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Socio‐genetic structure and mating system of a wild boar population

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Wild boars Sus scrofa have a social organization based on female groups that can include several generations of adults and offspring, and are thus likely matrilineal. However, little is known about the degree of relatedness between animals living in such groups or occupying the same core area of spatial activity. Also, polygynous male mating combined with matrilineal female groups can have strong influences on the genetic structure of populations. We used microsatellite genotyping combined with behavioral data to investigate the fine-scale population genetic structure and the mating system of wild boars in a multi-year study at Châteauvillain-Arc-en-Barrois (France). According to spatial genetic autocorrelation, females in spatial proximity were significantly inter-related. However, we found that numerous males contributed to the next generation, even within the same social group. Based on our genetic data and behavioral observations, wild boars in this population appear to have a low level of polygyny associated with matrilineal female groups, and infrequent multiple paternity. Mortality due to hunting may facilitate the breakup of what historically has been a more predominantly polygynous mating system, and likely accelerates the turnover of adults within the matrilineal groups.
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Socio-genetic structure and mating system of a wild
boar population
C. Poteaux
, E. Baubet
, G. Kaminski
, S. Brandt
, F. S. Dobson
& C. Baudoin
1 CNRS UMR 7153, Laboratoire d’Ethologie, Expe
´rimentale et Compare
´e, Universite
´Paris 13, Villetaneuse, France
2 Office National de la Chasse et de la Faune Sauvage, CNERA – CS, station d’e
´tude sanglier, Cha
ˆteauvillain, France
3 Centre d’Ecologie Fonctionnelle et Evolutive, CNRS, Montpellier Cedex 5, France; & Department of Biological Sciences, Auburn University,
Auburn, AL, USA
matrilines; polygyny; social organization;
genetic structure; wild boar.
Poteaux Chantal, CNRS UMR 7153,
Laboratoire d’Ethologie Expe
´rimentale et
´e, Universite
´Paris 13, 99 Avenue
J. -B. Cle
´ment, 93430 Villetaneuse, France.
Tel: +33 0 1 49 40 32 29; Fax: +33 0 1 49
40 39 75
Editor: Jean-Nicolas Volff
Received 1 October 2008; revised 14
December 2008; accepted 28 December 2008
Wild boars Sus scrofa have a social organization based on female groups that can
include several generations of adults and offspring, and are thus likely matrilineal.
However, little is known about the degree of relatedness between animals living in
such groups or occupying the same core area of spatial activity. Also, polygynous
male mating combined with matrilineal female groups can have strong influences
on the genetic structure of populations. We used microsatellite genotyping
combined with behavioral data to investigate the fine-scale population genetic
structure and the mating system of wild boars in a multi-year study at Chaˆ teau-
villain-Arc-en-Barrois (France). According to spatial genetic autocorrelation,
females in spatial proximity were significantly inter-related. However, we found
that numerous males contributed to the next generation, even within the same
social group. Based on our genetic data and behavioral observations, wild boars in
this population appear to have a low level of polygyny associated with matrilineal
female groups, and infrequent multiple paternity. Mortality due to hunting may
facilitate the breakup of what historically has been a more predominantly
polygynous mating system, and likely accelerates the turnover of adults within
the matrilineal groups.
The evolution of mating systems is an important topic
in behavioral ecology (e.g. Emlen & Oring, 1977; Clutton-
Brock, 1989). In mammalian species, polygynous or poly-
gynandrous mating systems are common (Greenwood,
1980; Dobson, 1982; Komers & Brotherton, 1997). These
mating systems are often characterized by matrilineal asso-
ciations of philopatric females, and they also can have
substantial effects on the genetic properties of populations
(e.g. Sugg et al., 1996). In particular, studies of paternity
suggest that multiple mating by both sexes may be common
among mammals that produce more than one offspring at a
time (e.g. Lacey, Wieczorek & Tucker, 1997; Hoogland,
1998; Lane et al., 2007), and the different contribution of
fathers to the female offspring might have substantial
influences on sexual selection and on the genetic structure
of demes (reviewed by Parker & Waite, 1997; Dobson &
Zinner, 2003). Genetic influences of multiple mating likely
depend on both the number and pattern of patrilines, as well
as the number of offspring produced at each reproduction
and their pattern of survival.
Swine species reflect the mammalian variety of mating
systems, ranging from monogamous pairs to large female
groups with solitary males (Martys, 1991). Wild boars Sus
scrofa form female family groups, from 6 to 30 individuals,
as documented by both direct observations and mark–
recapture studies in semi-natural areas (Mauget et al., 1984;
Boitani et al., 1994). However, very little is known about the
degree of relatedness between animals living in such groups
or occupying the same core range area. Female family groups
might be based on kinship, in which case the conditions for
cooperation through kin selection and the genetic basis
for structured demes might be present (Chesser, 1991a).
Patterns of paternity are also unknown, and these might
also influence kinship and genetic structure (Chesser, 1991b;
Sugg & Chesser, 1994). The purpose of our study was to
examine relatedness structure in social groups of wild boars,
to discern their potential for kin-selected cooperation and to
define the genetic structure caused by their mating patterns
and social groups.
Socio-genetic structure depends thus on both social and
mating relationships among groups, and on inter-group
spatial organization. First, in wild boars, drastic changes in
group structure depend on dispersal pattern, which is
essentially male sex biased as in other mammals (Green-
wood, 1980; Dobson, 1982), and on fusion–fission events
among female groups. Another factor influencing group
Journal of Zoology
Journal of Zoology ]] (2009) 1–10 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 1
Journal of Zoology. Print ISSN 0952-8369
structure is hunting impact (Calenge et al., 2002; Sodeikat &
Pohlmeyer, 2003). In France, wild boars remain an impor-
tant hunted species and are managed as a game animal.
Because it reaches high densities throughout its range, wild
boars are also considered as a pest, due to their impact on
both agricultural and natural ecosystems. Consequently,
wild boar populations are controlled to limit such depreda-
tions. Secondly, even though wild boars are able to travel up
to 10 km per night (radio telemetry studies, Goulding, 1998),
social groups tend to be faithful to a resting place (Boitani
et al., 1994). Moreover, daughters tend to stay with their
mother rather than to constitute a new group (Kaminski
et al., 2005). We expected a high relatedness among group
members and local differentiation between groups of differ-
ent matrilineal origin.
In order to describe the mating system in the studied
population, we estimated the number of males contributing
to the next generation. The mating system in wild boars is
hypothesized to be polygynous based on (1) the spatial
distribution of individuals (Brandt, Vassant & Jullien,
1998); (2) the increase in male aggressiveness during the
rutting season (Beuerle, 1975); (3) male-biased sexual size
dimorphism. According to the polygyny assumption, we
predict that a male would monopolize all females in a group.
As females often belong to different generations, all off-
spring are expected to be full or half-sibs, increasing the
relatedness level between group members. In addition, wild
boars exhibit high reproductive capacity (5.5 0.1 pig-
lets per female in the studied population, Servanty et al.,
2007) compared with other ungulates of similar body size
(Carranza, 1996), which facilitates opportunities for multi-
ple paternity. The hypothesis of polygyny has been chal-
lenged in favor of polygynandry in other mammal species
(snowshoe hare: Burton, 2002; pronghorn antelope: Car-
ling, Wiseman & Byersa, 2003).
Wild boars are a good biological model for the study of a
polygynous social system in a large mammalian species.
However, these nocturnal animals are difficult to observe in
the field, not easy to follow in brush or forest, and stay in
dense cover during daytime (Boitani et al., 1994). Studies of
genealogical relationships in female groups have been based
on small samples of tagged animals, have not applied genetic
analyses (Mauget et al., 1984; Boitani et al., 1994), and were
performed in enclosures or semi-opened populations (Del-
croix, Mauget & Signoret, 1990). In the present study, we
used behavioral and genetic approaches to investigate the
group structure and reproductive system of an uncon-
strained and hunted wild boar population. Demography of
this population, located in an eastern French forest, is well
known because of observation and monitoring for over
25 years (Gaillard et al., 1992; Calenge et al., 2002; Kamins-
ki et al., 2005; Servanty et al., 2007). These demographical
observations were combined with genetic data. We could
thus investigate the fine-scale genetic structure of the popu-
lation and discuss about the potential impact of hunting on
genetic structure. We also estimated how many males con-
tributed to the offspring of a social group, to more fully
understand the current mating system.
Materials and methods
Study area and sampling
Wild boars were studied in the Chaˆ teauvillain-Arc-en-
Barrois national forest in the north-east of France (481020N,
41560E). The forest covers 8500 ha and is surrounded by
other private and communal forests (2500 ha), and all are
mixed broadleaved deciduous woodlands (for more details
on study area see Gaillard et al., 1992; Kaminski et al.,
2005). All methods and protocols used for our research
were approved by the French Agricultural and Forest
Wild boars have been studied and monitored in the
national forest since 1983 by a team from the ‘Office
National de la Chasse et de la Faune Sauvage’ (ONCFS,
National Office of Hunting and Wildlife). Boars were
caught in a network of box traps (Jullien et al., 1988) and
corral traps (Vassant & Brandt, 1995), baited with maize
and intensively used from March to September. Trap sizes
allowed simultaneous multiple captures and/or recaptures
of several animals at the same time (1–30 individuals). Sex
and age of all boars were recorded at first capture. Age was
estimated according to the tooth-eruption procedure de-
scribed by Matschke (1967), validated and adjusted to our
study area (Baubet et al., 1994). Three age classes were
distinguished: young ( 12 months), subadults (individuals
from 13 to 24 months) and adults (over 24 months). Wild
boars have a very short generation time, females becoming
reproductive as young as 12 months.
