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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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LETTERS
Female mate-choice drives the evolution of
male-biased dispersal in a social mammal
O. P. Ho
¨
ner
1
, B. Wachter
1
, M. L. East
1
, W. J. Streich
1
, K. Wilhelm
1
, T. Burke
2
& H. Hofer
1
Dispersal has a significant impact on lifetime reproductive suc-
cess
1
, and is often more prevalent in one sex than the other
2
.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
2–7
. 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
1
. In mammals with
polygynous mating systems, females are assumed to incur higher
costs from breeding with close relatives than males
8,9
. These sexual
asymmetries in costs are thought to cause sex-biased dispersal
8,10
.
High costs of inbreeding for females may favour female mate-choice
towards immigrant males and discrimination against male kin
3,11,12
and, in theory, female mate-choice can cause male-biased dispersal
3
.
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
females
2,4,5
, inbreeding avoidance by males
2,6
, or competition for
resources
2,7
. 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
offspring.
The spotted hyaena is a large carnivore that lives in social groups or
‘clans’ in which females socially dominate males
13
. Most but not all
natal males disperse (that is, males leave the clan in which they were
born and immigrate into a new clan)
14
, whereas female dispersal is
very rare
15
. Immigrant male social status increases with length of
tenure (time spent living in one group) because males observe strict
social queueing conventions
14
. Because of the unusual anatomy of the
female genitalia
16
, female cooperation is a prerequisite for intromis-
sion
13,17
, and as a result females exercise considerable mate-choice
18
and mate promiscuously in clans with numerous reproductively
active males
18,19
. 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
20
. Therefore, females would be
expected to avoid breeding with close kin and to be choosier than
males when selecting a mate
9,21
.
In species such as the spotted hyaena, where females mate with
several males in one oestrus cycle and males do not care for their
young
18,19
, 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
1
5 82 litters by young females,
N
2
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
14
, and the greater probability of
offspring of young females being sired by short-tenured rather than
1
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Strasse 17, D-10315 Berlin, Germany.
2
Department of Animal and Plant Sciences, University of Sheffield, Western
Bank, Sheffield S10 2TN, UK.
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long-tenured males (assortative mating)
18
. 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
15,22
. 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
2
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
1,23
5 20.563, r
2
5
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,
N
1
5 9 males that initiated their reproductive career in clans with the
highest number of young females, N
2
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
18
.
0
0
1
1
2
2
3
3
4
4
5
5
6
6
7
7
8
8
9
91011
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
resources
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.
–15
–10
–5
0
5
10
15
20
12345678
Clan rank based on number of
y
oun
g
females
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.
0
1412108642016
0.5
1.0
1.5
2.0
Number of
y
oun
g
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
hyaenas.
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
0.120x
.
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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
tenures
18,19
, 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
14
) 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
23
.
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)
3,11,12
, both important
parameters in theoretical models that seek to explain male dispersal
in social mammals
3
. Instead, they are consistent with indirect time-
based kin discrimination cues
24
. 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.
METHODS SUMMARY
Study area and groups. All approximately 370 hyaenas of the eight Crater clans
were individually known
15
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
25
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
26
B 5 Chesson’s a. Number of
young females included females that were between one and five years of age
18
.
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
18
. 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 www.nature.com/nature.
Received 21 March; accepted 21 June 2007.
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2.0
1.5
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0.5
0.0
2.5
Fewer
Youn
g
females in selected clan
Long-term reproductive success
Figure 4
|
The fitness benefits of male spotted hyaenas that selected clans
with the highest number of young females.
Long-term reproductive success
calculated as in Fig. 3. The box indicates the interquartile range around the
median (line inside the box), and the vertical error bars represent values plus
or minus 1.5 times the interquartile range.
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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
www.nature.com/reprints. The authors declare no competing financial interests.
Correspondence and requests for materials should be addressed to O.P.H.
(hoener@izw-berlin.de).
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METHODS
Study area and population. The floor of the Ngorongoro Crater in northern
Tanzania covers 250 km
2
and is inhabited by eight spotted hyaena clans with
between 24 and 65 members each that defended territories of 24 6 4km
2
(ref.
