple paternity is expected to be more common in species with synchronized oestrus and spatially clustered receptive females, making it more difficult for males
to monopolize individual receptive females (Clutton-Brock
1989; Isvaran and Clutton-Brock 2007).
Polar bears (Ursus maritimus Phipps, 1774) are solitary
marine carnivores. Their breeding season extends from
March to May (Lønø 1970; Tumanov 2001; Rosing-Asvid
et al. 2002). Most ovulations are believed to occur in April
and May (Rosing-Asvid et al. 2002) and the oestrus is thus
not synchronous. Female polar bears enter oestrus every 2 or
3 years after weaning off their offspring (Ramsay and Stirling 1986; Derocher and Stirling 1998), or after they have
lost their offspring before weaning (Ramsay and Stirling
1986). Polar bears live in a highly unstable environment;
sea-ice extent and characteristics are constantly changing
under the influence of temperature, wind, and sea currents
(Ferguson et al. 1998). Females in oestrus are not particularly clustered, but their distribution is considered to be determined by foraging opportunities. Males may be
distributed with the same relative densities as solitary females (Ramsay and Stirling 1986). The mating success of
female polar bears may depend both on the OSR and on the
density of available breeding males (Molnár et al. 2008). In
an area such as the Barents Sea with moderate or high densities of polar bears and where hunting is prohibited (Aars et
al. 2009), it is unlikely that lack of opportunity to find a
male partner restricts female reproduction.
Depending on social and ecological conditions, the timing
of first reproduction might be delayed well beyond sexual
maturity (Say et al. 1999). Male polar bears attain 97% of
their asymptotic body mass at approximately 13 years of
age (Derocher et al. 2005). Although age of maturity is
about 5 years, it is expected that middle-aged males will
have preferential access to females owing to increased competitiveness (Bunnell and Tait 1981; Ramsay and Stirling
1986). In addition, most polar bear populations are harvested
Can. J. Zool. Vol. 87, 2009
by indigenous people, and harvest is usually male-biased
(Derocher et al. 1997). Removal of problem bears is also
typically male-biased (Dyck 2006). In a long-term perspective, this could result in a lack of sexually mature males in
the population, which could impair fecundity (McLoughlin
et al. 2005; Taylor et al. 2008). Knowing how reproductive
success of males varies with age would prove valuable to
population dynamics modelling and management.
In the present study, we use genetic and parentage data
from the Barents Sea to gain information about the mating
system of polar bears, which is currently known only from
behavioral observations (Ramsay and Stirling 1986; Wiig et
al. 1992; Rosing-Asvid et al. 2002). First, we assess evidence for multiple paternity. Traditional methods to detect
multiple paternity require either that both parents are identified or that incompatible alleles are assessed within litters
consisting of at least three siblings (Burton 2002; Bellemain
et al. 2006a; Crawford et al. 2008). Here, two statistical
likelihood approaches were applied in addition to the traditional method (Bellemain et al. 2006a) to discriminate between half-siblings (HS) and full siblings (FS) within litters.
These methods were employed to discriminate between HS
and FS identified by at least one common parent (father or
mother) assigned through parentage analysis. Considering
the male-biased OSR in the Barents Sea population and earlier observations of females consorting successively with
several males (Wiig et al. 1992), we expect multiple paternity to occur. However, taking into account the long breeding period and the unpredictability of the spatial distribution
of females during the mating season owing to large temporal
changes in distribution of sea ice, multiple paternity may
also be relatively rare. Second, we investigate to which degree polar bears breed with the same mate in different years.
We also estimate the time span between litters sired by the
same male. Intense wounding and scaring (Ramsay and Stirling 1986) of males during the breeding season certainly indicates high male competition for mating opportunities.
Young males are hypothesized to have lesser competitive
abilities than older males (Ramsay and Stirling 1986) and to
be less attractive for females (Derocher et al. 2005). We
consequently expect low fidelity between mating partners
and a short time span between litters sired by reproductively
succesful males. Furthermore, we expect a propensity of
males siring litters to be older than the mean age of adult
males at capture. Finally, we compare the accuracy of the
different methods employed for discriminating between HS
and FS relationships.
Materials and methods
Study area, animal sampling, laboratory procedures, and
parentage analysis
The Barents Sea population of polar bears has been defined as the animals occupying the area between longitudes
of 108E and 608E, and latitudes of 728N and 838N (Wiig
and Derocher 1999); an area that belongs to Norway and
Russia. The population has been protected from harvesting
since 1973 (Prestrud and Strirling 1994). The mean density
of polar bears in the Barents Sea area is moderate to high
(1.1 bear per 100 km2 in August 2004) compared with
mean densities reported in several other surveyed areas, but
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Zeyl et al.
local density varies considerably (Aars et al. 2009). The
present study is based on animals captured during spring in
the years 1995–2006. A detailed description of the study
area and the sampling procedure was provided elsewhere
(Wiig 1995; Zeyl et al. 2009). The animal-handling methods
used had previously been granted approval by the Norwegian Animal Health Authority (Oslo, Norway).
