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Extra‐pair paternity in the strongly monogamous Wandering Albatross Diomedea exulans has no apparent benefits for females

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Although 92% of avian species are socially monogamous, extra-pair copulation (EPC), resulting in extra-pair paternity (EPP), is a common reproductive strategy in birds. Among seabirds, in which the rate of social monogamy reaches 100%, Procellariiformes (albatrosses and petrels) show low EPP rates, with the noticeable exception of the only albatross investigated in this regard, the Waved Albatross Phoebastria irrorata. This species, in which forced copulations are known to occur, showed a surprisingly high rate of EPP (25% of chicks). We investigate here EPP rates in another albatross species, the Wandering Albatross Diomedea exulans, subject to a demographic survey conducted for 38 years. We combined data on pair bonds with analysis of ten microsatellite loci and found that 10.7% of 75 chicks had an extra-pair sire. Although there was some evidence for inbreeding avoidance, within-pair and extra-pair chicks showed similar levels of heterozygosity, and the incidence of EPP was independent of age, experience or past reproductive success. Hence, we found no evidence that females benefit from EPCs. Owing to the male-biased sex ratio in adults, widowed and divorced males required more time to find a new mate (+28 and +72%, respectively) than did females. Combined with high sexual size dimorphism, this phenomenon might promote the forced copulations observed in this species. Our data therefore suggest that EPC is beneficial to unpaired males but occurs at random in females, consistent with the hypothesis that EPP results solely from forced EPCs. However, the importance of the latter for EPP and the part played by solitary males require further investigation.
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Ibis
(2007),
149
, 67–78
© 2006 The Authors
Journal compilation © 2006 British Ornithologists’ Union
Blackwell Publishing Ltd
Extra-pair paternity in the strongly monogamous
Wandering Albatross
Diomedea exulans
has no
apparent benefits for females
PIERRE JOUVENTIN,
1
* ANNE CHARMANTIER,
2
MARIE-PIERRE DUBOIS,
1
PHILIPPE JARNE
1
& JOËL BRIED
3
1
Centre d’Ecologie Fonctionnelle et Evolutive, UMR CNRS 5175, 1919 route de Mende,
34293 Montpellier Cedex 5, France
2
Edward Grey Institute, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
3
Departamento de Oceanografia e Pescas, Centro do IMAR da Universidade dos Açores,
9901-862 Horta, Açores, Portugal
Although 92% of avian species are socially monogamous, extra-pair copulation (EPC),
resulting in extra-pair paternity (EPP), is a common reproductive strategy in birds. Among
seabirds, in which the rate of social monogamy reaches 100%, Procellariiformes (albatrosses
and petrels) show low EPP rates, with the noticeable exception of the only albatross inves-
tigated in this regard, the Waved Albatross
Phoebastria irrorata
. This species, in which forced
copulations are known to occur, showed a surprisingly high rate of EPP (25% of chicks).
We investigate here EPP rates in another albatross species, the Wandering Albatross
Diome-
dea exulans
, subject to a demographic survey conducted for 38 years. We combined data
on pair bonds with analysis of ten microsatellite loci and found that 10.7% of 75 chicks had
an extra-pair sire. Although there was some evidence for inbreeding avoidance, within-pair
and extra-pair chicks showed similar levels of heterozygosity, and the incidence of EPP was
independent of age, experience or past reproductive success. Hence, we found no evidence
that females benefit from EPCs. Owing to the male-biased sex ratio in adults, widowed and
divorced males required more time to find a new mate (+28 and +72%, respectively) than
did females. Combined with high sexual size dimorphism, this phenomenon might promote
the forced copulations observed in this species. Our data therefore suggest that EPC is bene-
ficial to unpaired males but occurs at random in females, consistent with the hypothesis that
EPP results solely from forced EPCs. However, the importance of the latter for EPP and the
part played by solitary males require further investigation.
Extra-pair copulation (EPC) in birds is a classic
example illustrating the conflicts of interest in
reproduction between males and females, given that
(1) females that seek EPCs, e.g. to improve the
number or the quality of their offspring, may put
their social mates at risk of increased cuckoldry,
and (2) forced copulations by extra-pair males
may be costly for females (Chapman
et al
. 2003,
Westneat & Stewart 2003). Although more than
90% of avian species (and 100% of seabirds) are
socially monogamous (Lack 1968), an increasing
number of studies have shown that social monogamy
must be distinguished from genetic monogamy (Ford
1983, Bennett & Owens 2002).
In socially monogamous species with biparental
care, selection may favour male attempts to engage
in EPCs in order to increase their breeding success
(Trivers 1972, Ford 1983). For females, the suggested
benefits of EPCs include higher genetic diversity in
their brood (sometimes combined with inbreeding
avoidance), higher genetic quality of their young (or
better combination of genes), access to resources
defended by males and fertility insurance (reviewed
by Kempenaers & Dhondt 1993, Jennions & Petrie
2000, Westneat & Stewart 2003). Nonetheless, the
predictions regarding the incidence of EPCs and extra-
pair paternity (EPP) remain contradictory. Hasselquist
*Corresponding author.
Email: pierre.jouventin@cefe.cnrs.fr
68
P. Jouventin
et al.
© 2006 The Authors
Journal compilation © 2006 British Ornithologists’ Union
and Sherman (2001) suggested that social monog-
amy should favour potentially high rates of EPCs and
EPP resulting from adjustment of social mate choice
by females. By contrast, Møller (2000) and Griffith
et al
. (2002) suggested that the incidence of EPP
should be low in those species in which paternal
investment was important, such as seabirds.
