Social structure influences extra-pair
paternity in socially monogamous mammals
The genetic similarity between pair members influences the frequency of extrapair paternity in alpine marmots
Extrapair paternity is widespread in birds and mammals. In particular, the alpine marmot, Marmota marmota, has a high frequency of extrapair paternity that seems to be explained by the genetic compatibility hypothesis. We investigated whether the number and proportion of extrapair young depend on the heterozygosity (individual genetic diversity) of the social male, or on the genetic similarity between the social male and his mate (relatedness). Both the number and the proportion of extrapair young increased with both high similarity and dissimilarity between the social pair. In combination with previous results, our study suggests that patterns of extrapair paternity in alpine marmots can best be explained by the genetic compatibility hypothesis, and more precisely its optimal outbreeding variant. Our results indeed suggest that extrapair paternity is a mechanism to avoid both in- and outbreeding depression. We discuss which proximal mechanisms may be involved in extrapair paternity in this species. Pour en savoir plus
Are extra-pair young better than within-pair young?
A comparison of survival and dominance in alpine marmot
In socially monogamous species, females may seek extra-pair copulation to gain genetic benefits. In order to test this ‘genetic quality’ hypothesis, one must compare the performance of extra-pair young (EPY) and within-pair young (WPY). Such tests, however, are scarce and results published so far are inconclusive. Here, we test the ‘genetic quality’ hypothesis using multistate capture–recapture models to compare age-specific survival and access to dominance between EPY and WPY in the alpine marmot Marmota marmota, a socially monogamous mammal showing extra-pair paternities. When compared with WPY, survival of EPY was higher by 15%, 10% and 30%, for juveniles, yearlings and 2-year-old individuals, respectively. Survival at older ages did not differ. Survival corresponded to true survival for yearlings and juveniles as dispersal does not occur before 2 years of age in marmots. For older individuals, survival estimates included a mixture of survival and dispersal. The 30% increase of the 2-year-old EPY survival might reflect delayed dispersal rather than high survival of EPY as compared with WPY. WPY and EPY had the same probability (0·28) to access dominance at 2 years of age, but EPY were more successful at older ages than WPY (0·46 vs. 0·10). Both survival and reproductive performance were higher in EPY than in WPY. The fitness advantages of adopting such a mixed mating tactic are thus likely to be high for marmot females. We suggest that obtaining genetic benefits is the main evolutionary force driving extra-pair paternity in alpine marmots. Pour en savoir plus
Extra-pair paternity in alpine marmot (Marmota marmota): Genetic quality and genetic diversity effects
Using
the genetic estimates of
paternity available
for 22 species of socially
monogamous mammals,
we investigated the impact of
the social
structure and of the type of pair bonding on
the interspecific variations of extra-pair
paternity
rates. To this purpose,
we classified species
in three categories of social structure— solitary,
pair or family-living
species—and in two
categories of pair bonding—intermittent or continuous.
We show that interspecific variations
of extra-pair paternity rates
are better explained
by the social structure
than by the type
of pair bonding. Species with intermittent and
continuous pair bonding present
similar rates
of extra-pair paternity, while solitary and family-living
species present higher extra-pair paternity
rates than pair-living species. This can be
explained by both higher male–male competition
and higher female mate
choice opportunities
in solitary and family-living species than in
pair-living species. Pour en savoir
plus
The genetic similarity between pair members influences the frequency of extrapair paternity in alpine marmots
Extrapair paternity is widespread in birds and mammals. In particular, the alpine marmot, Marmota marmota, has a high frequency of extrapair paternity that seems to be explained by the genetic compatibility hypothesis. We investigated whether the number and proportion of extrapair young depend on the heterozygosity (individual genetic diversity) of the social male, or on the genetic similarity between the social male and his mate (relatedness). Both the number and the proportion of extrapair young increased with both high similarity and dissimilarity between the social pair. In combination with previous results, our study suggests that patterns of extrapair paternity in alpine marmots can best be explained by the genetic compatibility hypothesis, and more precisely its optimal outbreeding variant. Our results indeed suggest that extrapair paternity is a mechanism to avoid both in- and outbreeding depression. We discuss which proximal mechanisms may be involved in extrapair paternity in this species. Pour en savoir plus
Are extra-pair young better than within-pair young?