The laboratory methods and basic population genetics
analysis tools used in this study have been previously described (Zeyl et al. 2009). In brief, DNA was isolated from
tissue samples following a standard chloroform–phenol protocol for 151 samples (Sambrook and Russell 2001) or the
manufacturer’s instructions of the DNeasy tissue kit
(Qiagen, Hilden, Germany) for 432 samples. Twenty-seven
bear-specific polymorphic microsatellite loci (Crompton et
al. 2008) were amplified in six multiplex polymerase chain
reactions for 583 samples and 126 blind replicates, i.e.,
21% of the samples. The mean error rate per locus was
0.004 (range = 0–0.045) for allelic dropout (ADO) and
0.005 (range = 0–0.023) for false alleles. Two of 89
mother–offspring pairs identified by field observations
showed one incompatibility each, which is likely to result
from the mistyping of adjacent alleles corresponding to an
estimated error rate of 8.3 10–5 per locus. Evidence for
significant scoring errors was not found when comparing
the consensus of 126 samples with the consensus of the 126
blind replicates. The mean number of alleles per locus estimated using GENALEX version 6 (Peakall and Smouse 2006)
was 8.04 (SD = 3.07, range = 2–15), the mean observed heterozygosity was 0.61 (SD = 0.24, range = 0.02–0.85), and
the mean expected heterozygosity was 0.62 (SD = 0.24,
range = 0.02–0.85). The level of resolution was high with
an estimated probability of identity of 6.74 10–23, following Paetkau and Strobeck (1994). The probability of identity
among siblings, accounting for the presence of relatives in
the data set, remained low (1.92 10–9), following Waits
et al. (2001). No individuals shared identical genotypes. Deviations from Hardy–Weinberg and linkage equilibriums
were tested for each locus using the GENEPOP version 3.4
software (Raymond and Rousset 1995). No deviation from
Hardy–Weinberg equilibrium was observed for the adult individuals (FIS = 0.003, p = 0.0798). There was no indication
that loci were physically linked (Zeyl et al. 2009).
We herein use the results of DNA-based parentage analyses from 583 individuals (309 females, 271 males, and 3
mislabeled samples for which the reference number did not
correspond to any individual in the field data; Zeyl et al.
2009), performed using the software Parente (Cercueil et al.
2002). To avoid the incorrect rejection of parentages, a maximum of three incompatibilities between parent–offspring
pairs was accepted. Even in the case of a low mean error
rate of only 1% over all loci up to 40.7% of erroneous genotypes can be expected, following Bonin et al. (2004). Parentage was assigned when the probability of being the true
parent was >0.5, a rather conservative cutoff value. In addition, two mother–offspring relationships were assigned because the mothers had been captured together with the cubs.
The respective probabilities of being the true mother in
these cases were low (0.2404 and 0.4802), but no genotype
incompatibility was observed. In all other cases of parentage
assigned with only low probability, we noted that several
1197
relatives of the parent–offspring pairs were included in the
data set, which might explain the low probabilities for assigning the true parent (Jones and Ardren 2003; Morrissey
and Wilson 2005). The mean probability of being the true
parent for assigned parentage was high (0.97 for mother–offspring and 0.96 for father–offspring). Relatedness between
individuals was computed using ML-Relate (Kalinowski et
al. 2006) on all genotyped individuals (n = 583). Allele frequencies were estimated with the software ML-Relate from
412 bears captured as adults, as these should represent the
reproductive part of the population.
Discriminating between full siblings and half-siblings
Directly assessing incompatible alleles within groups of
offspring (the traditional method) allows identifying HS
only in cases where three or more siblings were assigned to
a common parent (parent 1). If, in addition to the two alleles
from parent 1, three or more alleles were detected, this was
taken as an indication that the siblings were born from at
least two different parents of the sex opposite to that of the
parent 1 (i.e., that at least one of them was a HS). If no
more than two additional alleles were detected, this would,
however, not prove that the siblings were FS. Thus, the traditional method provides a minimum estimate of the number
of HS. We report the results of this method only for comparison with two other statistical methods that can be applied to
the entire data set.
The second method uses maximum-likelihood estimates
of relatedness and performs a statistical test based on simulated genotypes to assess the significance of the likelihood
ratio (LR) between the most likely relationship and an alternative relationship (Kalinowski et al. 2006). The pairwise
relationship tests are implemented in the software MLRelate (Kalinowski et al. 2006). For each pair of siblings
we tested either FS against HS or HS against FS, depending on which relationship had the highest likelihood.
The p value of each hypothesis was computed using
100 000 simulated genotypes. If the p value was £0.05,
we accepted the relationship with the highest likelihood;
otherwise we considered the relationship as uncertain.
The third method uses also LRs to compare the evidence
for two alternative relationship hypotheses (Mayor and
Balding 2006). It differs from the ML-Relate method by taking into account the genotype of the assigned parent when
computing likelihoods. Analysis were run in R version 2.8.0
(R Development Core Team 2008). Mayor and Balding
(2006) showed that if the maternal genotype is known, only
22–24 loci are required to obtain misclassification rates below 2%, applying a decision rule based on LRs larger or
smaller than 1. We used a somewhat more stringent decision
rule, as our objective was to minimize the risk of erroneously accepting a HS relation when a FS relation is true.
Thus, individuals were considered FS when LRs were ‡2,
and HS when LRs were £0.5. Between those values, the relationship was considered uncertain.
In case of incongruent outcomes between the methods, we
accepted the results from Mayor’s method (method 3), as it
was considered more powerful (see comparison between the
methods below).
