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Dispersal has a significant impact on lifetime reproductive success, and is often more prevalent in one sex than the other. In group-living mammals, dispersal is normally male-biased and in theory this sexual bias could be a response by males to female mate preferences, competition for access to females or resources, or the result of males avoiding inbreeding. There is a lack of studies on social mammals that simultaneously assess these factors and measure the fitness consequences of male dispersal decisions. Here we show that male-biased dispersal in the spotted hyaena (Crocuta crocuta) most probably results from an adaptive response by males to simple female mate-choice rules that have evolved to avoid inbreeding. Microsatellite profiling revealed that females preferred sires that were born into or immigrated into the female's group after the female was born. Furthermore, young females preferred short-tenured sires and older females preferred longer-tenured sires. Males responded to these female mate preferences by initiating their reproductive careers in groups containing the highest number of young females. As a consequence, 11% of males started their reproductive career in their natal group and 89% of males dispersed. Males that started reproduction in groups containing the highest number of young females had a higher long-term reproductive success than males that did not. The female mate-choice rules ensured that females effectively avoided inbreeding without the need to discriminate directly against close kin or males born in their own group, or to favour immigrant males. The extent of male dispersal as a response to such female mate preferences depends on the demographic structure of breeding groups, rather than the genetic relatedness between females and males.
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Female mate-choice drives the evolution of
male-biased dispersal in a social mammal
O. P. Ho
, B. Wachter
, M. L. East
, W. J. Streich
, K. Wilhelm
, T. Burke
& H. Hofer
Dispersal has a significant impact on lifetime reproductive suc-
, and is often more prevalent in one sex than the other
group-living mammals, dispersal is normally male-biased and in
theory this sexual bias could be a response by males to female mate
preferences, competition for access to females or resources, or the
result of males avoiding inbreeding
. There is a lack of studies on
social mammals that simultaneously assess these factors and mea-
sure the fitness consequences of male dispersal decisions. Here we
show that male-biased dispersal in the spotted hyaena (Crocuta
crocuta) most probably results from an adaptive response by males
to simple female mate-choice rules that have evolved to avoid
inbreeding. Microsatellite profiling revealed that females pre-
ferred sires that were born into or immigrated into the female’s
group after the female was born. Furthermore, young females
preferred short-tenured sires and older females preferred
longer-tenured sires. Males responded to these female mate pre-
ferences by initiating their reproductive careers in groups contain-
ing the highest number of young females. As a consequence, 11%
of males started their reproductive career in their natal group and
89% of males dispersed. Males that started reproduction in groups
containing the highest number of young females had a higher
long-term reproductive success than males that did not. The
female mate-choice rules ensured that females effectively avoided
inbreeding without the need to discriminate directly against close
kin or males born in their own group, or to favour immigrant
males. The extent of male dispersal as a response to such female
mate preferences depends on the demographic structure of breed-
ing groups, rather than the genetic relatedness between females
and males.
Why is dispersal in most group-living mammals heavily biased
towards males and which social groups offer males the best repro-
ductive prospects? Answers to these questions are important because
dispersal influences crucial components of lifetime reproductive suc-
cess and is a major source of variance in fitness
. In mammals with
polygynous mating systems, females are assumed to incur higher
costs from breeding with close relatives than males
. These sexual
asymmetries in costs are thought to cause sex-biased dispersal
High costs of inbreeding for females may favour female mate-choice
towards immigrant males and discrimination against male kin
and, in theory, female mate-choice can cause male-biased dispersal
We are unaware of any study that has assessed the impact on fitness
of the decision by males about where to initiate their reproductive
career and simultaneously evaluated the ultimate causes proposed
for male-biased dispersal in social mammals. Here we tested whether
male-biased dispersal in spotted hyaenas is driven by female mate-
choice or by one of the other three main factors proposed to
explain male-biased dispersal: male–male competition for access to
, inbreeding avoidance by males
, or competition for
. We used ten years of detailed demographic data from
the entire hyaena population (eight social groups) in the Ngorongoro
Crater (hereafter referred to as ‘Crater’) in Tanzania, a habitat where
processes of natural selection are still intact. To assess fitness benefits
in terms of reproductive success of males after they initiated their
reproductive career in a group we used microsatellite profiling of 426
The spotted hyaena is a large carnivore that lives in social groups or
‘clans’ in which females socially dominate males
. Most but not all
natal males disperse (that is, males leave the clan in which they were
born and immigrate into a new clan)
, whereas female dispersal is
very rare
. Immigrant male social status increases with length of
tenure (time spent living in one group) because males observe strict
social queueing conventions
. Because of the unusual anatomy of the
female genitalia
, female cooperation is a prerequisite for intromis-
, and as a result females exercise considerable mate-choice
and mate promiscuously in clans with numerous reproductively
active males
. Females are likely to incur far higher costs of
inbreeding than males because only females care for offspring, lact-
ating for an exceptionally long period and producing milk with a high
protein, fat and energy content
. Therefore, females would be
expected to avoid breeding with close kin and to be choosier than
males when selecting a mate
In species such as the spotted hyaena, where females mate with
several males in one oestrus cycle and males do not care for their
, females may not be able to distinguish their own father
from other potential mates. A simple female mate-choice rule—
‘avoid males that were members of your group when you were born
and favour males that were born into or immigrated into your group
after your birth’—would reduce the chance of costly inbreeding of
females with their father or with older brothers. Female Crater hyae-
nas generally adhered to this rule, choosing sires that were born into
or immigrated into their clan after their birth more often than
expected from the mean proportion of candidate males that fulfilled
this requirement (Wilcoxon signed-rank test, N 5 64 females of
known age, P 5 0.0001). Most females (81.3%, N 5 64) always
applied the rule; only a single female did not do so more than once.