However, EPC may also be costly; it can result in
an increased risk of disease transmission during cop-
ulations, in increased costs of competition for mates,
in lower parental investment from cuckolded males,
in a risk of copulation with a low-quality partner,
and an increased risk of cuckoldry for males when
seeking opportunities for EPC (reviewed by Wink &
Dyrcz 1999, Bennett & Owens 2002). Females are
expected to solicit or to refuse EPC depending on
the relative importance of the potential benefits and
costs (Westneat
et al
. 1990).
A specific type of conflict occurs when females are
involved in copulations that they would otherwise
refuse (McKinney
et al
. 1984, Morton
et al
. 1990).
Females may then incur costs of resisting that are too
high (risk of injury or egg loss), so that the best strat-
egy for them is to accept rather than to resist forced
attempts (Westneat
et al
. 1990). Forced EPC has
been observed in several bird species and it seems to
occur more frequently than EPC solicited by the
female (reviewed by Birkhead & Biggins 1987).
The Wandering Albatross
Diomedea exulans
is a
long-lived seabird exhibiting remarkable morpho-
logical, behavioural and life-history traits. In contrast
to many seabird species that are sexually monomor-
phic, female Wandering Albatrosses are darker, smaller
and
c.
20% lighter than males (Weimerskirch 1995,
Tickell 2000, Shaffer
et al
. 2001). Individuals can
live more than 50 years (Weimerskirch & Wilson 2000)
and are extremely selective during mate choice, which
can take several years (Jouventin
et al
. 1999), fol-
lowed by extreme social mate fidelity. Indeed, pair
bonds can last up to 28 years (J. Bried & P. Jouventin
unpubl. data) and the incidence of divorces is very
low (4.9%, calculated from Bried & Jouventin 2002).
As with all seabirds (Bried & Jouventin 2002), the
Wandering Albatross has an extended period of obli-
gate biparental care. Because this period lasts almost
1 year from laying until fledging of the single chick
in this species (see Tickell 2000), Wandering Alba-
trosses are biennial breeders (i.e. pairs breed every other
year when they rear their chick successfully but annu-
ally when they fail during incubation; Tickell 2000).
Under these conditions, female Wandering Alba-
trosses are unlikely (1) to need adjustment for the choice
of their social mate (Slagsvold & Lifjeld 1994, Ben-
nett & Owens 2002; see also empirical studies by
Kempenaers
et al
. 1997, Voigt
et al
. 2003), (2) to put
their young at risk from a decrease in paternal invest-
ment if their mate is not confident about his degree
of paternity (Trivers 1972, Møller 1988, Griffith
et al
. 2002), and (3) to put themselves at risk from
decreased reproductive lifespan. Supporting these
hypotheses, female Wandering Albatrosses have, as
far as we know, never been observed seeking EPCs.
Consequently, we expect a very low frequency of EPP.
However, a factor that could favour the occur-
rence of EPC in Wandering Albatrosses is differential
mortality at sea between sexes (Weimerskirch
et al
.
2005). This mortality is incidental, being essentially
due to the fisheries that have been operating in the
Southern Ocean since the 1980s. Fishing mainly
occurs near the subtropical convergence (Weimers-
kirch
et al
. 1997), where female and immature
Wandering Albatrosses, but not adult males, forage
(Shaffer
et al
. 2001). Wandering Albatross popula-
tions, at least those from the Indian Ocean, therefore
have a male-biased sex ratio in adults (Jouventin
et al
. 1999, Nel
et al
. 2003, Weimerskirch
et al
.
2005). Consequently, old, solitary males, which are
dominant over young males, have regularly been
observed performing copulation attempts to which
females, which choose young males when starting
breeding (Jouventin
et al
. 1999), attempted to resist
by struggling (P. Jouventin pers. obs.; see also Mur-
phy 1936, Tickell 2000). Although they are smaller
than males, females seem to be able to thwart such
attempts (Tickell 2000). If they do manage to avoid
insemination, we should again expect a low rate of
EPP in this species, despite uneven sex ratio and
sexual size dimorphism. Forced EPCs have also been
observed in Buller’s Albatross
Thalassarche bulleri
(Richdale 1949), in the Laysan Albatross
Phoebastria
immutabilis
(Fisher 1971) and in the Waved Alba-
tross
Phoebastria irrorata
(Huyvaert
et al
. 2000), and
they were also suspected in the Northern Royal
Albatross
Diomedea sanfordi
by Richdale (1950). As
with all albatrosses, these species are long-lived, lay
only one egg per breeding attempt and show high
year-to-year mate fidelity (Tickell 2000, Bried &
Jouventin 2002).
In the Order Procellariiformes, including 125
species of albatrosses and petrels, EPP studies remain
scarce. EPP was detected in only two out of six petrel
species (Hunter
et al
. 1992, Swatschek
et al
. 1994,
Mauck
et al
. 1995, Austin & Parkin 1996, Lorentsen
et al
. 2000, Rabouam
et al
. 2000, Quillfeldt
et al
. 2001),
© 2006 The Authors
Journal compilation © 2006 British Ornithologists’ Union
Extra-pair paternity in Wandering Albatrosses
69
and its frequency was low (9% on average). How-
ever, surprisingly high rates of EPP (25% of off-
spring) were found in the only albatross species
investigated, the Waved Albatross (Huyvaert
et al
.
2000), where forced EPCs regularly occur. Because
field data were scarce in these species where EPP was
estimated, the demographical and social factors likely
to promote EPC in albatrosses remain undetermined.
We attempted to fill this gap by using both mole-
cular and demographic data. We conducted a micro-
satellite analysis on two distant populations of Wan-
dering Albatrosses from the southern Indian Ocean.
This dataset was supplemented by data from a 38-year
demographic survey, to determine and to explain the
social mechanisms underlying the occurrence of EPP
in this species. In particular, the demographic data
allowed us to determine if males needed more time
than females to form a new pair bond after the death
of their mate or a divorce due to the male-biased
sex-ratio, and if cuckolded males (if any) were young
and/or inexperienced adults.