Rejecting the FS hypothesis for siblings from a litter implies multiple paternity. Rejection of the HS hypothesis for
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1198
siblings from different litters suggests that the mother had
mated successfully with the same male in different years.
Siblings were only attributed to the same litter when they
had been captured as dependent young with their mother.
When offspring were not captured as dependent young with
their mother, their estimated year of birth is uncertain (see
below). In such cases, assigning siblings as FS could indicate either that the siblings originated from a single litter or
that repeated mating between the same partners occurred in
different years.
None of the used methods accommodates for genotyping
errors. Thus loci, at which offspring showed incompatibility
with their assigned parent owing to erroneous genotyping
(such as, e.g., allelic dropout), were removed from the analysis. Removed loci were UarMU50, G10C–UarMU61,
G10B, LIST11016–G10B, LIST11020, and G10C for individuals O6, O30, O33, O65, O77, and O79, respectively, in Table 1. Removed loci were G10D–G10P–G10B, LIST11020–
G10P, and LIST11020 for individuals O100, O105, and
O107, respectively, in Table 2. Missing loci owing to amplification failure were also excluded from the analysis with
Mayor’s method, as it does not allow for missing information. Excluded loci were UarMU61 for individual M36 in
Table 1 and UarMU50, G10D, UarMU10, and MSUT3–
G10H for individuals O28, F16, O119, and O120, respectively, in Table 2.
Both likelihood methods assume that neither of the two
individuals being compared are inbred. This appears to be a
reasonable assumption for the polar bear data set, as mating
can be considered random within the studied population (E.
Zeyl, J. Aars, D. Ehrich, L. Bachmann, and Ø. Wiig, unpublished data). The applied likelihood methods further assume
that no migrants are entering the population, in other words
allele frequencies do not change from one generation to the
next. The no-migrant assumption is likely to be violated.
However, we consider this only a minor bias because migrants are likely to originate from neighboring populations
with similar allele frequencies (Paetkau et al. 1999).
Age of males siring litters and time span between litters
Age was known with certainty only for bears captured as
dependent offsprings with their mother. For bears captured
later in life, age was estimated by the count of cementum
growth layers of a vestigial premolar tooth (Calvert and
Ramsay 1998) or in a few cases based on field observations
of body size and tooth wear. In the Barents Sea polar bears,
counts of cementum growth layers result in imprecise age
estimates; usually the age of younger bears (<7 years) is
overestimated, while the age of older bears (‡7 years) is
underestimated (Christensen-Dalsgaard 2006). Age estimates
based on count of cementum growth layers were available
for 544 samples. For 35 samples, age was estimated from
field observations (including 22 samples from which only a
minimum age estimate could be deduced according to the
categories adult, subadult, or cub, and year of capture). Age
estimates were lacking for four samples. In the present
study, the minimum age difference for parent–offspring
pairs was set to 4 years because this age has been reported
as the earliest age of female reproduction in the Barents Sea
population (Derocher 2005), and because males in the
Barents Sea population, according to Lønø (1970), can be
sexually mature at 3.5 years.
Can. J. Zool. Vol. 87, 2009
Sixty-one fathers were included to determine the age distribution of males siring cubs. The distribution of age at reproduction was compared with the distribution of age at
capture of 190 males that could potentially have been mating (‡4 years of age at capture; Fig. 1). When an adult
male had been captured several times, it was included several times in the age distribution of captured bears. Similarly, when a male had fathered several litters, it was
included several times in the distribution of age at reproduction. The males with several litters were used to estimate the
time span between successive litters.
Results
Multiple paternity and mate fidelity
From the total data set of the 583 individuals, parentage
analysis revealed 132 mother–offspring relations and 75
father–offspring relations (Zeyl et al. 2009). Twenty-six litters with two siblings and one litter with three siblings from
26 mothers were identified in the field and confirmed genetically (Table 1). For two additional litters observed with
their mothers in the field, genetic data were available only
for the cubs and not for the mothers. Consequently, only
the ML-Relate method could be applied for those two litters.
Both parents were assigned for eight litters. The 29 litters
were tested for multiple paternity (Table 1). Of those, 27 litters were confirmed to consist of FS. In one litter, the two
siblings were confirmed to be HS, showing a case of multiple paternity (M27; Table 1). Neither of the two fathers was
identified. Multiple paternity was likely also in one more litter, also with unidentified fathers. However, only Mayor’s
method supported the two siblings being HS in this case
(M36; Table 1).
Twenty females had two to four litters (consisting of one
to three offspring) hypothesized to be from different years.
Among those 20 females, it was certain that 1 female (M7)
reproduced with the same male in two different years (F8;
Table 1), as two of the offspring were captured in 2006 as
cubs, whereas the third sibling was captured in 2006 at an
estimated age of 4 years (cementum growth layers). It is
likely that two additional females (M38 and M39; Table 1)
had offspring from an identical but unidentified male in different years because two of their respective offspring (O87–
O89 and O90–O93), born in different years, turned out to be
FS. The age difference between offspring O87–O89 (5 years)
and O90–O93 (9 years) makes it unlikely that they were
born in a single litter. However, because of the uncertainty
of age estimates (Christensen-Dalsgaard 2006), this cannot
be firmly ruled out.