We obtained samples from two different sources between
October 1999 and February 2002: captured individuals
and hunted individuals. Captured animals (n=214) were
handled for only a few minutes in the early morning.
Animals were tagged with numbered plastic ear tags for
individual identification. Animals caught together in the
same trap were considered as belonging to the same group
and they received the same coloured set of tags, with
individual shape designs for adults and subadults. A punch
was used to collect small pieces of ear tissue, which was then
stored in 70% ethanol solution for subsequent genetic
analyses. To analyze relationships in female groups, we used
five family groups that were intensively followed for demo-
graphic and dynamic data (group composition, fusion–
fission events, death by hunting or disease) as well as for
space occupation over the 3-year sampling period (ONCFS,
unpubl. data).
The second part of our sampling (n= 274) came from
managed hunting in the national forest. This area has been
divided into 27 distinct plots (600–800 ha plot
). Hunting
occurred each year from October to February, in one or two
plots each day, and on almost every weekend. The demo-
graphy of this population has been followed by records from
hunting bags since 1978 (ONCFS, unpubl. data). During
our study period, wild boars were at high population
density. Each hunted animal and each catch were indexed
to a plot, allowing the description of individual and family-
group movements over time.
Journal of Zoology ]] (2009) 1–10 c2009 The Authors. Journal compilation c2009 The Zoological Society of London2
Socio-genetic structure of wild boar P. Chantal et al.
A total of 488 individuals, sampled by specific trapping
and by hunting, were studied in: 1999 (12 subadult females,
and six adult females with 52 piglets); 2000 (33 subadult
females, and 20 adult females with 102 piglets); 2001 (15
subadult females, and eight adult females with 81 winter-
born piglets). Additional hunt animals (n=159) were
sampled throughout the study area, with a substantial
number of tagged individuals helpful to reconstruct family-
group and to estimate group relatedness values.
Microsatellite loci and genetic structure
Twelve microsatellite loci were used (Robic et al., 1996). All
of these dinucleotide loci were highly polymorphic, un-
linked, and without null-alleles. Total DNA was extracted
by Qiamp minikit (Qiagen, Valencia, CA, USA). PCR
amplification was performed according to a standard proto-
col in two ways. For 289 individuals (59% of the sample),
PCR reactions were performed with a
P-dATP (Dallas
et al., 1995). Each PCR was run in a 10 mL volume contain-
ing 30–50 ng of DNA solution, 75 mM of each dNTP except
for dATP (5 mM), 0.04 mLofa
P-dATP, 0.10 mM of each
primer, 1 reaction buffer (50 mM KCl, 0.1% Triton X-
100, 10 mM Tris-HCl, pH 9.0), 1.5 mM MgCl
and 0.05 U of
Taq polymerase (Qiagen) using a PCR T1 thermal cycler
(Biometra, Goettingem, Germany). The thermal cycle pro-
file was an initial denaturation of 3 min at 94 1C; 30
amplification cycles of denaturation for 30 s at 94 1C,
annealing for 30 s at 53–61 1C (according the TM of the
locus) and extension for 45 s at 72 1C; and a final extension
for 5 min at 72 1C. PCR products were electrophoresed on a
standard 6% acrylamide sequencing gel and polymorphism
revealed by autoradiography. Genotypes were determined
at all loci. In the other part of the sample (n=199), only the
seven most polymorphic loci were examined. Genotypes
were produced by Antagene (Lyon, France), using fluores-
cent primers and an automated ABI Prism 310 sequencer
(Applied Biosystems, Foster city, CA, USA). A set of 15 in-
dividuals previously analyzed using radiolabel method were
also analyzed with the ABI system to validate consistency of
results. Allele size estimates were obtained by comparison
with a standard, using Genescan software.
Population differentiation between captured and hunted
samples, deviations from Hardy–Weinberg proportions
(HWE) and linkage equilibrium between loci were tested by
a Markov chain method (5000 steps of dememorization, 100
batches, 1000 iterations per batch) using Genepop 3.1c
(Raymond & Rousset, 1995). These tests were performed
on adults and subadults known to be alive in 2001, to avoid
use of non-independent genotypes caused by sampling
closely related boars. The number of alleles per locus (A),
observed (H
) and unbiased expected (H
) heterozygosi-
ties, and the likely frequency of null alleles (Nulls) were
computed using Cervus 2.0 (Marshall et al., 1998). The
population was tested for recent bottleneck effects (hetero-
zygote excess) with Bottleneck 1.2.02 (Cornuet & Luikart,
1996) assuming 10% multi-step mutations (Piry, Luikart &
Cornuet, 1999).
We used Wright’s F-statistics to analyze within and
between group social structures. We measured the departure
of heterozygosity from the expectation under random mat-
ing at the level of social groups by estimating F
, and F
at the level of the whole population. F
was obtained as
a measure of genetic differentiation among social groups.
F-statistics were estimated according to Weir & Cockerham
(1984), with f=F
and y=F
. Their departure from the
null hypothesis (no population differentiation for F
, and
random mating for F
and F
) was tested using 2500
permutations as implemented in Genetix 3.07 (Belkhir et al.,
1996–1997). F-statistics for piglets and adults were inter-
preted differently, because the former reflects the population
before dispersal and the latter after dispersal (Dobson, 2007).
To analyze the spatial genetic structure within the forest,
a spatial autocorrelation analysis was performed using
Spagedi 1.2 (Hardy & Vekemans, 2002). As wild boar males
disperse and females are philopatric, we expected related-
ness among females to be inversely related to distance.
Statistics were calculated for diploid multi-locus individual
genotypes for different classes of geographical distances
(individuals belonging to the same group (intra-group),
individuals caught in the same field (intra-field) or at 1500,
3000, 6000 and 11 000 m of distance. Spatial analyses were
carried out at the individual level using the kinship coeffi-
cient of Loiselle et al. (1995). Standard error (SE) for each
distance class was estimated by jackknifing over loci. P-
values were obtained by performing 10 000 permutations of
spatial locations of individuals within each class.
Relationships and parentage
Average relatedness (R) among piglets, adults and groups
was estimated using Relatedness 5.0.1 (Queller & Good-
night, 1989). To account for potential bias of related
animals in the estimation of population allele frequencies,
we calculated R-values using global allele frequencies esti-
mated over the entire sample of 488 wild boars. For R
estimations, groups were weighted equally and SEs were
obtained by jackknifing over groups or sites.
Parentage analyses were conducted using Cervus 2.0
(Marshall et al., 1998). We restricted paternity analyses to
cases where both mothers (adult or subadult females) and
their offspring were genotyped. As the wild boar could be a
facultative cooperative breeding species (Kaminski et al.,
2005), we first verified the absence of mismatches between
mother–offspring pair genotypes. All reproductive males
(410 months old, 50 kg) sampled in the studied area
during the breeding season (December–March) were con-
sidered as potential candidate fathers. Males sampled out of
the breeding season at Chaˆ teauvillain-Arc-en-Barrois were
also considered as father candidates when their weight was
compatible with a reproductive status during the last breed-
ing season. A special effort was made by hunters to sample
large males from hunting bags in 2000 and 2001; however,
low returns were obtained in 1999 and 2000 (Table 1). We
Journal of Zoology ]] (2009) 1–10 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 3
Socio-genetic structure of wild boarP. Chantal et al.
ran different simulations of Cervus keeping the following
parameters constant: 10 000 cycles, 100 candidate parents,
90% of loci typed and 1% of loci mistyped. Genetic
paternities were assigned when the combined score given
was 95% as the strict confidence interval, and 80% as the
relaxed level.
Considering litters for which no male was assigned, we
reconstructed the father genotype using Gerud 1.0 (Jones,
2001). This program estimated the minimum number of
males (if mothers were known) contributing to a progeny
array and reconstructed those genotypes based on multi-
locus data. When multiple solutions were found, we ranked
the solutions by likelihood using priority score based on
both allele frequencies and Mendelian segregation.
Microsatellite loci and genetic analysis
Genetic differentiation between captured and hunted sam-
ples was not significant (P=0.075), particularly given that
our sample size was sufficiently large for the statistical test
performed to have a high statistical power (n=214 and 274,
respectively). Thus, individuals were pooled for analyses.
The mean level of genetic diversity (H
) in our wild boar
population was 0.56 (range of H
=0.21–0.87) and a mean
number of alleles of 6.154 (Table 2). Exact tests for HWE
and linkage were performed on adults and subadults known
to be alive in 2001. No pair of loci departed significantly
from linkage disequilibrium after correcting for multiple
tests (adults; k=55, a=0.05; P= 0.021–0.96).
Departures of random mating within social groups (and
from H–W expectations of heterozygosity) as measured by
were not significant over the whole population
=0.008, P=0.21). Genetic structure was assessed for
social groups composed of adults (mainly females for 1999
and 2000) and piglet cohorts separately (Table 3). Except for
1999, offspring exhibited a greater degree of heterozygote
excess compared to adults. In all years, offspring exhibited a
high degree of inter-group genetic differentiation (F
0.15, 0.18 and 0.23, respectively, for 1999, 2000 and 2001).