As a result, most litters (89.6%, N 5 134) were sired by males that
were born into or immigrated into the female’s group after her birth
(Fig. 1).
Young females (less than five years of age) produced litters sired by
males with significantly shorter tenures than older females (Mann–
Whitney U test, U 5 1,416.5, N
5 82 litters by young females,
5 52 litters by older females, P 5 0.001). These results are con-
sistent with the previously reported greater tolerance by young
females of short-tenured males (with less than three years tenure)
than longer-tenured males
, and the greater probability of
offspring of young females being sired by short-tenured rather than
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Strasse 17, D-10315 Berlin, Germany.
Department of Animal and Plant Sciences, University of Sheffield, Western
Bank, Sheffield S10 2TN, UK.
Vol 448
16 August 2007
long-tenured males (assortative mating)
. Given these female pre-
ferences, we would expect males to initiate their reproductive career
in the clan with the highest number of young females, irrespective of
whether this was their natal or another clan.
Spotted hyaena males are likely to assess potential dispersal desti-
nations by undertaking short-term excursions into territories of
other clans
. Before natal adult males in the Crater initiated their
reproductive career in their natal or a non-natal clan, they were
frequently observed on excursions in territories of non-natal clans
(mean proportion of 0.2 6 0.02 of all sightings, N 5 114 males, of
which 62.3% were observed on such excursions). Furthermore, they
were more often observed on such excursions than their twin sisters
during the same period (Wilcoxon signed-rank test, N 5 20 brother–
sister twins, exact P 5 0.013). Thus, males in the Crater are unlikely
to be constrained in assessing potential dispersal destinations.
Of 142 males that were reared in Crater clans and reached adult-
hood, 114 males (80.3%) initiated their reproductive career in a clan
on the Crater floor and 28 males (19.7%) died or dispersed elsewhere.
Of the 114 males, 101 dispersed to a non-natal clan and 13 males
(11.4%) initiated their reproductive career in their natal clan. Eleven
males immigrated into Crater clans from elsewhere. For the 114
Crater-born males that initiated their reproductive career in a
Crater clan, we assessed the key factors hypothesized to influence
male dispersal (Table 1) for all eight clans on the Crater floor. As
predicted, clan selection was influenced by the number of young
females per group (Table 1), and males indeed preferred clans with
the highest number of young females (x
5 22.15, degrees of free-
dom, d.f. 5 1, P , 0.001; Fig. 2).
Males that initiated their reproductive tenure in clans with the
highest number of young females obtained fitness benefits because
male long-term reproductive success increased with the number of
young females present at clan selection (stepwise backward regres-
sion, final model: ln(y) 521.102 1 0.120x, F
5 20.563, r
0.472, P , 0.001; Fig. 3) after considering and removing from the
model the annual rate of mortality of these females (full model:
t 521.07, P 5 0.298). Furthermore, the long-term reproductive
success of such males was higher than that of other males (U 5 8,
5 9 males that initiated their reproductive career in clans with the
highest number of young females, N
5 16 males that initiated their
reproductive tenure in clans that did not contain the highest number
of young females, exact P , 0.0001; Fig. 4).
Males that initiated reproductive activity in the clan with the high-
est number of young females were likely to secure long-term access to
numerous mating partners because survivorship of these females was
above 75% during the first six years of male tenure. Thus, a judicious
clan selection provides males with a high number of females with
which they can develop long-term ‘friendly’ associations as both male
and female tenure increases—a male tactic actively preferred by
females that promotes male reproductive success
Age of mother (years)
Tenure of father (years)
Figure 1
The relationship between the age of the mother on the date of
conception and the tenure of the father. (N 5 134 litters.) Filled circles,
litters sired by males that were born into or immigrated into the mother’s
clan after the mother’s birth. Open circles, litters sired by males that were
present when the mother was born.
Table 1
Test of predictions from the main hypotheses for the evolution of male-biased dispersal
Hypothesis Variable predicted to influence the likelihood of males
to select a clan
Model coefficient Standard error t-ratio P
Avoidance of competition with
other males for access to females
Intensity of male
male competition* 0.001 0.029 0.024 (0. 122 *) 0.981 (0.903*)
Female mate-choice Number of females most likely to breed with
males (‘young females’ as defined in Methods)
0.072 0.034 2.102 (2.064*) 0.036 (0.039*)
Avoidance of breeding with close
female relatives
Number of unrelated adult females with
relatedness of , 0.5
0.005 0.024 0.224 (0.298*) 0.823 (0.766*)
Avoidance of competition for
Number of main prey animals per adult or
yearling spotted hyaena
0.001 0.001 0.464 (0.456*) 0.643 (0.649*)
Discrete choice regression model with the identity of the clan selected by 114 males as dependent variable; log-likelihood of whole model 52229.988.