Among 17 males siring two to four offspring, 8 males had
several offspring (FS) born in the same year. In these cases,
the mother was identified genetically (M1–M8; Table 1) and
had also been observed with the cubs in the field. Twelve
males had sired two or three litters in different years. One
male certainly had offspring twice with the same female in
different years (F8 and M7; Table 2). If the offsprings’ birth
years were estimated correctly, another male is likely to
have reproduced with the same female in different years
(F17, estimated age difference between O117 and O118 was
4 years based on cementum growth layers; Table 2).
Published by NRC Research Press
Zeyl et al.
Comparison between the methods
Siblings for which both parents were assigned through parentage analysis allowed us to assess the accuracy of the two
statistical methods: ML-Relate and Mayor’s method. In one
case, ML-Relate erroneously classified a pair of HS as being
FS (O100 and O36, F9; Table 2). Mayor’s method did not
reach any incorrect conclusions with the applied settings for
acceptance. ML-Relate was inconclusive in three cases
where both parents were assigned (M4 and F3, M6 and F8,
M8 and F5, F6; Tables 1 and 2) and in one case where only
one parent was assigned (F8; Table 2). Mayor’s method was
only inconclusive in the M4–F3 case, when using the genotype of the mother (M4; Table 1) but provided a correct result when using the genotype of the father (F3; Table 2).
Overall, ML-Relate was inconclusive in 17 of 114 tests
(15%) and Mayor’s method was inconclusive in 3 of 126
tests (2%). Thus, we decided to rely on the results provided
by Mayor’s method in case of inconsistencies between
methods. In total, four inconsistencies between the two
methods were observed (Tables 1 and 2). The traditional
method did not reveal any contradiction with the results
shown by the two other methods. However, very little information was gained using this method, as it was only applicable in 11 siblings groups out of 41 defined through the
mother and in 7 siblings groups out of 17 from a common
father.
Mayor’s method was inconclusive for the siblings O91
and O92 (M39; Table 1); however, the LR was in favour of
FS (LR = 1.26). Mayor’s method was also inconclusive for
the siblings O52 and O53 (M21; Table 1). The LR was
slightly in favour of HS (LR = 0.9). In both cases, ML-Relate
concluded FS. For the siblings O7 and O8, the LR test was
inconclusive (LR = 0.59) when using the mother’s genotype
(M4; Table 1) but was strongly in favour of FS (LR = 956)
when using the father’s genotype (F3; Table 2). Thus, we accepted FS. In that case, the relatedness between the identified
parents was high (R = 0.19), possibly leading to the inconclusive outcome of one of the LR tests.
Both methods identified the case of multiple paternity
(M27; Table 1). The relatedness between the siblings was
R = 0.2317, which corresponds to what is expected for HS.
ML-Relate was not able to distinguish between HS and FS
for siblings O82 and O83 (PFS = 0.08; see M36, Table 1).
However, Mayor’s method indicated this was another case
of multiple paternity (LR = 0.3014). The relatedness between the siblings was high for HS with R = 0.4261. Thus,
we considered this case a likely multiple paternity.
Relatedness
The mean relatedness among the 583 genotyped bears
was R = 0.0428 (SD = 0.06, n = 169 653 pairwise comparisons). The mean relatedness between litter mates was close
to the mean expected relatedness for FS: R = 0.47 (SD =
0.013, n = 31 pairwise comparisons from 29 litters consisting of 28 duplets and 1 triplet). Offspring sharing the same
mother who were hypothesized not to originate from the
same litter had a mean relatedness of R = 0.28 (SD =
0.012, n = 56 pairwise comparisons), a value close to the
expected relatedness for HS. Confirmed FS had a mean relatedness of R = 0.486 (SD = 0.010, n = 33 pairwise comparisons). Identified reproductive pairs had a mean
1199
relatedness of R = 0.039 (SD = 0.049, n = 21 pairwise comparisons).
Incestuous mating
We revealed one case of incestuous mating. F18 successfully mated with his daughter O119, resulting in the inbred
offspring O121. The relatedness between F18 and O121
was R = 0.7878, and the relatedness between O119 and
O121 was R = 0.6251 (Table 2). F18 was heterozygous at
14 of 27 loci; O119 (which is the mother of O121) was heterozygous at 13 of 26 loci (amplification failure of 1 locus);
and O121 was heterozygous at 14 of 27 loci. Manual examination of the raw data indicates that individual O121 can
have received one allele from F18 and one allele from
O119 at each locus. Such high values of relatedness are in
line with the assumption of inbreeding. However, when individuals are inbred, a correction for co-ancestry is required to
differentiate between HS and FS. This was not done in our
analyses. Nevertheless, Mayor’s method appeared more robust than ML-Relate in detecting HS in case of co-ancestry
between parents.
Age distribution of males siring cubs and mean time
span between litters
Comparison of the distribution of the males’ age at capture and the age at reproduction revealed that males from
10 to 14 years of age were slightly under-represented among
successful fathers, while young males (4–9 years) and bears
aged 15–19 years were slightly over-represented (Fig. 1).
However, the differences were not significant (ANOVA,
F[1,335] = 0.0472, p = 0.8281), indicating that the mean age
at capture was not different than the mean age of reproduction. The mean time span between litters sired by the same
male was 3.9 years (n = 18, range 1–11 years). Five males
sired litters with an interval of 6 years or more (6, 6, 9, 9,
and 11 years, respectively). They were between 13 and
23 years old when they sired their last observed litter (13,
17, 15, 23, and 17 years, respectively).