A comparison of survival and dominance in alpine marmot
In socially monogamous species, females may seek extra-pair copulation to gain genetic benefits. In order to test this ‘genetic quality’ hypothesis, one must compare the performance of extra-pair young (EPY) and within-pair young (WPY). Such tests, however, are scarce and results published so far are inconclusive. Here, we test the ‘genetic quality’ hypothesis using multistate capture–recapture models to compare age-specific survival and access to dominance between EPY and WPY in the alpine marmot Marmota marmota, a socially monogamous mammal showing extra-pair paternities. When compared with WPY, survival of EPY was higher by 15%, 10% and 30%, for juveniles, yearlings and 2-year-old individuals, respectively. Survival at older ages did not differ. Survival corresponded to true survival for yearlings and juveniles as dispersal does not occur before 2 years of age in marmots. For older individuals, survival estimates included a mixture of survival and dispersal. The 30% increase of the 2-year-old EPY survival might reflect delayed dispersal rather than high survival of EPY as compared with WPY. WPY and EPY had the same probability (0·28) to access dominance at 2 years of age, but EPY were more successful at older ages than WPY (0·46 vs. 0·10). Both survival and reproductive performance were higher in EPY than in WPY. The fitness advantages of adopting such a mixed mating tactic are thus likely to be high for marmot females. We suggest that obtaining genetic benefits is the main evolutionary force driving extra-pair paternity in alpine marmots. Pour en savoir plus
Extra-pair paternity in alpine marmot (Marmota marmota): Genetic quality and genetic diversity effects
Assuming that a male’s genetic characteristics affect those of his offspring, extra-pair copulation has been hypothesized to increase heterozygosity of the progeny - the “genetic compatibility” hypothesis - and the genetic diversity within litters - the “genetic diversity” hypothesis. We tested these two hypotheses in the alpine marmot (Marmota marmota), a socially monogamous mammal showing a high rate of extra-pair paternity (EPP). In a first step, we tested the assumption that a male’s genetic characteristics (heterozygosity and genetic similarity to the female) affect those of his offspring. Genetic similarity between parents influenced offspring heterozygosity, offspring genetic similarity to their mother, and litter genetic diversity. The father’s heterozygosity also influenced litter genetic diversity but did not affect offspring heterozygosity. Hence, heterozygosity seems not to be heritable in the alpine marmot. In a second step, we compared genetic characteristics of extra-pair young (EPY) and within-pair young (WPY). EPY were less genetically similar to their mother but not more heterozygous than WPY. EPY siblings were also less genetically similar than their WPY half siblings. Finally, the presence of EPY promoted genetic diversity within the litter. Thus, our data support both the “genetic compatibility” and the “genetic diversity” hypotheses. We discuss further investigations needed to determine the primary causes of EPP in this species. Pour en savoir plus
Extra-pair
paternity
in
the monogamous alpine marmot (Marmota
marmota):
The roles of social
setting and female mate choice.