* ‘Intensity of male
male competition’ refers to the number of reproductively active natal males plus immigrant males. In an alternative model (t-ratios and P values given in parentheses), the number
of reproductively active males per adult female was chosen instead.
Clan rank based on number of
Difference between observed and
expected number of clan selections
Figure 2
Preference of male spotted hyaenas for clans with the highest
number of young females.
Clans were ranked in relation to the number of
young female clan members on each date of clan selection by 114 males; in
each case the clan with the highest number of young females had rank 1.
*P , 0.05; ***P , 0.001.
Number of
females, x
Long-term reproductive success, y
Figure 3
The influence of the number of young female clan members at
clan selection on the long-term reproductive success of male spotted
Long-term reproductive success was the mean number of cubs
produced per year of tenure for 25 males with a minimum tenure of four
years in a clan. The line shows regression of long-term reproductive success
by number of young females, y 5 0.332 3 e
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16 August 2007 LETTERS
As male tenure in a clan increased, the number of females in the
clan that were young at the time the males initiated their reproductive
career in the clan declined because of female mortality; after seven
years of tenure only 59.3% and after eight years only 45.8% of these
females remained alive. This may explain the decrease in reproduct-
ive performance of long-tenured males towards the end of their
, and (secondary) dispersal of 16.7% of Crater males with
tenures exceeding six years, despite the fact that these males had
obtained a high social status in the male hierarchy.
There was little evidence that females produced offspring sired by
close male relatives, thereby risking fitness costs of inbreeding. Only
four of 426 cubs in two of 309 litters (0.6% ) produced by one of 110
females (0.9%) resulted from daughter–father matings. Females that
conceived when their father was a member of their clan produced
only two of 88 litters with their father. None of the five litters that
mothers conceived when their sons were reproductively active in
their clan resulted from mother–son matings. None of the males that
were reproductively active in their natal clan had a sister that con-
ceived during their tenure, so breeding between females and their
brothers could not occur.
Males did not appear to avoid the chance of breeding with close
female relatives, because clan selection was independent of the
number of unrelated females in a clan (Table 1). Furthermore, of
76 males that consorted with (shadowed
) females, the 13 males that
had the opportunity to shadow daughters did not shadow daughters
less often than expected from the mean proportion of daughters
in the pool of adult females (Wilcoxon signed-rank test, exact
P 5 0.542).
Males did not select clans with respect to the likely level of male–
male competition because clan selection was independent of two
measures of competition: the total number of male competitors
and the number of male competitors per adult female (Table 1).
Males thus did not prefer clans with short male social queues, a result
consistent with the idea that when the number of potential mating
partners available to males in a long queue is greater than that in a
shorter queue, males benefit more by joining longer queues
There was also no evidence that clan selection was influenced by
competition for food because selection was independent of the per
capita number of main prey animals in a clan territory (Table 1).
Our findings suggest that female mate-choice is the main factor
determining the clan in which males initiate their reproductive
career. Males that responded best to the observed female mate
preferences had the highest long-term reproducti ve success. We
conclude that female mate-choice represents a sufficient cause for
the evolution of sex-biased dispersal in social mammals.
The observed female preferences were simple mate-choice rules
that radically reduced the chance of costly inbreeding for females.
These rules do not require direct kin discrimination, nor indirect
location-based kin discrimination (such as preference for immigrant
males or discrimination against natal males)
, both important
parameters in theoretical models that seek to explain male dispersal
in social mammals
. Instead, they are consistent with indirect time-
based kin discrimination cues
. This means that an intrinsically
demographic property—fluctuations in the number of young
females in different clans—can lead to male dispersal in the majority
of cases. Thus, changes in the demographic structure of groups will
alter the likelihood of males dispersing, and the demographic struc-
ture of a group in relation to other groups will set the level of emig-
ration from and immigration into that group.
Study area and groups. All approximately 370 hyaenas of the eight Crater clans
were individually known
and studied between April 1996 and April 2006. Natal
adult males that attempted to mate with or shadowed females from their natal
clan or that excluded competing males from access to a female
were termed
‘reproductively active natal males’. Immigrant males were considered members
of the new clan if they initiated non-aggressive interactions with its members
over a period of at least three months. Date of clan selection was the date of first
sighting in the new clan’s territory (immigrant males) or of first observation of
mating, shadowing, or defending (reproductively active natal males). Male
tenure was calculated as the number of days from the date of clan selection until
the date of the event in question.
Social status, clan selection and paternity analysis. To test whether males
preferred to initiate their reproductive career in the clan with the highest number
of young females, the eight clans (including each male’s natal clan) were placed in
a linear rank order on each date a male selected a clan. Rank 1 was the clan with
the highest, and rank 8 the clan with the lowest number of young females. This
expected pattern of clan selection was compared with the observed pattern by
calculating Manly’s standardized selection ratio
B 5 Chesson’s a. Number of
young females included females that were between one and five years of age
Relatedness between individuals was calculated from known pedigrees based on
genetic paternity analyses; first-degree relatives were referred to as ‘closely
related’. Paternity analyses were based on amplification of six highly poly-
morphic microsatellite loci using genetic material from 575 Crater individuals
collected as previously described
. Results are quoted as means 6 standard
error, and probabilities are for two-tailed tests.