Deviations of inbreeding from that expected under random
mating within social groups (F
=f) across years and for
offspring ranged from 0.045 to 0.041, while for adults it
varied from 0.009 to 0.1. In the bottleneck analysis, tests
for heterozygote excess were significant for both the sign test
(P=0.008) and the standardized differences test (P=0.004).
Genetic spatial structure
We analyzed average relatedness values (R-values) for each
area when more than three animals were trapped together
(n=19 among the 27 areas), and R-values for females and
males separately. R-values were not significant from zero
for either males or females (R
= 0.037 0.086 and R
0.019 0.112). The mean R-value within area was
0.042 0.078 (range from 0.069 to 0.146). Adult between-
group differentiation was only estimated in 2001 and re-
sulted in a low but significant F
(0.017 0.005, Po0.01).
Table 1 Demographic data from hunting bags and males sampled
national forest
(8500 ha) N
1998–1999 546 271 (49.6%) 107 (39.5%) 10 (9%)
1999–2000 549 272 (49.5%) 96 (35.3%) 36 (37.5%)
2000–2001 535 263 (49.2%) 68 (25.9%) 56 (82%)
national forest
represents the number of individuals (males and
females) shot during the hunting season in the national forest, N
the total of males and their percentage from the total in brackets, N
is the number of large males as candidate father and their
percentage from total of males in brackets, N
is the number
of males really sampled for genetic analyses and their percentage
from total of candidate males.
Table 2 Characteristics of the microsatellite loci polymorphism analyzed in the Cha
ˆteauvillain-Arc-en-Barrois wild boar Sus scrofa population
Locus Chromosome AH
HWE PNulls P
S0155 1 2 0.20 0.21 0.37 0.023 0.09
2 5 0.54 0.50 0.06 0.043 0.25
SW240 2 8 0.68 0.71 0.19 0.029 0.47
3 10 0.77 0.77 0.19 0.001 0.58
4 5 0.48 0.48 0.62 0.018 0.26
5 11 0.80 0.77 0.02 0.014 0.57
5 16 0.83 0.87 0.11 0.023 0.75
6 5 0.29 0.28 0.69 0.021 0.27
8 10 0.78 0.78 0.02 0.0001 0.59
SW911 9 3 0.62 0.66 0.83 0.020 0.36
S0215 13 2 0.22 0.21 0.98 0.001 0.09
S0218 X 2 0 0.38
Mean 6.15 4.52 0.564 0.22 0.567 0.24
Loci used to amplify all the dataset.
The chromosome location is indicated; Ais the number of alleles observed for each locus; the mean, expected (H
) and observed (H
heterozygosity, the probability of H
given H
(HWE P), the likely frequency of null alleles (Nulls) and the probability of parentage exclusion (P
The sample size is 488.
Journal of Zoology ]] (2009) 1–10 c2009 The Authors. Journal compilation c2009 The Zoological Society of London4
Socio-genetic structure of wild boar P. Chantal et al.
Spatial autocorrelation analysis revealed the same pat-
tern of female structure for all 3 years (Fig. 1a for pooled
data): females showed significant negative spatial correla-
tion values (slope=0.005, P=0.04). F
for females were
only significantly different from zero at small scale. For
males, there was no evidence of spatial structuring (Fig.
1b), with all F
values being not significantly different
from zero.
Table 3 Genetic variance within and among generations of wild boar Sus scrofa
Number of
Number of
individuals Sex ratio (F/M) F
1999 parents
0.086 0.003
0.002 0.025
1999 piglets 12 52 0.94 0.041 0.002
0.05 0.024 (0.39 0.147)
2000 parents
39 1.6 0.10 0.004
0.001 0.027
2000 piglets 14 102 0.67 0.0230.001 0.003 0.02 (0.42 0.094)
2001 parents 19 167 0.96 0.0090.027 0.004 0.026
2001 piglets 11 81 0.81 0.045 0.002 0.017 0.029 (0.46 0.089)
Females older than 12 months (adults and subadults) and males older than 2 years were all putative parents and were pooled (all caught during
the breeding season, between October and March).
Average relatedness values within groups of piglets were reported between brackets.
Standard errors of F-statistics and average relatedness coefficients were obtained by jackknifing over loci.
Figure 1 Pattern of spatial autocorrelation ob-
served at the forest level for wild boar Sus
scrofa females and males for the three studied
years. Indices represent kinship coefficients
(Loiselle et al., 1995), given for each point,
1SE (jackknifed over loci). Indices are given
for individuals caught together (intra-group),
caught in the same field (intra-field) and accord-
ing to the logarithm of the distance separating
them (at 1500, 3000, 6000 and 11 000 m).
Journal of Zoology ]] (2009) 1–10 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 5
Socio-genetic structure of wild boarP. Chantal et al.
Relatedness in sampled groups
Individuals, both adults and piglets, were sometimes caught
together in the same trap. Overall, we caught 40 groups
composed of at least three individuals per catch (n= 280
individuals). Captured group size averaged 7.05 individuals
(range=3–21). Average relatedness coefficients observed
for individuals within a group ranged from 0.05 0.08 to
0.88 0.07. Except in four cases where the average related-
ness within groups were o0.1, our data confirmed that
piglets caught in the same trap belonged to the same litter
or were highly related (average relatedness within groups of
0.303 0.176, n=36).
Relationships in female groups
Five family groups were followed from 1999 to 2000 for
family A (all individuals were hunted in 2000) and from 1999
to 2001 for the other families. Individuals were distributed in
three to four overlapping generations (Fig. 2). Almost all
groups were characterized by high individual survival be-
tween years. The group organization was largely conserved,
but with an elevation of female status (e.g. family C). Some
groups exhibited a dynamic organization, with a fission–
fusion pattern (e.g. families B, C and D). Despite regular
follow-up, we lost track of some females that disappeared
due to death or dispersal. Old females were rarely sampled
because they were difficult to capture.
The animals of five groups were analyzed using all
microsatellite loci (n=128 boars). Relationships among
individuals (Fig. 2) were obtained, or checked when they
were known, from genotypic data. Average relatedness
among individuals within family groups ranged from 0.063
(group D, 40 individuals) to 0.31 (group B, 23 individuals).
We observed three separate cases of new female arrival (two
adults and one subadult, Fig. 2) into an already constituted
social group. At the end of 1999, the group E was composed
of two subadult females and their 6–8 month piglets. These
two females were highly related with a value of 0.38. Both
females founded their own group during 2000 and an adult
female with her piglets joined one of these groups. Accord-
ing to age and distribution of alleles among genotypes, she
could have been the mother of the female she joined, but not
of the other female. Another unknown adult female joined
this group next year but was never caught. We compared the
relatedness level between her 3 offspring and both females
of the same group and, according to this indirect estima-
tion, she was more related to the adult female she joined
=0.38) than the other (R
0.09). In group B, a subadult female joined the group with
her piglets in 1999. According to her genotype, she was
potentially the daughter of the old female, and the sister of
some females of her cohort.
Male genetic contribution
The total parentage exclusion probability was, respectively,
0.968 and 0.998 for the first and the second parent (Table 2).
We captured and genotyped 21 litters (five in 1999, eight in
2000 and eight in 2001) and their putative mother. Seven
piglets that did not match with the putative mother geno-
type were eliminated from these analyses. Litter size ranged
from two to six piglets (85 individuals, mean= 4.051 1.21).
Average relatedness among littermates (R
= 0.505 0.173)
and between mother–offspring (R
= 0.47 0.082) were not
Figure 2 Demography and R-values of five groups of wild boars Sus
scrofa sampled between 1999 and 2001 (&, male; , female; , never
caught for genetics; , unknown female joining the group). Individual
disappearance between 2 years was due to emigration, natural death
or hunting.
o1 year 42 years
Ontogeny: ? ??
Piglet Subadult Adult
Journal of Zoology ]] (2009) 1–10 c2009 The Authors. Journal compilation c2009 The Zoological Society of London6
Socio-genetic structure of wild boar P. Chantal et al.
different from the expected value of 0.5 in both cases (t-tests,
NS). For these 21 litters, paternity was assigned to 44 piglets
(451%). For the most stringent analysis, only 12 piglets
(14%) were assigned with 95% confidence. Rates of assign-
ment were always lower than those expected from simula-
tions. This can be due to a higher error rate or to a low
proportion of individuals sampled as true candidate fathers
in the population. From the 44 paternity assignments, 23
concerned at least two piglets of the same litter and corre-
sponded to 10 litters. Of these, five litters were assigned to
only one father while the other five litters were assigned to
more than one father. However, at 95% confidence, only
one litter had two different fathers assigned, four litters had
both piglets (and three piglets in one case) assigned the same
father. Only one male was assigned for the same breeding
season as father of two piglets from two different litters.
Results of the reconstruction of the father’s genotype
using Gerud 1.0 were more conservative; they were compa-
tible with single paternity in 19 litters. In the other two cases,
five piglets exhibited genotypes compatible with their
mother and one putative father, but the last piglet had an
incompatible allele with these two individuals for at least
three loci. Moreover, the reconstructed father genotypes
were compared to verify if a male sired several litters or
not during the same breeding season. When comparisons
were made for litter genotypes from the same family-groups
(12 sows, n=53 piglets), we found that different males
(11 different genotypes) each fertilized one female in the
group. In only one case, a male genotype was compatible as
father of two litters of separate females within the same
social group. These results are consistent with our Cervus
analyses. We obtained the same results when comparing
fertilization of synchronized (o10 days between estrous
peaks) females from different but adjacent areas (four sows,
n=16 piglets).