15). The Crater population is linked to the neighbouring Serengeti population by
individual movements and gene flow
27
. Both populations contain reproductively
active natal males and both have a similar incidence of inbreeding (Crater: 0.9%;
Serengeti
18
: 0.8%) and expected heterozygosity (Crater: 0.824, this work;
Serengeti
18
: 0.856). Sex, age and social status of individuals were determined
as previously described
15
. 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
16
.
Selection of clans. We assessed hypotheses for the evolution of male-biased
dispersal using a discrete choice (multinomial logistic) regression model
28
by
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
14
.
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
25
. 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
15
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
described
18,29
. 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
30
.
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.).
27. Albert, R. Genstruktur und Genfluß in ausgewa
¨
hlten Populationen der Tu¨pfelhya
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(Crocuta crocuta). PhD thesis, Freie Universita
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t Berlin (2002).
28. McFadden, D. in Frontiers in Econometrics (ed. Zarembka, P.) 105
142 (Academic
Press, New York, 1974).
29. Wilhelm, K. et al. Characterization of spotted hyena, Crocuta crocuta,
microsatellite loci. Mol. Ecol. Notes 3, 360
362 (2003).
30. Marshall, T. C., Slate, J., Kruuk, L. E. B. & Pemberton, J. M. Statistical confidence for
likelihood-based paternity inference in natural populations. Mol. Ecol. 7, 639
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doi:10.1038/nature06040
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©2007
Publishing
Group
... Furthermore, offspring of high-ranking mothers benefit from silver spoon effects; they grow faster, have a higher chance of survival to adulthood, start to reproduce earlier and have a higher lifetime reproductive success (210,212). Dispersal is strongly male-biased, with approximately 85% of males and 1.5% of females leaving their birth clan and immigrating into another clan or founding a new clan in a vacated area (211,213). The mating system is polygynandrous. ...
... For those males that do prospect, the probability of dispersing to a given clan is determined from a multinomial distribution where probability of selecting a given clan is equal to the proportion of all young females (1 -5yo) living in the crater that are found in the clan. This age range is based on work by (213) concerning spotted hyena dispersal. ...
... Potential males are determined by the female-mate choice rule (213). Assuming there is more than one potential male, the female will select the one with the highest tenure (i.e., that has inhabited the clan the longest). ...
Article
The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.
... Physical contests between immigrant males to increase their status are rare, thus high-ranking immigrant males are those with the longest tenure (East and Hofer, 2001). Although most breeding males in a clan are immigrants, occasionally males do not disperse and become breeding males in their natal clan, in which case they join the breeding male hierarchy ahead of the immigrant males (East and Hofer, 2001;Höner et al., 2007). ...
... The unusual anatomy of female reproductive organs (Matthews, 1939), in particular the penile clitoris positioned between the hind legs, ensures that copulation cannot be successful without the complete cooperation of females (East et al., 1993). Genetic studies on the paternity of offspring provide strong evidence that female mate-choice preferences do not necessarily match that of breeding males (Engh et al., 2002;East et al., 2003;Höner et al., 2007). For example, high-ranking males attempt to monopolize access to high-ranking females (East and Hofer, 2001;Szykman et al., 2001) but genetic paternity of cubs produced by highranking mothers is not skewed toward high-ranking males (Engh et al., 2002;East et al., 2003;Höner et al., 2007) and there is little evidence that coercion of females is an effective tactic to secure paternity . ...
... Genetic studies on the paternity of offspring provide strong evidence that female mate-choice preferences do not necessarily match that of breeding males (Engh et al., 2002;East et al., 2003;Höner et al., 2007). For example, high-ranking males attempt to monopolize access to high-ranking females (East and Hofer, 2001;Szykman et al., 2001) but genetic paternity of cubs produced by highranking mothers is not skewed toward high-ranking males (Engh et al., 2002;East et al., 2003;Höner et al., 2007) and there is little evidence that coercion of females is an effective tactic to secure paternity . Thus female mate-choice is a likely source of sexual conflict in spotted hyenas . ...