Full Methods and any associated references are available in the online version of
the paper at
Received 21 March; accepted 21 June 2007.
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Figure 4
The fitness benefits of male spotted hyaenas that selected clans
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Vol 448
16 August 2007
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Acknowledgements We thank the Tanzania Commission for Science and
Technology for permission to conduct the study, the Tanzania Wildlife Research
Institute, the Ngorongoro Conservation Area Authority, A. Francis, L. Kimaay,
T. Ndooto, G. Orio, H. Richner, D. Thierer, C. Trout, L. Trout, C. Voigt and
W. Wickler for their assistance and suggestions. This study was financed by the
Leibniz Institute for Zoo and Wildlife Research, the Fritz-Thyssen-Stiftung, the
Stifterverband der deutschen Wissenschaft, the Max Planck Society, the German
Academic Exchange Service (DAAD) and the Messerli Foundation.
Author Information Reprints and permissions information is available at The authors declare no competing financial interests.
Correspondence and requests for materials should be addressed to O.P.H.
Vol 448
16 August 2007 LETTERS
Study area and population. The floor of the Ngorongoro Crater in northern
Tanzania covers 250 km
and is inhabited by eight spotted hyaena clans with
between 24 and 65 members each that defended territories of 24 6 4km
15). The Crater population is linked to the neighbouring Serengeti population by
individual movements and gene flow
. Both populations contain reproductively
active natal males and both have a similar incidence of inbreeding (Crater: 0.9%;
: 0.8%) and expected heterozygosity (Crater: 0.824, this work;
: 0.856). Sex, age and social status of individuals were determined
as previously described
. Individuals less than 12 months of age were classified
as cubs, those aged between 12 and 24 months as yearlings, and those 24 months
of age or older as adults. The date of conception was calculated from litter birth
dates on the basis of a gestation period of 110 days
Selection of clans. We assessed hypotheses for the evolution of male-biased
dispersal using a discrete choice (multinomial logistic) regression model
asking which of four variables predicts the clan in which males started their
reproductive career (this may have been their natal clan). The variables were
(1) intensity of male–male competition, (2) number of young females, (3)
number of unrelated females, and (4) mean number of main prey animals per
hyaena (adults and yearlings) on the dates of clan selection (Table 1). Intensity of
male–male competition was the length of the male social queue (that is, the
number of reproductively active natal males plus immigrant males), or the
number of reproductively active males per adult female. In spotted hyaenas,
the length of the male queue may be the more appropriate measure of male–
male competition because males need to build friendly relationships with
females to reproduce and queue for social status, and as a result, levels of aggres-
sion between males are low
From the perspective of each male, young females in non-natal clans were
those between one and less than five years of age on the date of clan selection,
since recent immigrant males rarely have contact with female cubs less than 12
months of age
. Young females in his natal clan were those that were born before
the male’s birth and less than five years of age. The number of unrelated females
was all adult females with a coefficient of relatedness r , 0.5. The mean number
of main prey animals per hyaena was determined from data on mean main prey
density and territory size
divided by the mean clan size (adults and yearlings).
Genetic analysis and survivorship of females. Methods for the collection and
processing of genetic material for paternity analysis have been previously
. Microsatellite loci were typed for 575 Crater individuals including
434 offspring (65.2% of all offspring born during the study period). Paternity
was assessed using maximum-likelihood methods as implemented in Cervus
All immigrant and reproductively active natal males that were clan members
when a litter was conceived were considered to be putative fathers. The mean
proportion of candidate males that were typed was 0.979; for 386 (88.9%) off-
spring all candidate males were typed. Hence, for 426 (98.2%) of the 434 off-
spring from which DNA was isolated, paternity was determined with 95%
confidence. The mean expected heterozygosity was 0.824, total exclusionary
power was 0.999, the mean proportion of individuals typed was 0.992, and the
error rate was 0.0052 and was set at 1.0%. The survivorship of young females was
calculated as the mean proportion of young females present at clan selection that
survived to the end of each year of male tenure.
Statistical analysis. Nonparametric tests, the discrete choice regression model
and the stepwise regression model were performed using Systat 11.0 (Systat
Software Inc.). For the stepwise regression model, natural-logarithm trans-
formation was applied to the dependent variable to satisfy the requirement of
normal distribution of residuals as judged by the Lilliefors test. The significance
of Wilcoxon signed-rank and Mann–Whitney U tests with sample sizes below 30
were based on exact P-values calculated with StatXact 7.0 (Cytel Inc.).
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likelihood-based paternity inference in natural populations. Mol. Ecol. 7, 639
... The same-cohort cubs born in the same clan are raised in a communal den and therefore are familiar with each other. Mother-offspring affiliation was assessed via observations of suckling interactions and confirmed by genetic analyses [39,40]; birthdates of cubs were estimated with an accuracy of ± 7 days [41]. Relatedness and kinship were derived from genetic pedigree information across nine generations. ...