MATERIALS AND METHODS
Fieldwork was conducted in the southern Indian Ocean,
on Possession Island, Crozet archipelago (46
°
25
S,
51
°
45
E), and on the Courbet Peninsula, Kerguelen
archipelago (48
°
28
′−
50
°
00
S, 68
°
28
′−
70
°
35
E),
1500 km east of Crozet. The samples for the genetic
analysis were collected between November 2001
(onset of the laying period) and October 2002 (chicks
were sampled when 7 months old, i.e. 2 months before
fledging) at the former locality, and between Decem-
ber 2002 and July 2003 (middle of the chick-rearing
period) at the latter.
Blood sampling and microsatellite
analysis
We collected 50–100
µ
L of blood from the brachial
veins of 226 individuals representing 75 families
(i.e. the two parents and their single chick) plus one
solitary adult, using 1-mL non-heparinized syringes.
Each blood sample was stored in 1 mL of Queen’s
lysis buffer (Seutin
et al
. 1991), in the field at ambi-
ent temperature and later at 4
°
C. On Possession
Island, blood was collected from 50 families from
the two main colonies of the island, namely the
colony from Baie du Marin (167 breeding pairs, 25
families sampled) and that from Pointe Basse (181
breeding pairs, 25 families plus one solitary male
sampled), situated
c.
15 km apart. Because these
colonies are close enough for males from one colony
to copulate with females from the other, they were
pooled in the paternity analysis. Twenty-five families
were sampled at Kerguelen, in a 54-pair colony.
DNA extraction was performed using the Dneasy™
Tissue Kit (Qiagen, Inc.). Adults were sexed by
amplification of the
CHD
gene, using primers 2550F
and 2718R (Fridolfsson & Ellegren 1999). Genotyp-
ing for the paternity analysis was conducted using
ten microsatellite loci: 11H7, 12H8, 11H1, 12C8,
12E1 (Dubois
et al
. 2005), De3, De7, De37 and Dc5,
and the sex-linked De33 (Burg 1999, Burg & Croxall
2004). All these loci were isolated from the Wander-
ing Albatross, except for Dc5, which was isolated
from the Grey-headed Albatross
Thalassarche chryso-
stoma
. Microsatellite loci were amplified by poly-
merase chain reaction (PCR). PCRs were multiplexed
for five subsets of loci (11H1, 11H7, 12C8 and 12H8;
12E1; De7; De37 and Dc5; De3 and De33) in a 10-
µ
L
final volume including 0.2
µ
M
of each primer and
1.5
µ
L genomic DNA, and using the Qiagen multi-
plex PCR kit (Qiagen, Inc.). PCRs were conducted
using a PTC100 thermocycler (MJ Research) under
the following conditions: 15 min activation of the
HotStart
Taq
DNA polymerase at 95
°
C, 30 cycles of
30 s of initial denaturation at 94
°
C, 90 s annealing
(58
°
C for 11H1, 11H7, 12C8 and 12H8; 54
°
C
for 12E1, De37 and Dc5; 52
°
C for De3, De7 and
De33) and 60 s extension at 72
°
C, and then a final
30-min extension at 60
°
C.
Microsatellite profiles were obtained with an ABI
PRISM 310 Genetic Analyser (Applied Biosystems).
PCR products were run in three groups (12H8,
12C8, 11H7 and 11H1; 12E1 and De7; De3, De33,
De37 and Dc5). Reactions were conducted in a
mix containing 2
µ
L PCR products (dilution 90),
15
µ
L deionized formamide and 0.2
µ
L GeneScan-
500 XLROX Size Standard. The solutions were
migrated in a capillary soaked with POP4 polymere.
All profiles were conducted simultaneously in
multiplex reactions and then analysed using
GENESCAN
and
GENOTYPER
computer programs. To avoid geno-
typing errors that might result in some chicks being
wrongly considered as within-pair or extra-pair, PCRs
were re-done and PCR products were run again when
ill-defined peaks or mismatches were detected
during the analysis of the genetic profiles (in the
same groups of loci as during the first run, but also
by running separately the loci for which there was a
mismatch). In addition, each profile was analysed
independently by two observers who were unaware
of family relationships; there was 100% matching
70
P. Jouventin
et al.
© 2006 The Authors
Journal compilation © 2006 British Ornithologists’ Union
concerning each genotype for each allele between
the two observers.
Analysis of molecular data
Regardless of whether or not the sex-linked De33
was included in the analyses, no significant genetic
differentiation was detected between the two colo-
nies from Possession Island (adults: both
F
st
< 0.0018,
n
= 101; chicks: both
F
st
< 0.0013,
n
= 50; exact test,
all
P
> 0.34). Given that these colonies are separated
by a short geographical distance, individuals were
pooled during analyses. Conversely, the populations
from Possession Island and Kerguelen appear to
be genetically differentiated (Bried
et al
. in press);
therefore, genetic analyses were conducted separately
at each locality. Allelic frequencies per locus were
estimated in each population in adults and chicks,
using
GENETIX
(version 4; Belkhir
et al
. 1996–2004;
see Appendix). Further details, including expected
and observed heterozygosities at each locus and
Hardy–Weinberg equilibrium, are given in another
study (Bried
et al
. in press).
Paternity was excluded when mismatches between
the chick and its social father occurred at two or
more loci. A single mismatch between offspring and
parental genotypes was interpreted as a mutation.