Group structure
In Chaˆ teauvillain-Arc-en-Barrois, the average group size of
captured individuals was seven, with a high degree of
relatedness among individuals caught in the same trap,
especially among adult females. Consistent with previous
reports, our study confirms the wild boar’s matrilineal
structure of social groups (Kaminski et al., 2005) for up to
three generations in our sample (Fig. 2). Aggregation of
related individuals in family groups, as well as female
philopatry, structured the population genetically (Fig. 1
and strong F
). High relatedness undoubtedly facilitates
the social cohesion observed in wild boars, in terms of
spatial and temporal associations, and of social interactions
among group members (Kaminski et al., 2005). For old
females, benefits of association with their daughter(s) likely
include the opportunity to be ‘helped’ by these close kin in
terms of thermoregulation during cold periods and ‘baby-
sitting’ piglets (Delcroix et al., 1990).
Changes in female social groups occurred in the wild
temporarily due to parturitions and/or to the departure of
subadult females (in 20% of cases, Kaminski et al., 2005).
A pattern of fission–fusion was observed during the study
period, as it has occurred often during long-term studies
conducted in the same population (ONCFS, unpubl. data)
and in other semi-natural populations (Delcroix et al.,
1990). Moreover we observed the arrival of new females
into already established groups, and with no ensuing ag-
gressive interactions (Fig. 2). In these cases, we showed that
new individuals were closely related to some members of
the group. Similar dynamic structure was reported for feral
pigs by Gabor et al. (1999) and Spencer et al. (2005). Such
a dynamic pattern was also genetically documented in the
African elephant and, in this highly matriarchal society,
maternal kinship predicts the fusion of social groups
(Archie, Moss & Alberts, 2006).
Factors influencing boar group-structure
Hunting practices may strongly modify wild boar socio-
genetic structure over the short and long term. During the
hunting season, hunting may facilitate changes in home
range (Sodeikat & Pohlmeyer, 2003) and in group structure
(Maillard & Fournier, 1995). Hunting may also influence
population size, with genetic long-term consequences as
shown by our bottleneck results. Tests for bottleneck effects
were significant in tests, indicating that the wild boar
population at Chaˆ teauvillain-Arc-en-Barrois had been re-
duced in the recent past. In addition to direct observation,
demography of this population is well known from hunting
bags. Records show that the population remained stable at
low density before 1988. Then, the population size quickly
increased from this date to a maximum of more than 1000
individuals shot per year, until a crash was recorded in 1993.
This crash caused the Hunting Federation to change the
hunting rules locally to preserve the population. Since this
change, the population increased up to the present, reaching
a high density of individuals again as elsewhere in Europe
(Monz ´
on & Bento, 2004).
Mating system
According to results from both observation and hunting
records, single paternity of wild boar litters was found to
be common. Litters were consistent with a single father in
19 cases, as opposed to two litters with multiple father
assignments. Monopaternity in feral pigs was reported by
Hampton, Pluske & Spencer (2004) in Australian popula-
tions and one rare case of multiple paternity was observed
by Delgado et al. (2008) in a Mediterranean region. Rearing
of piglets is likely cooperative in this species (Kaminski
et al., 2005), making misidentification between offspring
and their putative mother a distinct possibility. However,
in domestic pigs, it has been observed that sows mate with
different males and often produce litters of mixed paternity
(Aguilera-Reyes et al., 2006; Drake, Fraser & Weary, 2008).
Multiple paternities were also observed in a large proportion
Journal of Zoology ]] (2009) 1–10 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 7
Socio-genetic structure of wild boarP. Chantal et al.
of feral sows from another Australian population (Spencer
et al., 2005). Thus, we tentatively conclude the possibility of
multiple paternity in this population of wild boars, but at a
very low rate during our study period.
The wild boar mating system has been described as
polygynous, with a male dominance hierarchy (Beuerle,
1975; Martys, 1991). Our data showed a low level of
polygyny inside social groups, numerous males contributing
to the next generation (12 sows mated with 11 different
males). For the sows that were receptive at the same time
and living in adjacent areas, we found that their piglets had
different fathers. According to genetic models (Chesser,
1991a,b), female natal philopatry and polygyny may coe-
volve to promote increased coancestry within social lineages
in small family groups. Polygyny in wild boars has also been
assumed because of individual distribution in forest and the
increase in male aggression in winter that coincides with
competition for females (Beuerle, 1975; Goulding, 1998).
However, we were unable to confirm strict monopolization
of females by highly polygynous males, as observed by
Hampton et al. (2004) for feral pigs.
Several factors might explain the absence of complete
polygyny encountered in this wild boar population. The first
one is the absence of dominant males. From 1993 to 2003,
hunting rules prohibited the killing of females weighing
more than 50 kg. According to the hunting records, killed
animals were either young animals of both sexes or adult
males, almost all males were shot before reaching 3 years
old (ONCFS), which is in accordance with results from
long-term studies in Europe (Fruzinski & Labudzki, 2002).
Hunting pressure may have acted as a regulating factor on
genetic diversity by increasing male turnover. A conse-
quence of hunting selection may be the progressive disap-
pearance of old and dominant males, which might
monopolize females during the breeding season. Hunting
regulations lead to selective effects that could be dramatic
for harvested populations. Recent reviews (Coltman, 2007;
Milner, Nilsen & Andreassen, 2007) have called attention to
the potential selective effects of sport hunting on wild
ungulates, particularly for trophy individuals. Recently,
wildlife managers at Chaˆ teauvillain-Arc-en-Barrois consid-
ered such evidence, and amended hunting rules to include
harvesting of large females.
In conclusion, even though a low level of multiple
paternity may occur, the social and mating system of the
wild boar at Chaˆ teauvillain-Arc-en-Barrois is probably best
described as polygynous, as opposed to polygynandrous.
Nonetheless, the degree of polygyny was not high, and lower
levels of polygyny produce lower degrees of genetic differ-
entiation among social groups. Yet wild boars exhibited
significant genetic structure among social groups, probably
due to female philopatry. In addition, single paternity of
litters, which seemed to be most common, produced litters
composed of full rather than half siblings. Male dispersal
and female fidelity to dynamic social groups produced a
remarkable social system in which cooperative reproduction
by females and high genetic diversity are both possible
(Dobson, 2007).
This study was supported financially and logistically by the
Office National de la Chasse et de la Faune Sauvage
(ONCFS). We wish to thank Jacques Vassant, the ‘Fe
tion des chasseurs de Haute-Marne,’ and all students and
volunteers for their help in the field. We are very grateful to
Prof. Monique Monnerot who welcomed C.P. into her
laboratory and to T. Do Chui and N. Dennebouy for
technical help. We also wish to thank N. Busquet, N.
Chaline, A Nettel-Hernanz, L. Say and J.M. Gaillard for
constructive comments. The genetic analysis was supported
by the grant no. 2000/6 between ONCFS and the University
Paris 13, LEEC. This work was conducted under France
legal requirements.
Aguilera-Reyes, U., Zavala-P ´
aramo, G., Valdez-Alarc ´
J.J., Cano-Camacho, H., Garc ´
ıa-L ´
opez, G. & Pescador-
Salas, N. (2006). Multiple mating and paternity determi-
nations in domestic swine (Sus scrofa). Anim. Res. 55,
Archie, E.A., Moss, C.J. & Alberts, S. (2006). The ties that
bind: genetic relatedness predicts the fission and fusion of
social groups in wild African elephants. Proc. Roy. Soc.
Lond. Ser. B 273, 513–522.
Baubet, E., Brandt, S., Jullien, J.M. & Vassant, J. (1994).
Valeur de la denture pour la de
´termination de l’aˆ ge chez le
sanglier (Sus scrofa). Gibier Faune Sauvage 11, 119–132.
Belkhir, K., Borsa, P., Chikhi, L., Goudet, J. & Bonhomme,
F. (1996-1997). GENETIX 3.07, Windows
software for
population genetics. Laboratoire Ge
´nome et Populations,
Montpellier II University, Montpellier, France.
Beuerle, W. (1975). Field observations of aggressive sexual
behaviour in European wild hog (Sus scrofa L.). Zeit.
Tierpsych. 39, 211–258.
Boitani, L., Mattei, L., Nonis, D. & Corsi, F. (1994). Spatial
and activity patterns of wild boars in Tuscany, Italy.
J. Mammal. 75, 600–612.
Brandt, S., Vassant, J. & Jullien, J.M. (1998). Domaine vital
diurne des sangliers en foreˆ t de Chaˆ teauvillain - Arc-en-
Barrois. Bull. Mens. Office Chasse 234, 4–11.
Burton, C. (2002). Microsatellite analysis of multiple pater-
nity and male reproductive success in the promiscuous
snowshoe hare. Can. J. Zool. 80, 1948–1956.
Calenge, C., Maillard, D., Vassant, J. & Brandt, S. (2002).
Summer and hunting season home ranges of wild boar (Sus
scrofa) in two habitats in France. Game Wildl. Sci. 19,
Carling, M.D., Wiseman, P.A. & Byersa, J.A. (2003).
Microsatellite analysis reveals multiple paternity in a
population of wild pronghorn antelopes (Antilocapra
americana). J. Mammal. 84, 1237–1243.
Journal of Zoology ]] (2009) 1–10 c2009 The Authors. Journal compilation c2009 The Zoological Society of London8
Socio-genetic structure of wild boar P. Chantal et al.