Discussion
Copulations with multiple males within one breeding period are known to occur in female polar bears (Ramsay and
Stirling 1986; Wiig et al. 1992). We document for the first
time that this behavior can result in multiple paternities.
One multiple paternity was unambiguously identified among
29 litters and in another case multiple paternity was likely.
The frequency of multiple paternities in polar bears was expected to be low because of the rather long breeding period
in the population, implying asynchronous oestrus among females. Furthermore, the predictability of female locations in
the mating season is low because of the large changes in
sea-ice distribution. However, a larger data set is needed to
statistically compare the frequency of multiple paternity in
polar bears with that reported in brown bears (14.5%; Bellemain et al. 2006a). Multiple paternities in bears occur in
general at relatively low rates in comparison with other
mammals such as rodents (Baker et al. 1999; Burton 2002;
Crawford et al. 2008), insectivores (Stockley et al. 1993), or
social carnivores (Randall et al. 2007). In the gray redbacked vole (Clethrionomys rufocanus (Sundevall, 1846)),
Published by NRC Research Press
1200
Can. J. Zool. Vol. 87, 2009
Table 1. Full-sibling (FS) and half-sibling (HS) assignments (based on traditional, ML-Relate, and Mayor’s methods) of Barents
ML-Relate
Mother
M1a
M2a
M3a
M4a,b
M5a
M6a
M7a,c
M8a
M9
M10
M11
d
M12
M13
M14
M15
M16
M17
M18
M19
M20
e
M21
M22
M23
M24
M25
Offspring
O1j
O2j
O3j
O4j
O5j
O6j
O7j
O8j
O9j
O10j
O11j
O12j
O13j
O14j
O15j
O16j
O17j
O18j
O19j
O20
O21j
O22
O23j
O24j
O25
O26
O27
O28j
O29
O30j
O31
O32
O33
O34
O35
O36j
O37
O38
O39j
O40
O41
O42
O43
O44
O45
O46
O47
O48
O49
O50
O51
O52
O53
O54
O55
O56
O57
O56
O57
O58
O59
Birth
2003
2003
2004
2004
2006
2006
2006
2006
2006
2006
2002
2002
2002
2002t
2006
2006
2003
2006
2006
1994
2000t
1995
2000
1998t
2002
1996t
2002t
2003
1995t
2002ft
2003
2003
1993
1993
1997t
2000t
2002
2002
2005
1996
1996
1997
1997
1997
1997
1997
1997
1997
1997
1997
1997
2003
2003
2004
2004
2005
2005
2006
2006
2006
2006
Father
F7
F7
F1
F1
F2
F2
F3
F3
F4
F4
F6
F6
F6
F8
F8
F8
F6
F5
F5
Traditional
na
na
na
na
na
Negative
Negative
Different
1
#
#
#
#
#
#
*
*
#
#
#
#
#
#
&
&
na
F19
F11
na
na
Different
&
&
&
&
*
*
#
#
F12
Different
&
&
3
*
#
5
&
&
&
6
#
*
&
&
&
&
&
*
&
&
na
na
na
na
na
na
na
na
na
&
&
&
&
&
&
12
13
14
15
&
&
&
&
*
#
#
&
&
&
&
&
&
na
11
&
&
&
&
na
10
&
*
F21
9
#
#
&
Different
8
#
#
&
F9
7
#
#
&
#
#
4
*
*
F7
F20
2
&
&
*
#
#
#
#
#
#
#
#
#
#
*
*
#
#
#
#
*
*
#
#
#
#
Published by NRC Research Press
Zeyl et al.
1201
Sea polar bears (Ursus maritimus) as determined through the mother.
Mayor’s
16
17
18
19
20
21
1
#
#
#
#
#
#
*
*
#
#
#
#
#
#
&
&
2
&
&
#
#
5
&
&
&
6
#
&
&
&
&
&
&
&
10
11
&
&
&
&
&
&
12
13
14
15
&
&
&
&
&
16
17
18
&
&
&
&
19
20
#
#
&
21
&
&
&
&
&
&
&
&
&
&
&
&
#
#
&
&
&
*
*
9
#
#
&
#
#
8
#
#
&
&
&
7
#
#
&
#
#
4
#
&
&
&
&
&
&
&
&
&
3
&
&
&
&
&
&
&
&
&
&
&
&
&
#
#
#
#
#
#
#
#
#
#
#
#
*
*
#
#
#
#
#
#
#
#
Published by NRC Research Press
1202
Can. J. Zool. Vol. 87, 2009
Table 1 (concluded).
ML-Relate
Mother
Offspring
Birth
M26
O60
O61
O62
O63
O64
O65
O66
O67
O68
O69
O70
O71
O72
O73
O74
O75
O76
O77
O78
O79
O80
O81
O82
O83
O84
O85
O86
O87
O88
O89
O90
O91
O92
O93
O94
O95
O96
O97
2006
2006
2006
2006
1986t
1993t
1987t
1987ft
1987t
1993t
1988t
1991t
1989t
1996
1993t
1996t
1995
1997t
1991t
2004
2004
1995t
2006
2006
1989t
1993t
1996
1992t
1994
1997t
1993t
1994
1994
2002t
2001
2001
1992
1992
M27f
M28
M29
M30
M31
M32
M33
M34
M35
M36g
M37
M38h
M39e
(M40)i
(M41)
Father
Traditional
na
na
na
na
na
na
na
na
na
Different
Different
Different
Different
Different
1
#
#
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
*
*
&
&
2
3
na
na
5
#
#
*
6
7
8
9
10
11
12
13
14
15
&
&
&
&
&
&
#
#
&
#
#
*
*
&
&
&
&
#
&
#
F22
?F22
4
*
&
&
#
#
#
#
Note: The mothers in parenthesis were determined from field data only. Siblings for which both parents were assigned through parentage analysis
when age was determined from tooth cementum growth layers and ‘‘ft’’ indicating when age was determined from field measures of body size
denotes no indication that the siblings were sired by different fathers, and ‘‘different’’ denotes that there was indication that the siblings were sired
‘‘&’’s; inconclusive assignments are indicated by ‘‘*’’s.