The
CERVUS
software version 2.0 (Marshall
et al
. 1998)
was used to estimate the combined probability
of exclusion, i.e. the probability of excluding an
unrelated male as a father using all loci, as well
as to assign paternities when possible. In addition,
sampling the adults during incubation enabled us to
avoid mistaking non-pair males (e.g. non-breeders)
for the chicks’ social fathers; indeed, such mistakes
could lead wrongly to consider some chicks as extra-
pair chicks.
To compare the degree of relatedness between
social partners and extra-pair partners, we estimated
relatedness among adults of each population follow-
ing Wang (2002). To test for higher genetic diversity
for extra-pair compared with within-pair offspring,
we calculated individual heterozygosity as the number
of heterozygous loci divided by the total number of
typed loci (Foerster
et al
. 2003). To increase the reli-
ability of our results, we followed Amos
et al
. (2001),
and also estimated individual heterozygosity using
mean standardized
d
2
-values, where standardized
d
is the length difference between the alleles carried
by a given individual at a locus divided by the max-
imum observed difference at this locus. The sex-linked
locus De33 was excluded from calculations of
relatedness and individual heterozygosity, as well
as from paternity analyses.
Analysis of demographic data
Our long-term demographic survey (capture–mark–
recapture) of the entire population from Possession
Island (representing more than 6000 ringed indi-
viduals, both adults and chicks), which has been con-
ducted annually since 1966, enabled us to determine
the age and/or previous breeding experience of 83 of
the 101 adults from which blood samples were
collected. Birds were sexed in the field from both
plumage colour and body size, males being larger and
whiter than females (reviewed by Tickell 2000). We
first checked whether age, breeding experience and
fecundity of the mates differed between nests with
a within-pair or an extra-pair chick. The probability
of rearing an extra-pair chick can be considered as a
binary (yes/no) variable in the Wandering Albatross.
Logistic regressions (
CATMOD
procedure; SAS Insti-
tute 1999) were therefore performed to determine
whether age, experience, fecundity and genetic
relatedness between mates were associated with
cuckoldry. A preliminary model included all pair-
wise interactions, and interactions with the least sig-
nificant effects were removed in a stepwise fashion.
All statistical tests were two-tailed. Power analyses
were conducted using
GPOWER (Faul & Erdfelder 1992).
RESULTS
Occurrence of extra-pair paternity
Whenever several mismatches were found between
the genotype of a chick and that of its social father,
at least two of these mismatches occurred at auto-
somal loci. There was therefore no problem due to
the sex-linked De33 when classifying chicks as within-
pair or extra-pair. The minimum combined probability
of exclusion was at least 0.98 at each locality
(Table 1).
On Possession Island, at least two mismatches
were detected between the genotype of a chick and
that of its social father in six cases (three at each
colony), resulting in an EPP rate of 12%. In three
other instances, the offspring differed from the
parental genotypes by only one allele at one locus;
these were considered to be mutations occurring in
within-pair chicks.
At Kerguelen, two chicks met the condition to be
considered sired by an extra-pair male. A third chick
© 2006 The Authors
Journal compilation © 2006 British Ornithologists’ Union
Extra-pair paternity in Wandering Albatrosses 71
showed a mismatch at 11H1 between its genotype
and that of its mother, and another mismatch at
11H7 where one allele was found in neither social
parent. The possibility that this chick could have
resulted from a copulation involving its social father
and a female that would have performed brood para-
sitism (i.e. laying her egg in the nest of another pair)
cannot be dismissed here; this chick was excluded
from subsequent analyses. Therefore, the rate of
EPP at Kerguelen was 8%. Although this value was
lower than that observed on Possession Island, the
difference was not significant (G-test with Williams’
adjustment, G1 = 0.27, P = 0.60).
Characteristics of the adults rearing an
extra-pair chick and of the extra-pair
sires
Eighty-two per cent of the adults that were blood-
sampled on Possession Island had been ringed as
chicks, so that their age, previous breeding experi-
ence and previous reproductive performance were
accurately known. These parameters did not differ
significantly between the mothers of a chick sired by
an extra-pair male (such chicks are hereafter referred
to as extra-pair chicks) and the mothers of a within-
pair chick (Table 2). Similarly, cuckolded males did
not differ from the males that were not cuckolded in
terms of age, previous breeding experience, previous
reproductive performance (Table 2) and also when
considering the proportion of inexperienced individuals
(0/6 and 4/43, respectively, the breeding experience
of the 44th male that was not cuckolded was unknown;
Fisher exact test, P = 0.99). The mates of four of the
six pairs that had reared an extra-pair chick on Pos-
session Island in 2002 returned in 2004; these four
pairs reunited. Likewise, the two cuckolded males from
Kerguelen retained their previous mate in 2005.
When considering all the males that were blood-
sampled, we could assign paternity for two of the eight
Tab le 1. Characteristics of the ten microsatellite loci used for paternity analysis of Wandering Albatrosses in the colonies of Possession
Island and Kerguelen; the sex-linked De33 was excluded from paternity analyses.
Locus
No. of alleles Probability of exclusion
Possession Kerguelen Possession Kerguelen
11H7 10 8 0.551 0.461
12H8 4 2 0.108 0.123
11H1 15 14 0.747 0.763
12C8 5 4 0.230 0.267
12E1 6 6 0.395 0.464
De3 2 2 0.022 0.053
De7 2 2 0.173 0.169
De33 15 11
De37 8 6 0.571 0.410
Dc5 2 2 0.039 0.043
Average 6.9 5.7
Combined probability of exclusion 0.984 0.980
Tab le 2. Age (years), breeding experience (number of previous breeding attempts) and breeding success (number of chicks fledged
per breeding attempt, considering only the previous breeding attempts) of the adult Wandering Albatrosses that were blood-sampled on
Possession Island. Means are given ± sd.