Article
Full-text available
Infanticide by adult females includes any substantial contribution to the demise of young and inevitably imposes fitness costs on the victim’s genetic fathers, thereby generating sexual conflict with them. Few if any studies have quantified the impact of infanticide by females on male reproductive success, the magnitude of sexual conflict this causes and possible counterstrategies males use against infanticidal females. We examine these topics in spotted hyena (Crocuta crocuta) clans, where females socially dominate breeding males and strong female mate-choice is independent of male social status. We consider two causes of infanticide by females, violent attacks on cubs and fatal maternal neglect. Violent attacks are predicted during periods of social instability at the top of the female linear dominance hierarchy and victims are expected to predominantly have mothers above median rank. Fatal maternal neglect, when starving litters are abandoned, is associated with monopolization of food in clan territories by high-ranking females, and victims are predicted to have mothers below median rank. Female perpetrators of violent attacks are expected to reduce the reproductive success of the fathers of their victims more than perpetrators of fatal maternal neglect. We tested these predictions using 30 + years of data (54 recorded violent attacks, 43 cases of fatal maternal neglect, DNA profiling of 1,671 individuals). Using long-term observations at communal dens we investigated whether males use counterstrategies against infanticide reported in other mammals. Due to female social dominance over breeding males, strong female mate-choice and prolonged offspring dependence on lactation in spotted hyenas, we predicted that these counterstrategies were unlikely to be used by males against females, thus no incidences of them were likely to be observed. Our results revealed that breeding males lost cubs to violent attacks at all stages of their reproductive tenure and to perpetrators with whom they did not sire offspring. Amongst known sources of paternity loss, violent attacks comprised 12.2% and maternal neglect 9.8% of cases. Violent attacks significantly reduced offspring production rates of breeding males, suggesting that infanticide by females generates sexual conflict. As predicted, no evidence of males using counterstrategies against infanticide by females were observed.
... However, it is also the case that individuals can be highly plastic in their dispersal behaviour, making decisions that maximise fitness. Dispersal decisions can be influenced by a variety of factors including ecological constraints (Nelson-Flower et al. 2018), the availability and quality of mates (Packer & Pusey 1987;Höner et al. 2007), as well as the composition and genetic structure of groups (Rood 1987). ...
... Finally, dominants may also voluntarily abandon their position, commonly by dispersing from their group. The abandonment of position tends to be associated with individuals trying to maximise their fitness, resulting from reduced breeding opportunities in their resident group relative to other neighbouring groups (Packer & Pusey 1987;Höner et al. 2007). Dominants are commonly exposed to a multitude of distinct threats to their tenure, and the factors influencing tenure loss are likely to vary with the cause of tenure loss, possibly even having contrasting effects. ...
... One way subordinate males can do this is to increase the breeding rate of dominant males (Snyder-Mackler et al. 2012), for example, by increasing the number of breeding females they can control within their group or by increasing the survival of the dominant male's offspring (Feh 1999 However, even for immigrant male dominants, as their tenure progresses, unrelated females will die and be replaced by daughters recruiting into breeding positions. Subsequently, their pool of available breeding females will decline along with their reproductive success (Wikberg et al. 2017); which can drive secondary dispersal in long tenured breeding males (Höner et al. 2007 et al. 2000). Therefore, to acquire reproductively viable positions of dominance male meerkats must disperse (Spong et al. 2008). ...