a
The ML-Relate test for siblings with both parents assigned by parentage analysis is identical in Tables 1 and 2.
Both methods were inconclusive. FS was accepted following Mayor’s method using the father’s genotype.
c
Female that mated twice with the same male. O15 and O16 were captured as dependent cubs in 2006; O14 was captured as subadult in 2006.
d
Inconsistency between the two methods. Mayor’s results were accepted (see text).
e
Mayor’s method was inconclusive.
f
Multiple paternity accepted.
g
Likely case of multiple paternity.
h
Same litter or the female mated twice with the same male.
i
The probability of being the true father (?F22) was low in this case (p = 0.3), but there were no incompatibilities. See parentage analysis (Zeyl et al. 2009).
b
Published by NRC Research Press
Zeyl et al.
1203
Mayor’s
16
17
18
19
20
21
1
#
#
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
&
2
3
4
5
*
*
&
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21ghifdeabc
&
&
&
&
&
&
#
#
&
#
#
&
&
&
&
&
&
#
&
#
&
&
&
na
na
are indicated by ‘‘j’’s. The offsprings’ year of birth appears in boldface type when first captured as juveniles together with their mother, with ‘‘t’’ indicating
and tooth-wear examination). The fathers in boldface type also appear in Table 2. For the traditional method, ‘‘na’’ denotes not applicable, ‘‘negative’’
by at least two different fathers. For ML-Relate and Mayor’s methods, FS pairwise relationships are indicated by ‘‘#’’s and HS pairwise relationships by
Published by NRC Research Press
1204
Can. J. Zool. Vol. 87, 2009
Table 2. Full-sibling (FS) and half-sibling (HS) assignments (based on traditional, ML-Relate, and Mayor’s methods) of Barents
Sea polar bears (Ursus maritimus) as determined through the father.
ML-Relate
Father
F1a
a
F2
a
F3
a
F4
a
F5
a
F6
F7a
F8a,b
F9c,d
F10
F11
F12
F13c
F14
F15
c
F16
F17e
F18f
Offspring
O3j
O4j
O5j
O6j
O7j
O8j
O9j
O10j
O18j
O19j
O17j
O11j
O12j
O13j
O21j
O1j
O2j
O98j
O14j
O99
O15j
O16j
O100
O36j
O101
O102
O103
O24j
O104j
O105
O106
O28j
O107
O108
O109
O110
O111
O112
O113
O114
O115
O116
O117
O118
O119
O120j
O121j
Birth
2004
2004
2006
2006
2006
2006
2006
2006
2006
2006
2000t
2002
2002
2002
2000t
2003
2003
2005
2002t
2004t
2006
2006
1995
2000t
2002
2003t
1989t
1998t
1999
1992t
2001
2003t
1986t
1997t
1989t
1995t
1990t
1996t
1994t
1995t
1999t
1990t
1991t
1995t
1997t
1998ft
2003t
Mother
M2
M2
M3
M3
M4
M4
M5
M5
M8
M8
M8
M6
M6
M6
M9
M1
M1
M42
M7
M7
M7
(M43)
M14
(M44)
Traditional
na
na
na
na
na
Different
Different
Different
1
#
#
#
#
*
*
#
#
#
#
&
&
2
3
&
&
&
&
&
&
#
na
na
Different
(M46)
M12
Different
*
*
&
na
na
na
Different
Different
#
#
&
&
&
&
&
&
&
&
*
#
#
&
&
&
&
#
#
*
na
*
*
&
&
#
#
#
#
6
2
3
&
&
&
&
&
&
&
&
#
#
#
&
&
&
&
#
&
&
&
&
#
#
&
&
&
&
#
#
&
&
&
&
&
&
&
&
&
&
#
6
&
&
&
&
&
&
&
&
&
&
#
#
&
#
#
&
&
5
#
#
#
&
&
&
&
&
&
4
&
&
&
&
&
&
&
1
#
#
#
#
#
#
#
#
#
#
&
&
#
#
&
&
*
*
*
*
&
#
#
&
#
#
#
#
*
*
*
*
5
#
#
&
&
&
4
&
&
#
M11
M45
M47
O119
Mayor’s
na
&
&
#
#
#
#
Note: Siblings for which both parents were assigned through parentage analysis are indicated by ‘‘j’’s. The offsprings’ year of birth appears in
boldface type when first captured as juveniles together with their mother, with ‘‘t’’ indicating when age was determined from tooth cementum
growth layers and ‘‘ft’’ indicating when age was determined from field measures of body size and tooth-wear examination). The mothers in boldface type also appear in Table 1; mothers in parenthesis were determined from field data only. For the traditional method, ‘‘na’’ denotes not applicable, ‘‘negative’’ denotes no indication that the siblings were born by different mothers, and ‘‘different’’ denotes that there was indication that
the siblings had at least two different mothers. For ML-Relate and Mayor’s methods, FS pairwise relationships are indicated by ‘‘#’’s and HS
pairwise relationships by ‘‘&’’s; inconclusive assignments are indicated by ‘‘*’’s. Data in italic type indicate a father who mated incestuously with
his daughter.
a
The ML-Relate test for siblings with both parents assigned by parentage analysis is identical in Tables 1 and 2.