Age Breeding experience Breeding success
Females
Rearing an extra-pair chick 19.5 ± 6.2, n = 6 4.5 ± 2.8, n = 6 0.8 ± 0.1, n = 6
Rearing a within-pair chick 16.2 ± 6.2, n = 35 3.5 ± 2.5, n = 31 0.8 ± 0.3, n = 26
Mann–Whitney test U = 70.5, P > 0.2 U = 75.5, P > 0.4 U = 79.5, P > 0.9
Males
Cuckolded 21.6 ± 4.8, n = 5 5.6 ± 1.8, n = 5 0.7 ± 0.2, n = 5
Not cuckolded 18.1 ± 6.0, n = 37 3.6 ± 2.6, n = 32 0.7 ± 0.3, n = 29
Mann–Whitney test U = 59, P > 0.2 U = 41, P = 0.09 U = 91.5, P > 0.3
72 P. Jouventin et al.
© 2006 The Authors
Journal compilation © 2006 British Ornithologists’ Union
extra-pair young, one on Possession Island and the
other at Kerguelen. No EPP attributable to the soli-
tary male was detected. On Possession Island, the
putative extra-pair sire we identified was a male
from Pointe Basse who had sired a chick from Baie
du Marin. At Kerguelen, the putative extra-pair sire
was himself cuckolded.
Genetic benefits of EPCs for females
On each island, relatedness coefficients between mates
tended to be higher in pairs raising an extra-pair
chick than in pairs in which the male was the genetic
father of the chick, the difference became significant
when pooling the data from the two islands together
(Table 3).
However, the probability of a female from Posses-
sion Island having her chick sired by an extra-pair
male was not related to her genetic relatedness to her
social male, her age, previous breeding experience,
fecundity or common pair experience (Table 4).
Similarly, the probability of a male being cuckolded
did not depend on his genetic relatedness to his
female, his age, previous experience, fecundity or
common pair breeding experience (Table 4). When
only considering relatedness between the two pair
mates, the probability of a pair rearing an extra-pair
chick (after excluding the chick possibly resulting
from brood parasitism on Kerguelen) tended to
increase with relatedness between the two pair mates,
but the trend did not reach significance (CATMOD,
n = 74, Wald χ2 = 3.62, df = 1, P = 0.06; power to
detect a medium effect size = 0.73, power to detect
a large effect size = 0.99).
Within-pair and extra-pair chicks showed similar
levels of heterozygosity, regardless of whether we
used individual heterozygosity or standardized
d2-values as estimates (Mann–Whitney U, n1 = 8,
n2 = 66, both P > 0.3; power to detect a medium
effect size = 0.26). When assessing chick quality
from their survival rate until departure to sea, all the
chicks that were blood-sampled in this study fledged
successfully.
How could a male-biased sex ratio
promote EPCs?
As stated earlier, we expect males to have more
difficulty than females in obtaining a new mate after
becoming widowed or after a divorce on Possession
Island. If this prediction proves to be true, EPCs
would be especially advantageous (if successful) for
the male Wandering Albatrosses that have lost their
females, creating an opportunity to gain additional
paternities. On Possession Island, widowed males
skipped significantly more years than widowed females
before resuming breeding with a new mate (3.2
years ± 0.1 se, n = 259, vs. 2.5 years ± 0.1 se, n = 230;
Wilcoxon rank sum test, z = 5.21, P < 0.0001). The
same phenomenon occurred for divorced individuals
(males: 3.1 years ± 0.3 se, n = 60; females: 1.8 years
± 0.2 se, n = 76; Wilcoxon rank sum test, z = 3.79,
P = 0.0001; to avoid a bias in the distribution of
the number of years skipped due to birds that
already remated after recently losing their mate, the
Tab le 3. Relatedness coefficients between social pair mates according to whether or not their chick had been sired by an extra-pair
male. Means are given ± se; sample size in parentheses.
Possession Island Kerguelen Both islands pooled
Rearing an extra-pair chick 0.151 ± 0.003 (6) 0.144 ± 0.345 (2) 0.150 ± 0.070 (8)
Rearing a within-pair chick 0.026 ± 0.042 (44) 0.067 ± 0.045 (22) 0.040 ± 0.032 (66)
Mann–Whitney test U = 67, 0.05 < P < 0.1 U = 16, P > 0.5 U = 138, P < 0.05
Tab le 4. Logistic regressions determining the factors influencing
the probability of a female having her chick sired by an extra-pair
male and for a male to be cuckolded. Interactions were deleted
from preliminary models (all P > 0.5).
Wald χ2-value df P
Females (n = 26)
Age 1.10 1 0.29
Female experience 1.34 1 0.25
Pair experience 0.80 1 0.37
Female fecundity 0.34 1 0.56
Relatedness 1.78 1 0.18
Intercept 1.96 1 0.16
Likelihood ratio 17.08 20 0.65
Males (n = 31)
Age 1.35 1 0.25
Male experience 1.66 1 0.20
Pair experience 0.11 1 0.74
Male fecundity 0.22 1 0.64
Relatedness 3.05 1 0.08
Intercept 0.02 1 0.88
Likelihood ratio 15.67 25 0.92
© 2006 The Authors
Journal compilation © 2006 British Ornithologists’ Union
Extra-pair paternity in Wandering Albatrosses 73
individuals that lost their mate after 1997 were
excluded from both analyses).
DISCUSSION
What can explain the occurrence of EPP?
The polymorphism in the microsatellite loci used
gave us enough power to detect EPP. The overall rate
of EPP found in this study (10.7%) is the third high-
est observed in a procellariiform species and shows
that, contrary to our expectations, female Wandering
Albatrosses cannot, or do not, thwart all EPC attempts.