Thesis
In group-living species with strong reproductive skew, acquiring a position of dominance is often essential for maximising fitness, and where the frequency of lifetime dominance acquisition is low, substantial variation in fitness among individuals can arise. However, even among dominant individuals there is still substantial variance in fitness attainment, driven by processes such as the maintenance of status, fecundity, and fertility. In this thesis, to understand better the variation in fitness among individuals, I use 26 years of long-term data to investigate the acquisition of dominance and the subsequent maintenance of status and group persistence in a population of cooperatively breeding meerkats, Suricata suricatta, located in the Southern Kalahari. In Chapters 3 and 4, I characterise the distinct routes that subordinates of both sexes pursue to acquire dominance. While there is variation in the frequency that certain dominance routes are used, I find no substantial differences between routes in the traits that determine the acquisition of dominance, the length of tenures or the reproductive success of dominants. In Chapter 5, I distinguish between the reproductive consequences of intrasexual competition from within and outside the group for dominant males. This reveals that while resident immigrant subordinate males compete with the dominant male for reproduction, they also buffer against reproductive competition from outside the group, thereby offsetting their reproductive costs. In Chapter 6, I investigate the factors that influence the maintenance of both sexes’ dominance tenures, while accounting for the distinct causes of tenure loss. I show that heavier dominants are more likely to maintain their position and that dominants of both sexes experience similar levels of within-group intrasexual competition, with increasing numbers of resident competitors increasing the risk of displacement. In addition, dominant males are uniquely vulnerable to extra-group takeovers and resident subordinate males appear to aid in the defence of the group, with higher numbers of subordinate males reducing takeover risk. Furthermore, males are also distinct from female dominants in that a substantial number abandon their dominance, a process that I find is associated with the availability of reproductive opportunities within the group. Finally in Chapter 7, I characterise the processes influencing group persistence, which is important for both the maintenance of a dominant’s tenure and ensuring the persistence of their lineage. I show that groups iii can persist for over a decade and that maintaining a large group size is essential for maximising group longevity. I also find that an endemic form of tuberculosis, Mycobacterium suricattae, plays a considerable role in the failure of groups, being associated with the failure of most long lived groups in the population.
... Here, we addressed these gaps and investigated whether the social correlates of male social rank mediate the interplay between glucocorticoid concentrations and male investment in social and sexual activities in the spotted hyena Crocuta crocuta. Spotted hyenas are long-lived social carnivores that live in large clans characterised by a stable linear hierarchy (East & Hofer, 2001), fission-fusion dynamics (Smith et al., 2008), male-biased dispersal (Höner et al., 2007) and promiscuous breeding with no distinct breeding season Engh et al., 2002). Male reproductive success strongly and positively correlates with male social rank (Davidian et al., 2016) but in contrast to many species, this is not the result of female mate preference for particular rank-related male attributes nor of rank-related fighting ability and competitive exclusion. ...
... Female spotted hyenas have control over copulation owing to the masculinisation of their outer genitalia (East et al., 1993;Szykman et al., 2007); they are not sexually coerced by males and exercise mate choice. Females prefer males who became members of the clan after they were born (Höner et al., 2007) and males who invest in fostering a relationship with them Szykman et al., 2001). Male spotted hyenas do not adopt alternative reproductive tactics but they do express various behaviours to foster relationships with and express their sexual interest in females (Szykman et al., 2007); these behaviours are here referred to as 'sexual activities' or 'courting' (see Section 2 for details). ...
... Their age (±7 days) was estimated based on pelage characteristics, body size, locomotory abilities and behavioural development (Pournelle, 1965). Dispersal is strongly male-biased; approximately 85% of males leave their natal clan and immigrate into another Crater clan to breed whereas virtually all females remain in their natal clan throughout their life (Davidian et al., 2016;Höner et al., 2007). Extra-clan paternity is extremely rare; male breeding prospects therefore depend on their clan membership and the number of young females in the clan (Davidian et al., 2016;Höner et al., 2007Höner et al., , 2010. ...