Carranza, J. (1996). Sexual selection for male body mass and
the evolution of litter size in mammals. Am. Nat. 148,
Chesser, R.K. (1991a). Gene diversity and female philopatry.
Genetics 127, 437–447.
Chesser, R.K. (1991b). Influence of gene flow and breeding
tactics on gene diversity within populations. Genetics 129,
Clutton-Brock, T.H. (1989). Mammalian mating systems.
Proc. Roy. Soc. Lond. Ser. B 236, 339–372.
Coltman, D.W. (2007). Molecular ecological approaches to
studying the evolutionary impact of selective harvesting in
wildlife. Mol. Ecol. 17, 221–235.
Cornuet, J.M. & Luikart, G. (1996). Description and power
analysis of two tests for detecting recent population
bottlenecks from allele frequency data. Genetics 144,
Dallas, J., Dod, B., Boursot, P., Prager, E.M. & Bonhomme,
F. (1995). Population subdivision and gene flow in Danish
house mice. Mol. Ecol. 4, 311–320.
Delcroix, I., Mauget, R. & Signoret, J.P. (1990). Existence of
synchronisation of reproduction at the level of the social
group of the European wild boar (Sus scrofa). J. Reprod.
Fertil. 89, 613–617.
Delgado, R., Fernande
´z-Llario, P., Azevedo, M., Beja-
Pereira, A. & Santos, P. (2008). Paternity assessment in
free-ranging wild boar (Sus scrofa) – are littermates
full-sibs? Mammal Biol. 73, 169–176.
Dobson, F.S. (1982). Competition for mates and predominant
juvenile male dispersal in mammals. Anim. Behav. 30,
Dobson, F.S. & Zinner, B. (2003). Social groups, genetic
structure, and conservation. In: Animal Behavior and Wild-
life Conservation: 211–228. Festa-Bianchet, M. & Apollo-
nia, M. (Eds). Washington D.C.: Island Press.
Dobson, F.S. (2007). Gene dynamics and social behaviour. In
Rodent societies: 163–172. Wolff, J.O. & Sherman, P.W.
(Eds). Illinois: University of Chicago Press.
Drake, A., Fraser, D. & Weary, D.M. (2008). Parent–
offspring resource allocation in domestic pigs. Behav.
Ecol. Sociobiol. 62, 309–319.
Emlen, S.T. & Oring, L.W. (1977). Ecology, sexual selection,
and the evolution of mating systems. Science 197, 215–223.
Fruzinski, B. & Labudzki, L. (2002). Management of wild
boar in Poland. Z. Jagdwiss. 48, 201–207.
Gabor, T.M., Hellengren, E.C., Van Den Bussche, R.A. &
Silvy, N.J. (1999). Demography, socio-spatial behaviour
and genetics of feral pigs (Sus scrofa) in a semi-arid
environment. J. Zool. (Lond.) 247, 311–322.
Gaillard, J.-M., Pontier, D., Brandt, S., Jullien, J.-M. &
´, D. (1992). Sex differentiation in postnatal growth
rate: a test in a wild boar population. Oecologia 90,
Goulding, M.J. (1998). Current Status and Potential Impact of
Wild Boar (Sus scrofa) in the English Countryside: a Risk
Assessment. Report to Conservation Management
Division C, Ministry of Agriculture, Fisheries and Food.
March 1998.
Greenwood, P.J. (1980). Mating systems, philopatry and
dispersal in birds and mammals. Anim. Behav. 28,
Hampton, J., Pluske, J. & Spencer, P. (2004). A preliminary
genetic study of the social biology of feral pigs in south-
western Australia and the implication for management.
Wildl. Res. 31, 375–381.
Hardy, O.J. & Vekemans, X. (2002). SPAGeDi: a versatile
computer program to analyse spatial genetic structure at
the individual or population levels. Mol. Ecol. Notes 2,
Hoogland, J.L. (1998). Why do female Gunnison’s prairie
dogs copulate with more than one male? Anim. Behav. 55,
Jones, A.G. (2001). Gerud 1.0: a computer program for
the reconstruction of parental genotypes from progeny
arrays using multilocus DNA data. Mol. Ecol. Notes 1,
Jullien, J.M., Vassant, J., Delorme, D. & Brandt, S. (1988).
Techniques de capture de sangliers. Bull. Mens. Office
Chasse 122, 28–35.
Kaminski, G., Brandt, S., Baubet, E. & Baudoin, C. (2005).
Life-history patterns in female wild boars (Sus scrofa L.,
1758): mother–daughter postweaning associations. Can.
J. Zool. 83, 474–480.
Komers, P.E. & Brotherton, P.N. (1997). Female space use is
the best predictor of monogamy in mammals. Proc. Roy.
Soc. Lond. Ser. B 264, 1261–1270.
Lacey, E.A., Wieczorek, J.R. & Tucker, P.K. (1997). Male
mating behaviour and patterns of sperm precedence in
Arctic ground squirrels. Anim. Behav. 53, 767–779.
Lane, J.E., Boutin, S., Gunn, M.R., Slate, J. & Coltman,
D.W. (2007). Relatedness of mates does not predict
patterns of parentage in North American red squirrels.
Anim. Behav. 74, 611–619.
Loiselle, B.A., Sork, V.L., Nason, J. & Graham, C. (1995).
Spatial genetic structure of a tropical understory shrub,
Psychotria officinalis (Rubiaceae). Am. J. Botany 82,
Maillard, D. & Fournier, P. (1995). Effects of shooting with
hounds on size of resting range of wild boar (Sus scrofa L.)
groups in Mediterranean habitat. J. Mount. Ecol. 3,
Marshall, T.C., Slate, J., Kruuk, L.E. & Pemberton, J.M.
(1998). Statistical confidence for likelihood-based paternity
inference in natural populations. Mol. Ecol. 7, 639–655.
Martys, M.F. (1991). Social organisation and behaviour in
the Suidae and Tassuidae. In Biology of Suidae: 65–77.
Barrett, R.H. & Spitz, F. (Eds). Toulouse: Institut de
Recherche sur les Grands Mammife
Matschke, G.H. (1967). Aging European wild hogs by denti-
tion. J. Wildl. Mgmt. 31, 109–113.
Mauget, R., Campan, R., Spitz, F., Dardaillon, M., Goneau,
G. & Pe
´pin, D. (1984). Synthe
`se des connaissances actuelles
Journal of Zoology ]] (2009) 1–10 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 9
Socio-genetic structure of wild boarP. Chantal et al.
sur la biologie du sanglier, perspectives de recherche. Symp.
Int. sur le sanglier, Colloque INRA 22, 15–50.
Milner, J.M., Nilsen, E.B. & Andreassen, H.P. (2007). De-
mographic side effects of selective hunting in ungulates and
carnivores. Conserv. Biol. 21, 36–47.
Monz ´
on, A. & Bento, P. (2004). An analysis of the hunting
pressure on wild boar (Sus scrofa) in the Tr ´
region of northern Portugal. In Wild Boar Research
(2002). A selection and edited papers from the ‘‘4th
International Wild boar Symposium’’. Fonseca, C.,
Herrero, J., Lu ´
ıs, A. & Soares, A.M. (Eds). Galemys 16,
Parker, P.G. & Waite, T.A. (1997). Mating systems, effective
population size, and conservation of natural populations.
In Behavioral approaches to conservation in the wild:
243–261. Clemmons, J.R. & Buchholz, R. (Eds). Cam-
bridge: Cambridge University Press.
Piry, S., Luikart, G. & Cornuet, J.M. (1999). Bottleneck: a
computer program for detecting recent reductions in the
effective population size using allele frequency data.
J. Hered. 90, 502–503.
Queller, D.C. & Goodnight, K.F. (1989). Estimating related-
ness using genetic markers. Evolution 43, 258–275.
Raymond, M. & Rousset, F. (1995). Genepop. version 1.2
population genetics software for exact tests and ecumeni-
cism. J. Hered. 86, 248–249.
Robic, A., Riquet, J. & Yerle, M., Milan, D., Lahbib-Mansais,
Y., Dubut-Fontana, C. & Gellin, J. (1996). Porcine linkage
and cytogenetic maps integrated by regional mapping of 100
microsatellites on somatic cell hybrid panel. Mammal Gen-
ome 7, 438–45.
Servanty, S., Gaillard, J.-M., Allaine
´, D., Brandt, S. &
Baubet, E. (2007). Litter size and fetal sex ratio adjustment
in a highly polytocous species: the wild boar. Behav. Ecol.
18, 427–432.
Sodeikat, G. & Pohlmeyer, K. (2003). Escape movements of
family groups of wild boar Sus scrofa influenced by drive
hunts in Lower Saxony, Germany. Wildl. Biol. 9, 43–49.
Spencer, P., Lapidge, S., Hampton, J. & Pluske, J. (2005). The
socio-genetic structure of a controlled feral pig population.
Wildl. Res. 32, 297–304.
Sugg, D.W. & Chesser, R.K. (1994). Effective population
sizes with multiple paternity. Genetics 137, 1147–1155.
Sugg, D.W., Chesser, R.K., Dobson, F.S. & Hoogland, J.L.
(1996). Population genetics meets behavioral ecology.
Trends Ecol Evol 11, 338–342.
Vassant, J. & Brandt, S. (1995). Adaptation du pie
´geage par
`ge de type corral pour la capture de compagnies
de sangliers (Sus scrofa). Gibier Faune Sauvage, Game
Wildl. 12, 51–61.