This rate, however, is much lower than that observed
in the Waved Albatross (25%; Huyvaert et al. 2000),
and close to that found in the Short-tailed Shearwater
Puffinus tenuirostris, a burrow-nesting petrel (10.8%;
Austin & Parkin 1996). EPP rates were similar among
our study colonies, and were also comparable with
those found by T.M. Burg (unpubl. data) in the Wan-
dering Albatrosses on Marion Island, 900 km west of
Crozet (10%), and on South Georgia in the southern
Atlantic Ocean (10.9%). These similarities suggest that
the phenomenon may be evenly distributed and wide-
spread among the different populations of this species.
Social parents of extra-pair chicks tended to have
a higher relatedness, as estimated with microsatellite
markers, than parents rearing a within-pair chick. In
the Wandering Albatross, however, the average level
of genetic relatedness between mates is similar to
that between pairs chosen at random in the popula-
tion (Bried et al. in press), and the heterozygosity
levels and survival rates to fledging calculated in this
study were similar for within-pair and extra-pair
chicks. Nonetheless, and because Wandering Alba-
trosses spend several years at sea between fledging
and their first return ashore (Tickell 2000), the long-
term consequences of EPP for offspring quality
(estimated through survival rate) cannot be assessed
here. Therefore, the relationships between mate
choice, inbreeding avoidance and higher genetic
compatibility for the offspring are equivocal, and it
is premature to conclude that EPCs may not enable
female Wandering Albatrosses to provide their off-
spring with a better combination of genes. Further
investigations with larger sample sizes, and perhaps
also using more loci (Pemberton 2004), are neces-
sary to clarify the relationships between inbreeding
and EPP and to reject fully the ‘genetic benefits’
hypothesis, as offspring genotype may explain only a
small part of the variance in reproductive success,
undetectable with 75 families.
There was also no evidence for effects of age,
breeding experience and fecundity of the social par-
ents on the occurrence of EPP. This suggests that the
probability of a pair rearing an extra-pair chick does
not depend on the age, the social status or the quality
of the mates. Therefore, our results, combined with
the absence of observations of females seeking EPCs,
are compatible with the hypothesis that female
Wandering Albatrosses do not seek EPCs, that they
do not operate a choice on the cuckolding male, and
that they do not benefit from EPP. Similarly, they
suggest that males target females randomly when
performing EPCs.
However, our genetic study was conducted during
only one breeding season at each locality. Because
EPP rates can show inter-annual variations within
the same population (Graves et al. 1993, Yezerinac
et al. 1995, Petrie & Kempenaers 1998), and even
for the same pairs (Weatherhead 1999), the factors
promoting EPP might also differ from year to year
(Petrie & Kempenaers 1998). In the Wandering Alba-
tross, the very low incidence of divorce, the high
adult survival rate (Bried & Jouventin 2002) and the
extreme fidelity of adults to their breeding localities
(Weimerskirch et al. 1997, Tickell 2000, Cooper &
Weimerskirch 2003) enable the same pairs and the
same extra-pair males to return to the same place at
the onset of the new breeding season. This strongly
suggests that the factors leading the females of this
species to adjust their social mate choice through
EPCs (if any) should be similar from one breeding
season to the next. In addition, the foraging strategy
and ecology of the Wandering Albatross are extremely
buffered against environmental instability caused by
variations in food availability at sea (Weimerskirch
1999, Xavier et al. 2003), so that the influence of
ecological factors on EPP rates (e.g. Graves et al. 1993,
Korpimäki et al. 1996, Petrie & Kempenaers 1998,
Rätti et al. 2001) can also be excluded, at least
when considering those factors operating at sea.
Under these conditions, the only factor susceptible
to show important inter-annual variations should be
the pressure exerted by extra-pair males on paired
females.
Because of the male-biased sex ratio in the Wan-
dering Albatross, divorced and widowed males have
greater difficulties in obtaining a new mate than the
females that are in the same situation (Nel et al. 2003,
this study). For such males, EPC represents the only
means to increase their lifetime reproductive success.
Under these circumstances, forced EPC, opportunis-
tically performed (sometimes during the absence of
74 P. Jouventin et al.
© 2006 The Authors
Journal compilation © 2006 British Ornithologists’ Union
the pair male; see Murphy 1936, p. 557), should
represent the most likely cause of EPP in the Wan-
dering Albatross. Although forced attempts performed
by solitary old males on Possession Island (P. Jouventin
pers. obs.) as well as in South Georgia (Murphy 1936)
have regularly been observed, our results suggest that
some paired males could manage to fertilize extra-
pair females. However, because we obtained genetic
profiles for only a small proportion of the population
on each island, the genuine extra-pair sires may in
fact be males that were not sampled here. Further
investigations paying special attention to genotyping
solitary males in Wandering Albatross colonies would
allow us to test whether cuckolding males are indeed
divorcees or widowers in search of a reproductive
opportunity.
In the Waved Albatross, Huyvaert et al. (2000)
also invoked forced EPC among the potential causes
of EPP, although they provided no demographic data
to support their hypothesis. When considering the
other albatross species in which forced copulations
occur, most EPC attempts are performed by solitary
males in Buller’s Albatross (Richdale 1949), whereas
in the Laysan Albatross, forced EPC attempts gener-
ally involve experienced individuals, both males and
females (Fisher 1971). Furthermore, the EPP rate
found in the Waved Albatross (Huyvaert et al. 2000)
differed from those observed in the Wandering
Albatross. Therefore, the factors and /or the strength
of the selective pressures promoting EPC may vary
among albatross species.