Article
Full-text available
1. In many animal societies, dominant males have a higher reproductive success than subordinate males. The proximate mechanisms by which social rank influences reproductive success are poorly understood. One prominent hypothesis posits that rank‐related male attributes of attractiveness and fighting ability are the main mediators of reproductive skew. Yet, empirical evidence in support of this hypothesis is limited. An alternative hypothesis emphasises the inherent social dimension of dominance relationships and posits that the relationship between male social rank and reproductive success is mediated by the physiological costs of male‐male competition. This has not been tested in systems in which the two hypotheses can be disentangled. 2. We investigated the interplay between male social rank, physiological costs and male investment in social and sexual activities. We used measurements of faecal glucocorticoid metabolite concentrations (fGMC) as biomarkers of physiological costs and long‐term behavioural data of 319 males in free‐ranging spotted hyenas (Crocuta crocuta), a species in which male access to females and reproductive success do not depend on physical attributes. 3. When males courted females and interacted with male competitors, low‐ranking males had higher fGMC than high‐ranking males. In contrast, fGMC did not vary with social rank when males were alone or when they courted females and competitors were absent. Low‐ranking males minimised their exposure to physiologically costly intrasexual competition; they spent more time alone and less time engaging in social and sexual activities than did high‐ranking males. They also invested less than high‐ranking males in courting the most contested and highest‐quality females. 4. Our findings demonstrate that the physiological costs of intrasexual competition in male spotted hyenas vary with social rank and shape behavioural trade‐offs between the allocation of time and physiological resources to social integration, reproduction, and self‐maintenance. Our study suggests that physiological and social constraints play a pivotal role in the emergence of rank‐related male reproductive success. The study provides insights into how the social organisation and breeding system shape physiological constraints and patterns of reproductive skew within and between species.
... Alternatively, female mate choice can promote intersexual power asymmetries indirectly. For example, in spotted hyenas, female reproductive control and mate preferences drive male dispersal [68], which decreases the number of social allies that males can recruit and thus reduces male social control [28]. Figure 2. Eco-evolutionary pathways to male and female empowerment in mammals. ...
Article
In animal societies, control over resources and reproduction is often biased towards one sex. Yet, the ecological and evolutionary underpinnings of male–female power asymmetries remain poorly understood. We outline a comprehensive framework to quantify and predict the dynamics of male–female power relationships within and across mammalian species. We show that male–female power relationships are more nuanced and flexible than previously acknowledged. We then propose that enhanced reproductive control over when and with whom to mate predicts social empowerment across ecological and evolutionary contexts. The framework explains distinct pathways to sex-biased power: coercion and male-biased dimorphism constitute a co-evolutionary highway to male power, whereas female power emerges through multiple physiological, morphological, behavioural, and socioecological pathways.
... Several hypotheses have been put forward to explain the evolution and adaptive significance of sex-biased dispersal (Beirinckx et al., 2006). For example, resource defence by males might favour female-biased dispersal (Nagy et al., 2007), whereas scramble male competition for females might favour male-biased dispersal (Höner et al., 2007;Spritzer et al., 2005). Inbreeding avoidance may favour dispersal in either sex (Pusey, 1987). ...
Article
Full-text available
1. Range expansions can be shaped by sex differences in behaviours and other phenotypic traits affecting dispersal and reproduction. 2. Here, we investigate sex differences in morphology, behaviour and genomic population differentiation along a climate‐mediated range expansion in the common bluetail damselfly (Ischnura elegans) in northern Europe. 3. We sampled 65 sites along a 583 km gradient spanning the I. elegans range in Sweden and quantified latitudinal gradients in site relative abundance, sex ratio and sex‐specific shifts in body size and mating status (a measure of sexual selection). Using single nucleotide polymorphism (SNP) data for 426 individuals from 25 sites, we further investigated sex‐specific landscape and climatic effects on neutral genetic connectivity and migration patterns. 4. We found evidence for sex differences associated with the I. elegans range expansion, namely (1) increased male body size with latitude, but no latitudinal effect on female body size, resulting in reduced sexual dimorphism towards the range limit, (2) a steeper decline in male genetic similarity with increasing geographic distance than in females, (3) male‐biased genetic migration propensity, and (4) a latitudinal cline in migration distance (increasing migratory distances towards the range margin), which was stronger in males. Cooler mean annual temperatures towards the range limit were associated with increased resistance to gene flow in both sexes. Sex ratios became increasingly male‐biased towards the range limit, and there was evidence for a changed sexual selection regime shifting from favouring larger males in the south, to favouring smaller males in the north. 5. Our findings suggest sex‐specific spatial phenotype sorting at the range limit, where larger males disperse more under higher landscape resistance associated with cooler climates. The combination of latitudinal gradients in sex‐biased dispersal, increasing male body size, and (reduced) sexual size dimorphism should have emergent consequences for sexual selection dynamics and the mating system at the expanding range front. Our study illustrates the importance of considering sex differences in the study of range expansions driven by ongoing climate change.