... Relatedness and kinship were derived from genetic pedigree information across nine generations. Over 80% of males born in the population choose one of the eight study clans to breed [10,39] and do so when 3.4 years old on average [10,13]; 85% of these males disperse from their birth clan and join another Crater clan as immigrant males while 15% establish themselves as reproducing 'philopatric' males in their birth clan [10]. Female philopatry is the norm [31,34]. ...
... We paired 296 males that chose a breeding clan during the study period. To control for the potential influence of age and the characteristics of dispersal destinations on clan choice [10,39] pairs consisted of males of the same cohort that were born within 60 days of one another. We assigned these pairs to one of three types: 'littermates' (n = 30 pairs) were brothers of the same litter; 'peers' (n = 63 pairs) were born within 17.7 ± 15.6 days in the same clan to different mothers; 'strangers' (n = 55 pairs) were born within 18.7 ± 15.0 days in different clans to different mothers. ...
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When and where animals reproduce influences the social, demographic and genetic properties of the groups and populations they live in. We examined the extent to which male spotted hyenas ( Crocuta crocuta ) coordinate their breeding-group choice. We tested whether their propensity to settle in the same group is shaped by passive processes driven by similarities in their socio-ecological background and genotype or by an adaptive process driven by kin selection. We compared the choices of 148 pairs of same-cohort males that varied in similarity and kinship. We found strong support for both processes. Coordination was highest (70% of pairs) for littermates, who share most cumulative similarity, lower (36%) among peers born in the same group to different mothers, and lowest (7%) among strangers originating from different groups and mothers. Consistent with the kin selection hypothesis, the propensity to choose the same group was density dependent for full siblings and close kin, but not distant kin. Coordination increased as the number of breeding females and male competitors in social groups increased, i.e. when costs of kin competition over mates decreased and benefits of kin cooperation increased. Our results contrast with the traditional view that breeding-group choice and dispersal are predominantly solitary processes.
... Behavioral studies of individually recognizable hyaenas have allowed researchers to investigate dispersal as well as its potential functions. Spotted hyenas exhibit male-biased dispersal (Höner et al. 2007), but dispersal processes and patterns may vary in different environments. In the Maasai Mara National Reserve, Kenya, most males disperse to new clans from their natal ones, and dispersers seem to experience greater mortality than non-dispersers (Smale et al. 1997), but also more mating opportunities. ...
... The difference in patterns between these two study sites may reflect either variation in constraints on dispersal or variation in the underlying processes of males' decisions to disperse or not, but further work on known individuals using consistent methodology across study sites is needed to address these hypotheses (Davidian et al. 2016). Collectively, studies of individually recognizable spotted hyenas have revealed that female mate choice drives malebiased dispersal (Smale et al. 1997;Engh et al. 2002;East et al. 2003;Höner et al. 2007;Davidian et al. 2016). ...
... For example, some studies have fitted subjects with collars to aid in visual identification or location of subjects for repeated behavioral observations, or to supplement data from direct observations with spatial data from GPS collars, while also using coat patterns to differentiate individuals (Richardson 1987a(Richardson , b, 1991Silwa 1996;Boydston et al. 2003;Califf et al. 2020). Individually known subjects may also be captured to obtain biosamples to complement behavioral data (Höner et al. 2007;Califf et al. 2020). Identification by natural markings has also been combined with various noninvasive methods (Table 1) to produce complementary datasets. ...
Unlabelled: From population estimates to social evolution, much of our understanding of the family Hyaenidae is drawn from studies of known individuals. The extant species in this family (spotted hyenas, Crocuta crocuta, brown hyenas, Parahyaena brunnea, striped hyenas, Hyaena hyaena, and aardwolves, Proteles cristata) are behaviorally diverse, presenting an equally diverse set of logistical constraints on capturing and marking individuals. All these species are individually identifiable by their coat patterns, providing a useful alternative to man-made markings. Many studies have demonstrated the utility of this method in answering a wide range of research questions across all four species, with some employing a creative fusion of techniques. Despite its pervasiveness in basic research on hyenas and aardwolves, individual identification has rarely been applied to the conservation and management of these species. We argue that individual identification using naturally occurring markings in applied research could prove immensely helpful, as this could further improve accuracy of density estimates, reveal characteristics of suitable habitat, identify threats to population persistence, and help to identify individual problem animals. Supplementary information: The online version contains supplementary material available at 10.1007/s42991-022-00309-4.
... They live in matrilineal societies that are structured by linear dominance hierarchies wherein an individual's social rank, which is not dependent on body size or fighting ability, determines access to resources and fitness (15,(20)(21)(22)(23). Hyena societies are also characterized by strong fission-fusion dynamics. Individuals mainly travel, rest, and forage alone or in small subgroups ("fission") that can "fuse" into larger groups (20,24,25). The spotted hyenas from our study population reside in the Masai Mara National Reserve (MMNR), Kenya, a savanna habitat that supports high densities of herbivores and carnivores (26). ...