Vernesi, C., Crestanello, B. & Pecchioli, E., Tartari, D.,
Caramelli, D., Hauffe, H. & Bertorelle, G. (2003). The
genetic impact of demographic decline and reintroduction
in the wild boar (Sus scrofa): a microsatellite study. Mol.
Ecol. 12, 585–595.
Weir, B.S. & Cockerham, C.C. (1984). Estimating Fstatistics
for the analysis of population structure. Evolution 38,
Journal of Zoology ]] (2009) 1–10 c2009 The Authors. Journal compilation c2009 The Zoological Society of London10
Socio-genetic structure of wild boar P. Chantal et al.
... As they are classified under the same taxon, many of the behavioral patterns observed among European wild boar (Sus scrofa spp.) in their native range are believed to be reflected in wild pigs among invaded ranges. The social organization of European wild boar is complex, but social units are generally characterized as matriarchal social groups (referred to as sounders) or solitary males that only temporarily associate with sounders to mate (Dardaillon 1988;Kaminski et al. 2005;Iacolina et al. 2009;Poteaux et al. 2009;Podgórski et al. 2014a, b;Battocchio et al. 2017;Beasley et al. 2018). Dardaillon (1988) documented a third social unit comprised of males believed to be young, dispersing individuals transitioning to solitary, breeding-aged adults, which has since been observed in other populations. ...
... Dardaillon (1988) documented a third social unit comprised of males believed to be young, dispersing individuals transitioning to solitary, breeding-aged adults, which has since been observed in other populations. Most studies have reported that sounders are typically composed of several closely related females and their offspring; however, genetic determinations of relatedness within social groups have often yielded conflicting reports (Dardaillon 1988;Poteaux et al. 2009;Podgórski et al. 2014a, b;Battocchio et al. 2017). For example, Iacolina et al. (2009) found that wild boar social groups in Italy consisted mostly of unrelated females and their offspring. ...
... Within the USA, wild pigs are presumed to reflect the social organization of European wild boar and sounders are assumed to be primarily composed of closely related females and their dependent offspring. Observational studies of wild pigs in the USA have demonstrated that sounders vary in size and composition (Mayer and Brisbin 2009;Poteaux et al. 2009;Beasley et al. 2018;Gaskamp et al. 2021), ranging from a single female with offspring to groups with over 30 pigs; however, sounders composed of 3-9 individuals have typically been reported. The underlying factors contributing to variance in sounder size are largely unexplored, although some studies have suggested water availability may influence group size in wild pigs (Gabor et al. 1999;Gaskamp et al. 2021). ...
Full-text available
A comprehensive understanding of sociality in wildlife is vital to optimizing conservation and management efforts. However, sociality is complicated, especially for widely distributed species that exhibit substantive behavioral plasticity. Invasive wild pigs (Sus scrofa), often representing hybrids of European wild boar and domestic pigs, are among the most adaptable and widely distributed large mammals. The social structure of wild pigs is believed to be similar to European wild boar, consisting of matriarchal groups (sounders) and solitary males. However, wild pig social structure is understudied and largely limited to visual observations. Using a hierarchical approach, we incorporated genomic tools to describe wild pig social group composition in two disparate ecoregions within their invaded range in North America. The most common social unit was sounders, which are characterized as the association of two or more breeding-aged wild pigs with or without dependent offspring. In addition to sounders, pseudo-solitary females and male-dominated bachelor groups were observed at a greater frequency than previously reported. Though primarily composed of close female kin, some sounders included unrelated females. Bachelor groups were predominantly composed of young, dispersal-aged males and almost always included only close kin. Collectively, our study suggests social organization of wild pigs in their invaded range is similar to that observed among wild boar but is complex, dynamic, and likely variable across invaded habitats.
... We hypothesized that the infection risk would correlate positively with proximity and relatedness to ASF-positive individuals. We expected relationships of infection risk and proximity or genetic relatedness to become weaker with increasing the distance between individuals due to decay in contact rates and genetic similarity Poteaux et al., 2009). Additionally, we explored the differences in effects of relatedness and spatial proximity on infection probability between direct and indirect transmission. ...
... Analysis of spatial-genetic structure was performed with GENALEX 6.5. Autocorrelation coefficients (r) between pairwise genetic and geographic distance matrices were calculated for pre-defined Euclidean distance classes (Supporting Information Figure S1) which correspond to spatial-genetic structure previously observed in wild boar populations Poteaux et al., 2009). Spatial-genetic structure was examined among all individuals as well as among ASF-positive and ASF-negative individuals separately. ...
... Our results showed that relatedness tended to have a larger effect on the probability of infections acquired from live carriers, particularly, at close distances. Such a pattern is consistent with kin-biased associations in wild boar manifested in more regular and longer lasting contacts with relatives (Podgórski, Lusseau et al., 2014;Poteaux et al., 2009) which can facilitate disease transmission. On the other hand, inter-and intra-group contacts in wild boar occur most frequently at a similar spatial scale of 0-2 km Yang et al., 2020). ...
The importance of social and spatial structuring of wildlife populations for disease spread, though widely recognized, is still poorly understood in many host-pathogen systems. In particular, system specific kin relationships among hosts can create contact heterogeneities and differential disease transmission rates. Here, we investigate how distance-dependent infection risk is influenced by genetic relatedness in a novel host-pathogen system: wild boar (Sus scrofa) and African swine fever (ASF). We hypothesized that infection risk would correlate positively with proximity and relatedness to ASF-infected individuals but expected those relationships to weaken with distance between individuals due to decay in contact rates and genetic similarity. We genotyped 323 wild boar samples (243 ASF-negative and 80 ASF-positive) collected in north-eastern Poland in 2014–2016 and modeled the effects of geographic distance, genetic relatedness, and ASF virus transmission mode (direct or carcass-based) on the probability of ASF infection. Infection risk was positively associated with spatial proximity and genetic relatedness to infected individuals with generally stronger effect of distance. In the high-contact zone (0-2 km), infection risk was shaped by the presence of infected individuals rather than by relatedness to them. In the medium-contact zone (2-5 km), infection risk decreased but was still associated with relatedness and paired infections were more frequent among relatives. At farther distances, infection risk further declined with relatedness and proximity to positive individuals, and was 60% lower among unrelated individuals in the no-contact zone (33% in10-20 km) compared with among relatives in the high-contact zone (93% in 0–2 km). Transmission mode influenced the relationship between proximity or relatedness and infection risk. Our results indicate that the presence of nearby infected individuals is most important for shaping ASF infection rates through carcass-based transmission, while relatedness plays an important role in shaping transmission rates between live animals. This article is protected by copyright. All rights reserved
... Furthermore, the amount of harvested wild boars is constantly rising (Massei et al., 2015). It has been previously shown that such high hunting pressure causes variations to the social structure of wild boar populations (Bieber et al., 2019;Poteaux et al., 2009) and instigates earlier sexual maturity, allowing juvenile females to reproduce earlier (Gamelon et al., 2011;Servanty et al., 2011;Toigo et al., 2008). These consequences eventually causes wild boar generation times to shorten and may eventually lead to the higher reproduction and population growth of wild boars (Servanty et al., 2009;Servanty et al., 2011;Toigo et al., 2008). ...
... Our results show an additive effect of hunting and social structure on the levels of reproductive hormones of female wild boars. Thus, the significantly higher progesterone levels we detected in female wild boars in high hunting pressure areas may be linked to the social disruption caused by high hunting pressure (Bieber et al., 2019;Massei et al., 2015;Poteaux et al., 2009). Turner and Tilbrook (2006) suggested that cortisol levels need to be elevated in a sustained manner for a substantial period (>4 days) in female domesticated pigs before repro-duction is negatively affected and, even then, reproduction in some individuals appears to be resistant to its effects. ...
... Furthermore, the mortality among individuals, especially adults, due to hunting has been considered a potential driver of variations in the social organization of wild boar populations. These variations may lead to the disassembly of family groups and thus to a chaotic social structure; disorientation among the remaining yearlings of the group may affect their social status and eventually reproduction (Bieber et al., 2019;Keuling et al., 2010;Poteaux et al., 2009). Additionally, it had been shown that hunting may facilitate the breakup of wild boars' polygynous mating system, due to selective hunting of adult males, and thus may contribute to a higher number of males in the next generation and the early access to reproduction for young males, even within the same social group (Poteaux et al., 2009). ...
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The predation-stress hypothesis has been proposed as a general mechanism to explain the negative effect of predation risk on reproduction, through a chronic activation of the stress response. However, in some cases, stress appears to augment the reproductive potential of mammals. Wild boar (Sus scrofa) populations are on a rise worldwide, despite the high hunting pressure that they are exposed to. This hunting pressure instigates, among other effects, earlier sexual maturity in juvenile females, leading to the shortening of wild boars’ generation time. The mechanism that underlies this earlier sexual maturity under high hunting pressure has not been examined to date. To explore the physiological effects that hunting has on the reproductive system and whether the stress response is involved, we examined steroid hormone levels in the hair of female wild boars in northern Israel, comparing populations exposed to high and low hunting pressure. Furthermore, we compared steroid levels in the hair of female wild boars that were roaming alone or as a part of a group. We found no hormonal signs of stress in the hunted boars. Cortisol levels were low in both the high and low hunting-pressure groups. Yet, progesterone levels were higher in females that were exposed to high hunting pressure. Females roaming in a group also had higher progesterone levels compared to females that were alone, with no distinguishable differences in cortisol levels. These elevations in reproductive hormones that were associated with hunting may lead to a higher reproductive potential in female wild boars. They further show that high hunting pressure does not necessarily lead to chronic stress that impairs the reproductive potential of female wild boars. This data suggests that a reproductive hormonal response may be one of the factors leading to the rapid wild boars population growth worldwide, despite the high hunting pressure.