Male mated twice with the same female. O15 and O16 were captured as dependent cubs in 2006. O14 was captured as subadult in 2006.
c
Inconsistency between the two methods. We accepted Mayor’s results (see text).
d
Inconsistency with the parentage analysis (with assigned mothers).
e
Same litter or male mated twice with the same female.
f
Inbreeding case. The female O119 is believed to be the mother of O121.
b
Published by NRC Research Press
Zeyl et al.
1205
Fig. 1. Histogram representing (a) the relative age distribution densities of adult male polar bears (Ursus maritimus) at capture and (b) the
relative age distribution densities of males when they sired cubs. For illustration purpose, we used five age categories (4–9, 10–14, 15–19,
20–24, and 25+ years). The number of observations (n) is shown above each bar.
the proportion of litters showing multiple paternities was
positively correlated with local density of males around females in oestrus (Ishibashi and Saitoh 2008). Further studies
are required to examine whether the frequencies of multiple
paternity in polar bears vary among populations with different densities.
Uncertainty in age estimation limited our ability to distinguish between litters of siblings identified through a common parent. However, our results indicated that both
females and males rarely mated with the same partner in different years. Most consecutive litters were sired by different
males. Both female and male polar bears show area fidelity
during the breeding season; however, gene flow appears to
be slightly male-biased within the Barents Sea population
(Zeyl et al. 2009). One could therefore expect that specific
females frequently mated with the same neighboring male
in different years. However, a relatively high number of
available males in most areas may be sufficient to counteract this. Fierce male competition because of a male-biased
operational sex ratio should work in the same direction. Accordingly, we detected only one case of incestuous mating.
Mating between father and daughter has not been documented previously in polar bears and has been rarely reported in other bear species. A putative case has been
mentioned in black bears (Costello et al. 2008). Father–
daughter matings were detected in 2 out of 95 litters in
Swedish brown bears (Bellemain et al. 2006b). The spatial
structure of bears, associated with low recruitment, malebiased dispersal, and male turnover, appears to prevent high
rates of incestuous mating. Thus, there is no need for active
inbreeding avoidance mechanisms as suggested by Bellemain et al. (2006b) and Costello et al. (2008). The mean relatedness observed between polar bear mating pairs is
consistent with the indication that female bears generally do
not mate with close relatives, as reported in brown bears
(Bellemain et al. 2006b).
It has previously been suggested that male polar bears are
polygynous (DeMaster and Stirling 1981) and that females
are polyandrous (Ramsay and Stirling 1986; Wiig et al.
1992; Molnár et al. 2008). Our results indicate that at least
in the Barents Sea, the mating system of polar bears is promiscuous (where males mate with any accessible receptive
female and there is no continuing bond between individual
males and females after mating has occurred. Females usually mate with different males in successive breeding attempts. In some species, females mate with several different
males during each period of receptivity, whereas in others,
they typically mate with a single male; Clutton-Brock
1989). Since this conclusion is only based on a limited number of litters, it should be taken with caution. Nevertheless,
the results are in accordance with Clutton-Brock (1989),
who predicted a promiscuous mating system when females
are widely and unpredictably distributed. The mating system
of a species is plastic: there is a correlation between the
mating system and population densities (Kokko and Rankin
2006). In swift foxes (Vulpes velox (Say, 1823)), the mating
system is polygynous in high-density areas, whereas it is
monogamous in low-densities areas (Kamler et al. 2004). In
European water voles (Arvicola terrestris (L., 1758)), consecutive litters were found fathered by a single male in lowdensity populations and usually by different males in a highdensity population (Aars et al. 2006). The Barents Sea has a
moderate to high polar bear density compared with several
other areas, but local densities are variable (Aars et al.
2009). A lower density of available breeders within a population that can, e.g., be caused by excessive hunting may induce a change in the mating system of the animals within
the area. If human hunting of polar bears is not male-biased,
or if no hunting occurs such as in the Barents Sea population, the adult sex ratio become close to 1:1. As many females in the mating season are with cubs and unavailable
for mating, more males than females will be available for
Published by NRC Research Press
1206
Can. J. Zool. Vol. 87, 2009
mating (Bunnell and Tait 1981; Ramsay and Stirling 1986).
Male-biased OSR is expected to favor numerous mating encounters for females (DeYoung et al. 2002). Indeed, field
observations indicate that female polar bears in oestrus may
copulate with several males (Ramsay and Stirling 1986;
Wiig et al. 1992). In contrast, very low densities and a
closer to even OSR, e.g., in areas with male-biased hunting
could lead to a more monogamous mating system.