... They also eat insects or scavenge when ungulate prey numbers are low. Second, they live in fission-fusion societies (20,24,25), where the compositions of subgroups of hyenas change many times per day, allowing hyenas opportunities to interact with different members of the clan throughout the day (75). Furthermore, the dispersal of immigrant males among neighboring clans diversifies the gene pool in this population (25); immigrant males sired the majority of cubs in our studied clans and because of this, overall clan relatedness was very low (76). ...
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There is a gap in knowledge regarding the genomic diversity and variation of the gut microbiome across a host’s life span and across multiple generations of hosts in wild mammals. Using two types of sequencing approaches, we found that although gut microbiomes were individualized and temporally variable among hyenas, they correlated similarly to large-scale changes in the ecological conditions experienced by their hosts.
... R. Soc. B 378: 20220308 hierarchy, ranking below all natal individuals [59]. Active dynamics were calculated as changes resulting from reversal of prior orderings, and passive dynamics were calculated by subtracting active dynamics from total dynamics [36]. ...
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Individuals and societies are linked through a feedback loop of mutual influence. Demographic turnover shapes group composition and structure by adding and removing individuals, and social inheritance shapes social structure through the transmission of social traits from parents to offspring. Here I examine how these drivers of social structure feedback to influence individual outcomes. I explore these society-to-individual effects in systems with social inheritance of hierarchy position, as occur in many primates and spotted hyenas. Applying Markov chain models to empirical and simulated data reveals how demography and social inheritance interact to strongly shape individual hierarchy positions. In hyena societies, demographic processes—not status seeking—account for the majority of hierarchy dynamics and cause an on-average lifetime decline in social hierarchy position. Simulated societies clarify how social inheritance alters demographic effects—demographic processes cause hierarchy position to regress to the mean, but the addition of social inheritance modifies this pattern. Notably, the combination of social inheritance and rank-related reproductive success causes individuals to decline in rank over their lifespans, as seen in the hyena data. Further analyses explore how ‘queens’ escape this pattern of decline, and how variation in social inheritance generates variability in reproductive inequality. This article is part of the theme issue ‘Evolutionary ecology of inequality’.
... Several hypotheses have been developed to explain the mechanisms underlying sex-specific dispersal. For instance, inbreeding avoidance may fuel dispersal in either sex (Pusey, 1987), while mate competition for females might favour male-biased dispersal (Höner et al., 2007). Correspondingly, sex-specific dispersal can play an essential role in the range dynamics of expanding species (Dudaniec et al., 2021;Greenwood, 1980;Li & Kokko, 2019;Trochet et al., 2016). ...
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Invasive species play increasing roles worldwide. Invasions are considered successful when species establish and spread in their exotic range. Subsequently, dispersal is a major determinant of species’ range dynamics. Mermessus trilobatus, native to North America, has rapidly spread in Europe via aerial dispersal. Here we investigated the interplay of ecological and evolutionary processes behind its colonisation success. First, we examined two possible ecological mechanisms. Similar to other invasive invertebrates, the colonisation success of Mermessus trilobatus might be related to human-induced habitat disturbance. Opposite to this expectation, our results showed that densities of Mermessus trilobatus decreased with soil disturbance in grasslands suggesting that its invasion success was not connected to a ruderal strategy. Further, invasive species often escape the ecological pressures from novel enemies in their exotic ranges. Unexpectedly, invasive Mermessus trilobatus was more sensitive to a native predator than native Erigone dentipalpis during our predator susceptibility trials. This indicates that the relation between the invasive spider and its native predator is dominated by prey naïveté rather than enemy release. The remaining three chapters of the thesis investigated the dispersal behaviour of this invasive species. Hitherto, studies of passive aerial dispersal used wind as the primary dispersal-initiating factor despite a recent demonstration of the effects of the atmospheric electric fields on spiders’ pre-dispersal behaviour. During our experiments, only the wind facilitated the flight, although electric fields induced pre-dispersal behaviour in spiders. Consequently, studies around passive aerial dispersal should control electric fields but use wind as a stimulating factor. Rapidly expanding species might be disproportionately distributed in their exotic range, with an accumulation of dispersive genotypes at the leading edge of their range. Such imbalanced spatial segregation is possible when the dispersal behaviour of expanding species is heritable. Our results showed that the dispersal traits of Mermessus trilobatus were heritable through both parents and for both sexes with recessive inheritance of high dispersal ability in this species. Following the heritability experiments, we documented an accelerated spread of Mermessus trilobatus in Europe and tested whether dispersal, reproduction or competing ability was at the source of this pattern. Our results showed that the accumulation of more mobile but not reproductive or competitive genotypes at the expansion front of this invasive species gave rise to an accelerated range expansion by more than 1350 km in under 45 years. Invasive Mermessus trilobatus is inferior to native sympatric species with respect to competing ability (Eichenberger et al., 2009), disturbance tolerance and predation pressure. Nevertheless, the species successfully established in its exotic range and spread by accelerating its expansion rate. Rapid reproduction that balances the high ecological pressures might be the other potential mechanism behind its colonisation success in Europe and deserves further investigation.
... One to 6 years after becoming reproductively mature, most male spotted hyenas disperse to join new social groups Höner et al., 2007), a process that induces a suite of physiological, behavioral, and social changes (Holekamp and Sisk, 2003). It also generates two classes of adult males in most hyena clans: immigrant males who have arrived from other clans and adult natal males who have not yet dispersed. ...