Consequences of EPC in Wandering
Albatrosses
Theory predicts a decreased participation in parental
duties by males if the latter have uncertainty about
their degree of paternity, especially in species which
can trade off current reproduction against future
reproduction (e.g. Mauck et al. 1999, Wink & Dyrcz
1999, Arnold & Owens 2002) and /or in which pater-
nal care is important for successful breeding (Griffith
et al. 2002). Because the Wandering Albatross meets
both criteria (Tickell 2000), a female Wandering
Albatross soliciting EPCs might incur the risk of
reproductive failure, thereby losing the benefits of
the increase in the efficiency of cooperation between
mates in the course of the years (Jouventin et al.
1999). However, all the extra-pair chicks found in
this study fledged successfully. Yet, we do not have
data concerning fledgling body condition or male
investment towards within-pair vs. extra-pair chicks,
and it remains unknown to what extent a male
Wandering Albatross knows whether his female was
involved in EPCs, and whether the latter were forced
or not. Therefore, care must be taken over interpre-
tation; our conclusion on the matter is restricted to
the fact that our data provide no evidence for decreased
paternal investment towards extra-pair chicks.
On the other hand, Wagner (1992) suggested that
males of long-lived and site-faithful species should not
decrease their parental investment despite uncer-
tainty about their paternity, because they might lose
attractiveness (compared with their neighbours), and
thereby incur a greater risk of being divorced at the
onset of the next breeding season. This hypothesis
has been supported by several studies of seabirds
(Moody et al. 2005, Paredes et al. 2005). Also, the-
ory predicts that cuckolded males should be more
tolerant to paternity loss if they have low reproduc-
tive future (Mauck et al. 1999). Wandering Alba-
trosses can live for decades (Weimerskirch & Wilson
2000, data from our demographic survey) and they
show very high fidelity (92.5%; Bried et al. 2003) to
an ‘attachment zone’ (i.e. a few metres radius around
their previous nest) and quasi-absolute fidelity to
their breeding colony (Tickell 2000, Cooper &
Weimerskirch 2003, data from our demographic
survey). In addition, divorce is very costly for indi-
viduals in terms of missed breeding years, the number
of which can exceed 20% of their reproductive
lifespan (Jouventin et al. 1999, this study), and we
showed that on Possession Island, males missed more
years than females after a divorce, as they also do on
the Prince Edward Islands (Nel et al. 2003).
Under these conditions, we suggest that a male
Wandering Albatross that is cuckolded or uncertain
of his paternity might face a trade-off between the
costs of current parental investment and those of
being divorced, in terms of number of future breed-
ing attempts (‘residual reproductive value’; see
Williams 1966 and Stearns 1992 for the former
costs, and the results from this study for the latter).
Although all the extra-pair chicks from this study
fledged successfully, it will be possible, by measuring
feeding rhythms, meal size and chick body condition
at fledging, to know better whether or not cuckolded
males decreased their parental investment. How-
ever, because male Wandering Albatrosses restore
their body reserves more rapidly than females when
foraging at sea during the breeding period (Weimers-
kirch 1995), the costs of rearing an unrelated chick
might be less important for them than those of
divorce. The absence of divorces at the onset of the
© 2006 The Authors
Journal compilation © 2006 British Ornithologists’ Union
Extra-pair paternity in Wandering Albatrosses 75
next breeding cycle in the pairs that had reared an
extra-pair chick is compatible with this interpretation.
CONCLUSION
The mating strategy and the life-history of the Wan-
dering Albatross promote ‘fine tuning’ during mate
choice, so that lifetime reproductive success can be
maximized through long-term pair bonds. This sys-
tem probably worked very well as long as the sex
ratio remained balanced. However, the disequilib-
rium arising from differential mortality due to fish-
eries may have increased the role of EPCs in male
reproductive tactics. In this study, we have provided
indirect but convergent arguments suggesting that
the pressure exerted by males on females results in
EPP in Wandering Albatrosses. Overall, however,
whether EPP yields benefits to females remains
unclear. Despite the theoretical costs of EPCs and
no firm evidence of benefits for female Wandering
Albatrosses, the consequences, if any, for social mate
choice, reproductive performance (at least until the
chick fledges) and pair bond duration seem negligi-
ble in this species. Forced EPCs and EPP have been
reported in several albatross species and may be
common in this seabird group, where paradoxically
mate choice can take several years and is exerted
through elaborate courtship displays (Jouventin et al.
1981, 1999). Selectivity during mate choice and extreme
social mate fidelity in albatrosses (Bried & Jouventin
2002) enable pair mates to achieve higher synchro-
nization during the long foraging trips performed
throughout incubation and chick-rearing as their
common breeding experience increases. Therefore,
female albatrosses are expected not to seek EPCs,
and the only possibility for the males that remain
unpaired after the death of their mate or after a
divorce to increase their lifetime reproductive suc-
cess should be to perform forced EPC attempts.
Field observations combined with blood-sampling of
the cuckolding males remain necessary to determine
the part of forced copulations in EPP in these spe-
cies. In addition, special efforts on genotyping soli-
tary males in Wandering Albatross colonies should
allow us to determine the proportion of divorcees
and widowers in search of a reproductive opportu-
nity among cuckolding males. Finally, comparing
paternal investment towards within-pair and extra-
pair chicks, and determining chick health status before
fledging (e.g. body condition, parasitic load) would
help to assess the potential costs and benefits of EPCs
in albatrosses more accurately.
This study was supported by the French Polar Institute
(IPEV). It was also part of J.B.’s postdoctoral contract at
the Instituto do Mar (IMAR/FCT-PDOC-001/2001-Bird-
Eco and FCT grant SFRH/BPD/20291/2004). Our bird
banding and blood-sampling were approved by the Ethical
Committee of IPEV. We thank all the fieldworkers involved
in the monitoring of Wandering Albatrosses on Possession
Island and at Kerguelen, M. Nicolaus, F. Pawlowski,
F.S. Dobson and C. Bajzak, for field assistance and prelim-
inary analyses. D. Besson helped with the demographic
database and L. Jouventin participated in the demographic
analyses. C. Debain, F. Di Giusto and P. Sourrouille helped
during the genetic analyses, and D.F. Westneat provided
helpful comments on an earlier version of the manuscript.