In black bears, paternity analyses revealed that male reproductive success was dominated by intermediate-aged
bears (Costello et al. 2008), which indicates that most males
would have a relatively short reproductive tenure. This is
congruent with the observation of Ramsay and Stirling
(1986) who reported that male polar bears associated with
adult females were, on average, older (median = 10.5 years
of age) than solitary males (median = 8 years of age). Taking into account the growth pattern in male polar bears, we
expected that males belonging to the age class 15–19 would
sire most litters. It also corresponds to the period when the
foreleg guard hairs, which are hypothetized to be a sexual
ornament, reach their maximum length (Derocher et al.
2005) and when most wounds and scars are observed on
males (A.E. Derocher et al., submitted).2 Sexual dimorphism
can be maintained through sexual selection, with larger body
size in males being correlated to higher reproductive success
through a better access to females (Andersson 1994). In general, the size difference in polar bears is large (Derocher et
al. 2005), indicating that male competition for females is
fierce. Our data set was not large enough to test with high
statistical power for smaller differences in age for male reproductive success, but showed that such differences seemed
small, contrary to our expectation. Some care should be
taken in any conclusion based on a comparison between the
age distribution of males at capture and the age distribution
of males when siring cubs. The youngest males are underrepresented in the capture data owing to lower trapability
(Derocher 2005). Older males that sired cubs may have
lower survival rates and less chance of being captured. The
main conclusion that reproductive success of adult males of
different ages were unlikely do differ profoundly still seems
to hold. Our results suggest that the male’s size and age
might be less indicative of the reproductive success than
previously thought.
The distribution of female polar bears during the mating
season is influenced by the distribution and accessibility of
their main prey (Stirling et al. 1993), which in the spring is
ringed seal (Pusa hispida (Schreber, 1775); Derocher et al.
2002). The prime habitat of ringed seals in Svalbard is near
glacier fronts in sheltered fjords and bays (Smith and Lydersen 1991). The distribution of males in spring appears to
be correlated with the distribution of females available for
reproduction (Ramsay and Stirling 1986; Stirling et al.
1993). Consequently, some areas have higher local bear densities than others (Wiig et al. 1992). This might influence
the pattern of age-related reproduction in males because the
level of competition between males may vary with density.
Indeed, in some species, fluctuations in population densities
might alter the outcome in the breeding success of males of
2 A.E.
different age classes. In the Saint Kilda population of promiscuous Soay sheep (Ovis aries L., 1758), the level of
male–male competition for mates varies with population
size and sex ratio. Old males sire larger sibships (i.e., a
group of offsprings produced by a male) than young males
at low population size when polygyny of old males is also
maximal. However, the size of sibships sired by young
males is small at any population size (Pemberton et al.
1999). In polar bears, both scramble competition (males disperse to find receptive females) and contest competition
(males fight to establish dominance over other males to get
access to females) are believed to occur (A.E. Derocher et
al., submitted).2 Sequestration and herding of females toward low-density areas could be advantageous for younger
males because it reduces the probability of encountering
older males with superior fighting abilities. Some field observations indicate that males might herd females in the
Barents Sea population (Wiig et al. 1992), and this behavior
has also been reported in Canadian polar bears (Ramsay and
Stirling 1986). The mountains and glaciers from the Svalbard archipelago might offer multiple herding opportunities
for young males. Thus, the observed absence of age-related
breeding success in male polar bears could be related to the
mechanism of intermale competition to gain breeding opportunities. The landscape in the Barents Sea might favor a
high proportion of young males being able to gain breeding
opportunities. The relation between age and breeding success of males may vary between populations according to
landscape characteristics, to the distribution of seals, and local bear densities.
Limitation of the statistical analysis
Costello et al. (2008) found that ML-Relate was likely to
infer genetic relationships between individuals to be closer
than they were. This seemed indeed to explain some inconsistencies between ML-Relate and Mayor’s method in this
study. However, ML-Relate also failed to distinguish between alternative relationships (FS and HS) in cases where
siblings were FS. This might be due to a violation of the assumption of co-ancestry between parents, to the presence of
groups of relatives in the data set, or this could also arise
because some parents might present genotypes with rare alleles. Indeed, this would influence the discriminating power
of the methods. Further studies evaluating the robustness of
those methods to hypothesis violation would be welcome.
The analysis performed with Mayor’s method appeared to
be more reliable than the results based on ML-Relate. This
is not surprising, as Mayor’s method uses the additional information provided by the genotype of one of the parents.
Moreover, both ML-Relate and Mayor’s method are able to
provide more information than the traditional method of parental allele counts, which is applicable only within groups
of n ‡ 3 siblings when searching for multiple paternities
and studying the mating system of a species. These statistical methods allow the detection of HS within litters with
only two siblings, and thus are likely to provide a better estimate of the minimal rate of multiple paternities than the
traditional method.
Derocher, J. Aars, M. Andersen, and Ø. Wiig. Mating ecology of polar bears at Svalbard. Submitted for publication.
Published by NRC Research Press
Zeyl et al.
Acknowledgements
We are grateful to Lianne Dance (previously Mayor) for
kindly providing the scripts necessary to perform the analysis. We thank the anonymous reviewers for their constructive comments. This work was supported by the Natural
History Museum of the University of Oslo, Norway, and the
Norwegian Research Council through the National Centre
for Biosystematics (project no. 146515/420). Samples were
provided by the Norwegian Polar Institute (Tromsø, Norway).
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Boltunov, A.N., and Wiig, Ø. 2009. Estimating the Barents Sea
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