... For group-living species such as the wild pig, hunting can also affect group composition and stability (Iacolina et al. 2009). In wild pigs, social groups may temporarily break, reform, or exchange individuals (Gabor et al. 1999, Poteaux et al. 2009), but group members usually form stable and long-lasting relationships, even under hunting conditions (Podgórski et al. 2014a). High removal pressure on 1 sex may lead also to changes in the mating systems. ...
... High removal pressure on 1 sex may lead also to changes in the mating systems. Poteaux et al. (2009) andMüller et al. (2018) suggest that high hunting pressure on males might shift from polygyny to promiscuity. ...
... Relatively few studies addressed the effects of recreational hunting on social behavior, social structure, and contact rates of wild pigs, which were altered indirectly by changes in spatial behavior or population structure (e.g., Poteaux et al. 2009;Podgórski et al. 2014bPodgórski et al. , 2018. Others hypothesized that hunting affects group size and composition, which in turn might influence spatial behavior and contact rates. ...
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Wild boar and feral swine (Sus scrofa) numbers are growing worldwide. In parallel, their severe ecological and economic impacts are also increasing and include vehicle collisions, damage to crops and amenities, reduction in plant and animal abundance and richness, and transmission of diseases, the latter causing billions of U.S. dollars in losses to the livestock industry each year. Recreational hunters are the main cause of mortality for this species, and hunting has traditionally been the main method to contain populations of wild pigs. Hunting might affect the behavior of the species, which potentially can lead to these animals moving to new areas or to an increase in disease transmission. This review summarized the evidence that recreational hunting influences the behavior of wild pigs. Twenty-nine studies reported the effect of recreational hunting on social, spatial, and temporal behavior. Although most found that recreational hunting caused changes in home range size, home range shifting, habitat use, and activity patterns, there was little agreement between studies on the size, direction, and duration of these effects. Several studies suggested that other factors, such as season and food availability, equally affect the behavior of this species. Very few studies provided details about the type and frequency of hunting, the number of hunters and dogs (Canis lupus familiaris), the number of animals harvested, or the presence of reserve areas where hunting was forbidden on neighboring sites. As wild pigs adapt to human disturbance, these factors should be investigated to minimize the effects of recreational hunting on the behavior of the species, particularly in the context of disease transmission.
... We hypothesized that the infection risk would correlate positively with proximity (H1, Table 1) and relatedness (H2, Table 1) to ASF-positive individuals. We expected relationships of infection risk and proximity or genetic relatedness to become weaker with increasing distance between individuals due to decay in contact rates and genetic similarity (Podgórski et al., 2014a;Poteaux et al., 2009) (H3, Table 1). Based on current knowledge of wild boar socio-spatial ecology, we analysed infection risk in four distance classes: 1) 'high-contact' zone (0-2 km): social contacts among individuals are most frequent, both within and between groups Yang et al., 2020) , 2) 'medium-contact' zone (2-5 km): interactions among neighbouring social groups , 3) 'low-contact' zone (5-10 km): sporadic contacts between distant groups with non-overlapping home ranges, distance of most natal dispersal (Keuling et al., 2010;Podgórski et al., 2014a;Prévot and Licoppe, 2013), 4) 'no-contact' zone (>10 km): groups do not interact, occasional long-distance movements (Andrzejewski and Jezierski, 1978;Podgórski et al., 2014a). ...
... Analysis of spatial-genetic structure was performed with GENALEX 6.5. Autocorrelation coefficients (r ) between pairwise genetic and geographic distance matrices were calculated for pre-defined Euclidean distance classes ( Supplementary Information: Fig. S1) which correspond to spatial genetic structure previously observed in wild boar populations Podgórski et al., 2014a;Poteaux et al., 2009). Spatial-genetic structure was examined among all individuals as well as among ASF-positive and ASF-negative individuals separately. ...
... This trend was particularly noticeable at the upper range of relatedness distribution, i.e. among close kin or group members. Such a pattern is consistent with kin-biased associations in wild boar, particularly among females and young animals, manifested in more regular and longer lasting contacts (Podgórski et al., 2014b;Poteaux et al., 2009) which facilitate disease transmission. Similarly, kinship was shown to drive bovine tuberculosis infections in badger cubs exposed to infectious females in a natal sett (Benton et al., 2016). ...
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The importance of social and spatial structuring of wildlife populations for disease spread, though widely recognized, is still poorly understood in many host-pathogen systems. In particular, system specific kin relationships among hosts can create contact heterogeneities and differential disease transmission rates. Here, we investigate how distance-dependent infection risk is influenced by genetic relatedness in a novel wild boar ( Sus scrofa ) - African swine fever (ASF) system. We hypothesized that the infection risk would correlate positively with proximity and relatedness to ASF-infected individuals but expected those relationships to weaken with distance between individuals due to decay in contact rates and genetic similarity. ASF infection risk was shaped by the number of infected animals throughout the zone of potential contact (0-10 km) but not beyond it. This effect was the strongest at close distances (0-2 km) and weakened further on (2-10 km), consistent with decreasing probability of contact. Overall, there was a positive association between genetic relatedness to infectees and infection risk within the contact zone but this effect varied in space. In the high-contact zone (0-2 km), infection risk was not influenced by relatedness when controlled for the number of ASF-positive animals. However, infections were more frequent among close relatives indicating that familial relationships could have played a role in ASF transmission. In the medium-contact zone (2-5 km), infection risk and frequency of paired infections were associated with relatedness. Relatedness did not predict infection risk in low- and no-contact zones (5-10 and >10 km, respectively). Together, our results indicate that the number of nearby infected individuals overrides the effect of relatedness in shaping ASF transmission rates which nevertheless can be higher among close relatives. Highly localized transmission highlights the possibility to control the disease if containment measures are employed quickly and efficiently.
... The given differences between male and female wild boar, with females having an overall higher cortisol level compared to males (469.65 ± 241.99 nmol/L compared to 353.67 ± 230.97 nmol/L, respectively), during drive hunts were very prominent to note. Female wild boar form social groups consisting mostly of mothers with their offspring, and are, therefore considered to be matrilineal 18,[54][55][56] . Male wild boar leave the group when reaching puberty 56 . ...
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Hunting can easily be linked to stress in wildlife. Drive hunts performed two to three times in one area during the respective hunting period, are thought to decrease the pressure hunting places on wildlife. Nevertheless, the expression of cortisol—one of the main mammalian stress hormones—is considered to have negative impacts on animals’ well-being if expressed excessively, which may occur during some (especially repeated) hunting events. We explored the effect of drive hunts on cortisol levels in wild boar in Lower Saxony, Germany, compared these cortisol levels to reference values given by a similar study, and investigated the effect of age, sex, and pregnancy. Blood collected from wild boar shot on drive hunts was analysed using a radioimmunoassay. As expected, we observed elevated cortisol levels in all samples, however, we still found significant differences between age groups and sexes, as well as an influence of pregnancy on cortisol levels. The effect of drive hunts on cortisol levels appears to be weaker than predicted, while the effects of other variables, such as sex, are distinct. Only half of the evaluated samples showed explicitly increased cortisol levels and no significant differences were found between sampling months and locations. Group living animals and pregnant females showed significantly higher cortisol levels. The impact of hunting is measurable but is masked by natural effects such as pregnancy. Thus, we need more information on stress levels in game species.
... The presence of empathy in wild boar is expected. Wild boars live in dynamic matrilineal societies composed of females and their offspring of several generations, with fission-fusion patterns and complex social relationships 49,61 . The group units of wild boar are cohesive with strong social bonds 62 and frequent social behaviour, including cooperation 48 and other forms of prosocial behaviour (e.g., alloparental care 63 ), which are conditions favouring the emergence of empathy 64 . ...
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Here, we provide unique photo documentation and observational evidence of rescue behaviour described for the first time in wild boar. Rescue behaviour represents an extreme form of prosocial behaviour that has so far only been demonstrated in a few species. It refers to a situation when one individual acts to help another individual that finds itself in a dangerous or stressful situation and it is considered by some authors as a complex form of empathy. We documented a case in which an adult female wild boar manipulated wooden logs securing the door mechanism of a cage trap and released two entrapped young wild boars. The whole rescue was fast and particular behaviours were complex and precisely targeted, suggesting profound prosocial tendencies and exceptional problem-solving capacities in wild boar. The rescue behaviour might have been motivated by empathy because the rescuer female exhibited piloerection, a sign of distress, indicating an empathetic emotional state matching or understanding the victims. We discuss this rescue behaviour in the light of possible underlying motivators, including empathy, learning and social facilitation.
... In the same species, failed breeding could cause the type of nest adoption (Santema & Kempenaers, 2021) which has also been described in the collared flycatcher (Löhrl, 1957) (see Introduction). Mating and parental care relationships can be flexibly fine-tuned in accordance with availability of either sex not only in birds, but also in mammals, as described, for example, in the wild boar (Sus scrofa), where hunting on males reduced the degree of polygyny (Poteaux et al., 2009). ...