... Mammals display considerable variation in male mating strategies, with mating success sometimes differing from paternity success (Pemberton et al. 1992;Coltman et al. 1999;Boyko and Marshall 2009). Moreover, while there is evidence for female mate choice, the criteria driving this choice remain largely ambiguous (Höner et al. 2007;Clutton-Brock and McAuliffe 2009). Therefore, the EC system offers a potential tool for exploring male fertility by relating this to observed patterns of mating strategies displayed in both sexes. ...
Article
Quantifying physiological challenges has gained increasing importance in evolutionary biology, behavioral physiology, and conservation. One matrix that is particularly useful for obtaining long-term records of physiological changes in mammals is hair. Potential markers are components of the endocannabinoid (EC) system, which regulates homeostasis of the brain as well as the endocrine and immune systems. Here, we present results from the first study to measure ECs (anandamide [AEA], 2-archidonyl glycerol [2-AG]) and EC-like compounds (N-palmitoylethanolamine [PEA], N-oleoylethanolamine [OEA], N-stearoylethanolamine [SEA]) in the hair of a nonhuman primate. We found that AEA, SEA, PEA, and OEA can be reliably measured in hair samples. When comparing the measurements of hair from different body parts, we found that variations of some analytes suggest that hair location is likely to affect results. For changes in health status, measurements of ECs and EC-like compounds reflected differences at both intra- and interindividual levels. We concluded that the EC system potentially provides novel tools to assess well-being, health status, and metabolic stress-not only in the hair of humans but also in that of domestic and wild animals. Measuring changes in ECs and EC-like compounds may improve the long-term monitoring of health status in captive and wild primates and may serve as a useful measure in animal welfare programs.
Chapter
The members of a species are distributed in a characteristic manner in space and time; they mate with different numbers of members of the opposite sex, differ in parental care behaviour, and their social interactions are not randomly distributed among conspecifics. Analyses of social systems deal with the causes, patterns, mechanisms and consequences of this diversity. In this chapter, I examine how societies of different species are organised, which factors determine the characteristics of different forms of organisation, which reproductive strategies are advantageous under which conditions, and which forms of parental care are necessary or possible.
Article
Long-term, individual-based field studies, the application of genetic techniques, and phylogenetic reconstructions have led to substantial advances in our understanding of the diversity and evolution of mammalian breeding systems and their consequences. These studies show how differences in ecology, life histories, and phylogeny affect the distributions of breeding females and breeding males; how the distributions of both sexes affect the evolution of breeding systems and the composition and kinship structure of social groups; how differences in breeding systems and the social environment that individuals encounter affect the selection pressures operating on both sexes and the evolution of their behavior, physiology, and morphology; and how these differences affect the demography and dynamics of populations and their responses to variation in density, climate, and human impact. © 2021 American Association for the Advancement of Science. All rights reserved.
Chapter
Die Mitglieder einer Art sind in charakteristischer Art und Weise in Raum und Zeit verteilt; sie verpaaren sich mit unterschiedlich vielen Mitgliedern des anderen Geschlechts, unterscheiden sich in ihrem elterlichen Fürsorgeverhalten und soziale Interaktionen sind nicht zufällig über Artgenossen verteilt. Analysen von Sozialsystemen beschäftigen sich mit den Ursachen, Mustern, Mechanismen und Konsequenzen dieser Diversität. Die Spannbreite der Sozialsysteme reicht von einzelgängerischen Individuen, die nur einmal im Leben mit einem Artgenossen zur Fortpflanzung zusammenkommen, bis hin zu Gruppen aus Tausenden Individuen, von denen manche Jahrzehnte lang zusammenleben. Wie die Gesellschaften verschiedener Arten organisiert sind, welche Faktoren die Ausprägung verschiedener Organisationsformen bestimmen, welche Fortpflanzungsstrategien unter welchen Bedingungen vorteilhaft sind und welche Formen der Jungenfürsorge nötig oder möglich sind, beschäftigt uns in diesem Kapitel.
Article
Full-text available
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.
Article
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.
Chapter
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.