M. de L. Brooke and two anonymous referees also provided
useful criticism.
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Received 12 December 2005; revision accepted 29 March 2006.
APPENDIX
Allele frequency distribution at ten microsatellite loci in the Wandering Albatrosses from Possession Island and Kerguelen. Sample size
is given in parentheses; allele size is reported in base pairs. The mean number of alleles per locus (nall) ± sd is given for each population.
Locus Allele
Possession Island Kerguelen
Adults (101) Chicks (50) Adults (50) Chicks (25)
11H7 125 0.020 0.030 0.010 0.000
129 0.089 0.090 0.110 0.080
131 0.025 0.040 0.040 0.060
133 0.416 0.490 0.530 0.540
135 0.158 0.160 0.160 0.140
137 0.178 0.110 0.100 0.120
139 0.015 0.020 0.000 0.000
141 0.020 0.020 0.030 0.020
143 0.049 0.010 0.020 0.040
145 0.030 0.030 0.000 0.000
12H8 171 0.896 0.860 0.830 0.820
173 0.069 0.090 0.000 0.000
175 0.005 0.010 0.000 0.000
177 0.030 0.040 0.170 0.180
11H1 156 0.010 0.010 0.000 0.000
164 0.054 0.040 0.070 0.120
166 0.099 0.060 0.090 0.100
168 0.079 0.120 0.030 0.040
170 0.059 0.050 0.060 0.040
172 0.243 0.280 0.260 0.200
174 0.153 0.110 0.070 0.040
176 0.129 0.080 0.150 0.060
178 0.045 0.060 0.100 0.180
78 P. Jouventin et al.
© 2006 The Authors
Journal compilation © 2006 British Ornithologists’ Union
180 0.054 0.090 0.020 0.040
182 0.045 0.070 0.080 0.060
184 0.015 0.010 0.000 0.000
186 0.000 0.000 0.020 0.040
188 0.005 0.010 0.000 0.000
192 0.005 0.000 0.030 0.060
194 0.000 0.000 0.010 0.000
206 0.000 0.000 0.010 0.020
208 0.005 0.010 0.000 0.000
12C8 212 0.005 0.000 0.000 0.000
214 0.015 0.030 0.020 0.040
216 0.614 0.540 0.440 0.420
218 0.346 0.420 0.500 0.500
220 0.020 0.010 0.040 0.040
12E1 214 0.010 0.020 0.030 0.060
218 0.124 0.170 0.180 0.160
220 0.564 0.540 0.490 0.440
222 0.183 0.170 0.200 0.180
224 0.114 0.100 0.090 0.160
226 0.005 0.000 0.010 0.000
De3 123 0.975 0.980 0.940 0.940
125 0.025 0.020 0.060 0.060
De7 118 0.346 0.310 0.330 0.280
120 0.654 0.690 0.670 0.720
De33* 156 0.020 0.000 0.000 0.000
165 0.020 0.000 0.019 0.000
168 0.010 0.033 0.000 0.000
171 0.010 0.000 0.212 0.125
174 0.206 0.283 0.269 0.188
177 0.000 0.000 0.019 0.031
180 0.235 0.250 0.058 0.219
183 0.108 0.100 0.058 0.031
186 0.000 0.033 0.000 0.000
189 0.078 0.083 0.173 0.156
192 0.049 0.033 0.000 0.000
195 0.059 0.017 0.077 0.063
198 0.157 0.100 0.096 0.125
201 0.039 0.017 0.000 0.031
204 0.000 0.000 0.019 0.031
210 0.010 0.017 0.000 0.000
213 0.000 0.033 0.000 0.000
De37 182 0.005 0.010 0.010 0.020
184 0.020 0.031 0.000 0.000
186 0.138 0.143 0.170 0.140
188 0.262 0.255 0.470 0.480
190 0.332 0.337 0.280 0.300
192 0.099 0.102 0.060 0.060
194 0.134 0.102 0.010 0.000
196 0.010 0.020 0.000 0.000
Dc5 168 0.955 0.960 0.960 0.940
170 0.045 0.040 0.040 0.060
nall 6.90 ± 5.02 5.70 ± 4.22
*Only males were considered here (adults: 51 on Possession Island, 26 at Kerguelen; chicks: 30 on Possession Island, 16 at Kerguelen).
†At De33, all the alleles found in females were also present in males; therefore, this locus was included in the calculations.
Locus Allele
Possession Island Kerguelen
Adults (101) Chicks (50) Adults (50) Chicks (25)
APPENDIX Continued
... Females in some species may increase the number and genetic quality of their offspring through extra-pair copulation (EPC) (Griffith et al. 2002;Westneat and Stewart 2003). However, females in other species obtain no benefit from EPC, and EPP can even occur by forced copulation (Jouventin et al. 2007;Hsu et al. 2015). Thus, the reasons for EPC are not as clear for females as they are for males (Forstmeier et al. 2014). ...
... In other, terrestrial, bird species, female preference towards larger males exists and EPP is female driven (Kempenaers et al. 1997). However, among Wandering Albatross (Diomedea exulans), the main cause for EPP might be forced copulation (Jouventin et al. 2007). Sexual size dimorphism is considerable in this species, therefore rejection of EPC risks injury to the female (Jouventin et al. 2007). ...
... However, among Wandering Albatross (Diomedea exulans), the main cause for EPP might be forced copulation (Jouventin et al. 2007). Sexual size dimorphism is considerable in this species, therefore rejection of EPC risks injury to the female (Jouventin et al. 2007). ...
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