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Certain predominant forms of mating and parental care systems are assumed in several model species among birds, but the opportunistic and apparently infrequent variations of “family structures” may often remain hidden due to methodological limitations with regard to genetic or behavioral observations. One of the intensively studied model species, the collared flycatcher (Ficedula albicollis), is usually characterized by social monogamy with polyterritorial, facultative social polygyny, and frequent extrapair mating and extrapair paternity. During a brood-size manipulation experiment, we observed two females and a male delivering food at an enlarged brood. A combination of breeding phenology data (egg laying and hatching date), behavioral data (feeding rates) from video recordings at 10 days of nestling age, and microsatellite genotyping for maternity and paternity suggests a situation of an unrelated female helping a pair in chick rearing. Such observations highlight the relevance of using traditional techniques and genetic analyses together to assess the parental roles within a population, which becomes more important where individuals may dynamically switch from their main and presupposed roles according to the actual environmental conditions.
... Due to considerable changes in the pig industry worldwide in favour to groups-housing systems, understanding social behaviour of pigs and its impact on welfare has become increasingly important. The wild counterparts of pigs are highly gregarious and form complex hierarchical structures of multigenerational and matrilineal social units centered around several philopatric females associated with their cohorts of offspring [1,2]. Despite occasional breakdown in social cohesion, feral pigs form strong social bonds with related individuals and aggression is very limited [3]. ...
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Mixing gestating sows implies hierarchy formation and has detrimental consequences on welfare. The effects of social stress on the most vulnerable individuals may be underestimated and it is therefore important to evaluate welfare between individuals within groups. This study aimed at investigating the impact of social status and previous experience in the group on well-being of sows housed in large semi-static groups. We assessed aggression (d0 (mixing), d2, d27, d29), body lesions (d1, d26, d84) and feeding order on 20 groups of 46–91 animals. Social status was based on the proportion of fights won during a 6-hr observation period between d0 and d2. Dominants (29%) were those who won more fights than they lost, Subdominants (25%) won fewer fights than they lost, Losers (23%) never won any fight in which they were involved while Avoiders (23%) were never involved in fights. Resident sows (70%) were already present in the group in the previous gestation while New sows (30%) were newly introduced at mixing. Subdominants and Dominants were highly involved in fights around mixing but this was more detrimental for Subdominants than Dominants, Losers and Avoiders since they had the highest body lesion scores at mixing. Avoiders received less non-reciprocal agonistic acts than Losers on d2 ( P = 0.0001) and had the lowest body lesion scores after mixing. However, Avoiders and Losers were more at risk in the long-term since they had the highest body lesions scores at d26 and d84. They were followed by Subdominants and then Dominants. New sows fought more ( P <0.0001), tended to be involved in longer fights ( P = 0.075) around mixing and had more body lesions throughout gestation than Resident sows. Feeding order from one-month post-mixing was influenced both by the previous experience in the group and social status ( P <0.0001). New sows, especially with a low social status, are more vulnerable throughout gestation and could serve as indicators of non-optimal conditions.
One of the factors facilitating the expansion and proliferation of wild boar Sus scrofa is the plasticity of its reproductive biology. Nevertheless, the real influence of maternal and environmental factors on number and sex of the offspring is still controversial. While the litter size was shown to be related with the maternal condition, the strength of this relation remains to be understood, together with the possible role played by environmental conditions. Analogously, it is unclear whether wild boar females can adjust their offspring sex. We investigated multiple aspects of wild boar maternal investment by means of a 10 years-dataset of female reproductive traits and a set of biologically meaningful environmental variables. The maternal condition slightly affected the litter size but not the offspring sex, and environment did not affect the litter size or the offspring sex. Moreover, mothers did not cope with the higher costs entailed by producing sons by placing them in the most advantageous intrauterine position, nor by allocating less resources on daughters. Our set of results showed that the female reproductive investment is quite rigid in comparison with other aspects of wild boar reproductive biology. Wild boar females seem to adopt a typical r-strategy, producing constantly large litters and allocating resources on both sexes regardless of internal and external conditions. Such strategy may be adaptive to cope with environmental unpredictability and an intense human harvest, contributing to explain the extreme success of wild boar within human-dominated landscapes.
The effect of female philopatry on the apportionment of gene diversity within a population is evaluated. Even with random mate selection, the apportionment of gene diversity within and among social lineages (groups of related females) is inherently different than in classically defined demic groups. Considerable excess heterozygosity occurs within lineages without substantial changes in total or population heterozygosity. The proportion of genetic variance among lineages within the population was dependent on the lineage size and the number of male breeders per lineage. The greatest genetic differentiation among lineages was evident when there was one polygynous male breeding within a lineage of philopatric females, a common breeding tactic in mammalian social systems. The fixation indices depicting the genetic structure of the population were found to attain constant values after the first few generations despite the continuous loss of gene diversity within the population by genetic drift. Additionally, the change of gene correlations within individuals relative to the change within the population attains a state of dynamic equilibrium, as do the changes of gene correlations within lineages relative to the total and within individuals relative to within lineages. Comparisons of coancestries and fixation indices for philopatric versus randomly dispersing females indicate that philopatry and polygyny have probably not evolved independently and that promotion of gene correlations among adults rather than offspring has been of primary importance.
While the concept of effective population size is of obvious applicability to many questions in population genetics and conservation biology, its utility has suffered due to a lack of agreement among its various formulations. Often, mathematical formulations for effective sizes apply restrictive assumptions that limit their applicability. Herein, expressions for effective sizes of populations that account for mating tactics, biases in sex ratios, and differential dispersal rates (among other parameters) are developed. Of primary interest is the influence of multiple paternity on the maintenance of genetic variation in a population. In addition to the standard inbreeding and variance effective sizes, intragroup (coancestral) and intergroup effective sizes also are developed. Expressions for effective sizes are developed for the beginning of nonrandom gene exchanges (initial effective sizes), the transition of gene correlations (instantaneous effective sizes), and the steady-state (asymptotic effective size). Results indicate that systems of mating that incorporate more than one male mate per female increase all effective sizes above those expected from polygyny and monogamy. Instantaneous and asymptotic sizes can be expressed relative to the fixation indices. The parameters presented herein can be utilized in models of effective sizes for the study of evolutionary biology and conservation genetics.
When a population experiences a reduction of its effective size, it generally develops a heterozygosity excess at selectively neutral loci, i.e., the heterozygosity computed from a sample of genes is larger than the heterozygosity expected from the number of alleles found in the sample if the population were at mutation drift equilibrium. The heterozygosity excess persists only a certain number of generations until a new equilibrium is established. Two statistical tests for detecting a heterozygosity excess are described. They require measurements of the number of alleles and heterozygosity at each of several loci from a population sample. The first test determines if the proportion of loci with heterozygosity excess is significantly larger than expected at equilibrium. The second test establishes if the average of standardized differences between observed and expected heterozygosities is significantly different from zero. Type I and II errors have been evaluated by computer simulations, varying sample size, number of loci, bottleneck size, time elapsed since the beginning of the bottleneck and level of variability of loci. These analyses show that the most useful markers for bottleneck detection are those evolving under the infinite allele model (IAM) and they provide guidelines for selecting sample sizes of individuals and loci. The usefulness of these tests for conservation biology is discussed.
Analyses of fine-scale and macrogeographic genetic structure in plant populations provide an initial indication of how gene flow, natural selection, and genetic drift may collectively influence the distribution of genetic variation. The objective of our study is to evaluate the spatial dispersion of alleles within and among subpopulations of a tropical shrub, Psychotria officinalis (Rubiaceae), in a lowland wet forest in Costa Rica. This insect-pollinated, self-incompatible understory plant is dispersed primarily by birds, some species of which drop the seeds immediately while others transport seeds away from the parent plant. Thus, pollination should promote gene flow while at least one type of seed dispersal agent might restrict gene flow. Sampling from five subpopulations in undisturbed wet forest at Estación Biologíca La Selva, Costa Rica, we used electrophoretically detected isozyme markers to examine the spatial scale of genetic structure. Our goals are: 1) describe genetic diversity of each of the five subpopulations of Psychotria officinalis sampled within a contiguous wet tropical forest; 2) evaluate fine-scale genetic structure of adults of P. officinalis within a single 2.25-ha mapped plot; and 3) estimate genetic structure of P. officinalis using data from five subpopulations located up to 2 km apart. Using estimates of coancestry, statistical analyses reveal significant positive genetic correlations between individuals on a scale of 5 m but no significant genetic relatedness beyond that interplant distance within the studied subpopulation. Multilocus estimates of genetic differentiation among subpopulations were low, but significant (Fst = 0.095). Significant Fst estimates were largely attributable to a single locus (Lap-2). Thus, multilocus estimates of Fst may be influenced by microgeographic selection. If true, then the observed levels of IBD may be overestimates.
A new method is described for estimating genetic relatedness from genetic markers such as protein polymorphisms. It is based on Grafen's (1985) relatedness coefficient and is most easily interpreted in terms of identity by descent rather than as a genetic regression. It has several advantages over methods currently in use: it eliminates a downward bias for small sample sizes; it improves estimation of relatedness for subsets of population samples; and it allows estimation of relatedness for a single group or for a single pair of individuals. Individual estimates of relatedness tend to be highly variable but, in aggregate, can still be very useful as data for nonparametric tests. Such tests allow testing for differences in relatedness between two samples or for correlating individual relatedness values with another variable.