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Introduction Dominance relationships in which females dominate males are rare among mammals. Mechanistic hypotheses explaining the occurrence of female dominance suggest that females dominate males because (1) they are intrinsically more aggressive or less submissive than males, and/or (2) they have access to more social support than males. Methods Here, we examine the determinants of female dominance across ontogenetic development in spotted hyenas ( Crocuta crocuta ) using 30 years of detailed behavioral observations from the Mara Hyena Project to evaluate these two hypotheses. Results Among adult hyenas, we find that females spontaneously aggress at higher rates than males, whereas males spontaneously submit at higher rates than females. Once an aggressive interaction has been initiated, adult females are more likely than immigrant males to elicit submission from members of the opposite sex, and both adult natal and immigrant males are more likely than adult females to offer submission in response to an aggressive act. We also find that adult male aggressors are more likely to receive social support than are adult female aggressors, and that both adult natal and immigrant males are 2–3 times more likely to receive support when attacking a female than when attacking another male. Across all age classes, females are more likely than males to be targets of aggressive acts that occur with support. Further, receiving social support does slightly help immigrant males elicit submission from adult females compared to immigrant males acting alone, and it also helps females elicit submission from other females. However, adult females can dominate immigrant males with or without support far more often than immigrant males can dominate females, even when the immigrants are supported against females. Discussion Overall, we find evidence for both mechanisms hypothesized to mediate female dominance in this species: (1) male and female hyenas clearly differ in their aggressive and submissive tendencies, and (2) realized social support plays an important role in shaping dominance relationships within a clan. Nevertheless, our results suggest that social support alone cannot explain sex-biased dominance in spotted hyenas. Although realized social support can certainly influence fight outcomes among females, adult females can easily dominate immigrant males without any support at all.
... Giant pandas appear to possess a kinship bonded society in spite of their solitary nature most of the time. As observed in giant pandas, male-biased post-natal dispersal is most common mode of dispersal among mammal species and males disperse greater distances than females [56,57]. For these species, females often form stronger associations (female-bonded) with kin than non-kin [31,58,59], and the clustering of kin, facilitated by female philopatry, can result in significantly higher within-community relatedness levels than expected by random assortment [60], which may lead to inbreeding. ...
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Background Indirect interactions between individual solitary mammals, such as the giant panda, are often overlooked because of their nature, yet are important for maintaining the necessary sociality in solitary species. Methods and results Here, we determined the genetic identity of all giant panda individuals in a local population and matched these identities with their associations to determine social network of this solitary animal. Total thirty-five giant panda individuals were found in our field survey, and we constructed genetic and social networks for thirty-three individuals who successfully obtained genetic, age and sex information. The results showed that sex had great impact on both social network and genetic network, and age may have the potential to influence the social network of the giant pandas. Adult males, mostly in the central of the social network, which appeared significantly larger network connections than adult females. Due to the female-biased dispersal pattern of wild giant pandas, male-male pairs showed higher relatedness than female-female ones and multi-generational patrilinear assemblages are expected in the study area. Conclusions The relatedness of individuals has an influence on the formation of community social structure of giant pandas, and indirect interactions among solitary giant pandas potentially function to reduce competition for resources and inbreeding.
... Several hypotheses have been developed to explain the mechanisms underlying sex-specific dispersal. For instance, inbreeding avoidance may fuel dispersal in either sex (Pusey, 1987), while mate competition for females might favour male-biased dispersal (Höner et al., 2007). Correspondingly, sex-specific dispersal can play an essential role in the range dynamics of expanding species (Dudaniec et al., 2021;Greenwood, 1980;Li & Kokko, 2019;Trochet et al., 2016). ...
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Aim The continuous spread of invasive species is attributed to demographic processes and high dispersal rates. Both can change and evolve during range expansion, eventually accelerating spread dynamics. Here, we document such an accelerated spread for one of the most invasive spiders in Europe, the dwarf spider Mermessus trilobatus , and test whether dispersal, reproduction or competitive ability is at the source of this pattern. Location Europe. Time period 1981–2021. Major taxon studied Mermessus trilobatus (Arachnida: Araneae: Linyphiidae). Methods First, we collected records from 21 countries across Europe to document the speed of progression of the invasion front over the last 40 years. Second, we collected live individuals from populations in the longest and more recently invaded areas and compared the dispersal propensity of offspring raised under standardized conditions. Third, we compared the reproduction and competitive ability of females derived from the populations of long‐invaded areas against areas with more recent establishment. Results The progression of the invaded range increased from about 150 km in the 1980s to some 400 km between 2010 and 2020. Dispersal‐related behaviour was nearly twice as frequent in offspring from invasion front populations compared to the core area. By contrast, we found no differences in reproduction or competitive ability among the studied populations. Further, neither joint inheritance nor trade‐offs of dispersal, reproduction or competitive ability were identified. Main conclusion As high dispersal is recessively inherited in M. trilobatus , our results suggest that the accelerated invasion is due to the accumulation of dispersive but not more reproductive or competitive genotypes in newly colonized areas. Given the high climatic amplitude of the species in North America, we expect it to spread over the remaining parts of Europe and large parts of Asia in the coming decades. Accelerated range expansion through the evolution of dispersal behaviour could play a role in numerous arthropod invasions worldwide.
Over the past seventy-five years, long-term population studies of individual organisms in their natural environments have been influential in illuminating how ecological and evolutionary processes operate, and the extent of variation and temporal change in these processes. As these studies have matured, the incorporation of new technologies has generated an ever-broadening perspective, from molecular and genomic to landscape-level analyses facilitated by remote-sensing.
Humans live in large and extensive societies and spend much of their time interacting socially. Likewise, most other animals also interact socially. Social behaviour is of constant fascination to biologists and psychologists of many disciplines, from behavioural ecology to comparative biology and sociobiology. The two major approaches used to study social behaviour involve either the mechanism of behaviour - where it has come from and how it has evolved, or the function of the behaviour studied. With guest articles from leaders in the field, theoretical foundations along with recent advances are presented to give a truly multidisciplinary overview of social behaviour, for advanced undergraduate and graduate students. Topics include aggression, communication, group living, sexual behaviour and co-operative breeding. With examples ranging from bacteria to social mammals and humans, a variety of research tools are used, including candidate gene approaches, quantitative genetics, neuro-endocrine studies, cost-benefit and phylogenetic analyses and evolutionary game theory.
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A long-term study of immigrant male spotted hyenas (Crocuta crocuta) living in large multimale/multifemale groups (clans) demonstrated that males acquire social status by queuing. Maximum likelihood estimates of parameters of a stochastic queuing model that assessed queuing discipline confirmed that immigrant males respected the convention that their positions in a queue of typically 15 or more individuals was determined by their sequence of arrival. Levels of aggression among males were low; males did not attempt to improve their social status through physical contests. Size and body mass did not influence male social status. The stability of queues was insured by an increase in the rate at which males formed coalitions against other males as they rose in social status and by coalitions between high-ranked males and dominant females. High-ranked, long-tenured males chiefly consorted with ("shadowed") and focused their affiliative behavior on females of high reproductive value and disrupted attempts by subordinate males to associate with these females. High-ranked males also supported females against lower-ranked males that harassed them. In contrast, lower-ranked, short-tenured males focused their affiliative behavior on young adult females and rarely shadowed or defended females. Males that did not disperse from their natal clan (nondispersers) quickly acquired top rank in the male social hierarchy. Irrespective of the social status acquired from their mother when young, nondisperser adult males submitted to all adult females.
We used naturally occurring spatial and temporal changes in prey abundance to investigate whether the foraging behavior of a social, territorial carnivore, the spotted hyena (Crocuta crocuta ), conformed to predictions derived from the ideal free distribution. We demonstrate that hyenas in the Ngorongoro Crater, Tanzania, redistributed themselves from less profitable to more profitable areas, even when this required them to undertake foraging trips to areas beyond their clan territory boundary, or required normally philopatric females to emigrate. As expected for a system with rank related access to food resources in the territory, females of low social status foraged more often outside their territory and were more likely to emigrate than dominant females. Probably because Crater hyenas regularly foraged outside their territories, there was no correlation between clan size and prey density within territories, suggesting that clan sizes may have exceeded the carrying capacity of territories. A substantial decline of the hyena population in the Crater from 385 adults in the mid 1960s to 117 in 1996 was most likely due to a substantial decline of their main prey. The decline in the hyena population was associated with a decline in the size of clans but not in the number of clans. The number of clans probably remained constant due to emigration by females from large clans into vacant areas or clans with no adult females, and because hyenas regularly fed in areas containing concentrations of prey beyond their territory boundary. Between 1996 and 2003 annual recruitment rates of Crater hyenas consistently exceeded annual mortality rates, resulting in an almost doubling of the adult population. This increase was most likely due to an increase in prey abundance, a relatively low level of predation on hyenas by lions (Panthera leo ), and an absence of high levels of disease related mortality.
We review available data documenting reproductive skew in the small group of mammals characterized by female dominance over males, focusing mainly on lemurs and spotted hyenas (Crocuta crocuta). Although most females in all lemur species examined here appear to bear young at each opportunity, we know very little about variation in longer-term reproductive success or rates of reproduction among female lemurs. Therefore we cannot draw firm conclusions in regard to reproductive skew among female lemurs except that at present this appears to be slight. However, current data show that female lemurs typically mate with multiple males, and that a substantial fraction of litters containing multiple offspring is sired by more than one male. The extent of reproductive skew in male lemurs varies among species, but there is a slight trend, among the lemur species for which genetic data exist, for male skew to decrease as the intensity of female dominance increases. Variance in reproductive success among female spotted hyenas appears to be substantially greater than it is in male-dominated species in which plural breeding occurs. In this species, female dominance, combined with virilization of the external genitalia, may increase female control over mating to its extreme limit, such that we find very little reproductive skew among males relative to that found in other polygynous mammals. The most dominant male hyenas often achieve very little reproductive success. Overall, reproductive skew among females in female-dominated mammals appears to be the same as or slightly greater than that in male-dominated species, whereas skew among males in female-dominated species generally tends to be relatively low.