Extra-pair paternity
(EPP) can be
influenced by both social setting and female mate choice. If evidence
suggests that females try to obtain extra-pair copulations (EPCs) in
order to gain genetic benefits when mated to a homozygous and/or to a
related male, females may not be able to choose freely among extra-pair
mates (EPMs) as the social mate may constrain female access to EPMs. In
this study, we investigated, first, how EPP depended on social setting
and specifically on the number of subordinate males in the family group
in a highly social and monogamous mammal, the alpine marmot. Second, we
investigated how EPP depended on female mate choice for genetic
benefits measured as male mate-heterozygosity and within-pair
relatedness. Our results reveal, first, that EPP depended on the social
setting, increasing with the number of subordinate males. Second, EPPs
were related to relatedness between mates. Third, EPMs were found to be
more heterozygous than within-pair males. Thus, social setting may
constrain female choice by limiting opportunities for EPC. However,
after accounting for social confounding factors, female choice for
genetic benefits may be a mechanism
driving EPP in monogamous species. Pour en savoir plus
Age-specific effect of heterozygosity on survival in alpine
marmots, Marmota marmota
The fitness consequences of heterozygosity and the mechanisms underpinning them are still highly controversial. Using capture–mark–recapture models, we investigated the effects of individual heterozygosity, measured at 16 microsatellite markers, on age-dependent survival and access to dominance in a socially monogamous mammalian species, the alpine marmot. We found a positive correlation between standardized multilocus heterozygosity and juvenile survival. However, there was no correlation between standardized multilocus heterozygosity and either survival of older individuals or access to dominance. The disappearance of a significant heterozygosity fitness correlation when individuals older than juveniles are considered is consistent with the prediction that differences in survival among individuals are maximal early in life. The lack of a correlation between heterozygosity and access to dominance may be a consequence of few homozygous individuals attaining the age at which they might reach dominance. Two hypotheses have been proposed to explain heterozygosity-fitness correlations: genome-wide effects reflected by all markers or local effects of specific markers linked to genes that determine fitness. In accordance with genome-wide effects of heterozygosity, we found significant correlations between heterozygosities calculated across single locus or across two sets of eight loci. Thus, the genome-wide heterozygosity effect seems to explain the observed heterozygosity-fitness correlation in the alpine marmot. Pour en savoir plus
driving EPP in monogamous species. Pour en savoir plus
Age-specific effect of heterozygosity on survival in alpine
marmots, Marmota marmota
The fitness consequences of heterozygosity and the mechanisms underpinning them are still highly controversial. Using capture–mark–recapture models, we investigated the effects of individual heterozygosity, measured at 16 microsatellite markers, on age-dependent survival and access to dominance in a socially monogamous mammalian species, the alpine marmot. We found a positive correlation between standardized multilocus heterozygosity and juvenile survival. However, there was no correlation between standardized multilocus heterozygosity and either survival of older individuals or access to dominance. The disappearance of a significant heterozygosity fitness correlation when individuals older than juveniles are considered is consistent with the prediction that differences in survival among individuals are maximal early in life. The lack of a correlation between heterozygosity and access to dominance may be a consequence of few homozygous individuals attaining the age at which they might reach dominance. Two hypotheses have been proposed to explain heterozygosity-fitness correlations: genome-wide effects reflected by all markers or local effects of specific markers linked to genes that determine fitness. In accordance with genome-wide effects of heterozygosity, we found significant correlations between heterozygosities calculated across single locus or across two sets of eight loci. Thus, the genome-wide heterozygosity effect seems to explain the observed heterozygosity-fitness correlation in the alpine marmot. Pour en savoir plus
Heterozygosity-Fitness-Correlation revealed by microsatellite analyses in European alpine marmots (Marmota marmota).
The relationship between individual
genetic diversity and
fitness-related traits are poorly understood in the wild. The
availability of highly polymorphic molecular markers, such as
microsatellites, has made research on this subject more feasible. We
used three microsatellite-based measures of genetic diversity,
individual heterozygosity H, mean d2 and mean d2 outbreeding
to test for a relationship between individual genetic diversity and
important fitness trait, juvenile survival, in a population of alpine
marmots (Marmota marmota), after controlling for the effects of
ecological, social and physiological parameters that potentially
influence juvenile survival in marmots. Analyses were conducted on 158
juveniles, and revealed a positive
association between juvenile survival and genetic diversity measured by mean H. No association was found with mean d2 and with mean d2 outbreeding. This suggests a fitness disadvantage to less heterozygous juveniles. The genetic diversity-fitness correlation (GDFC) was somewhat stronger during years with poor environmental conditions (i.e. wet summers). The stressful environmental conditions of this high mountain population might enhance inbreeding depression and make this association between genetic diversity and fitness detectable. Moreover the mating system, allowing extra pair copulation by occasional immigrants, as well as close inbreeding, favours a wide range of individual genetic diversity (mean H ranges from 0.125 to 1), which also may have facilitated the detection of the GDFC. The results further suggest that the observed GDFC is likely to be explained by the ‘‘local effect’’ hypothesis rather than by the ‘‘general effect’’ hypothesis. Pour en savoir plus
association between juvenile survival and genetic diversity measured by mean H. No association was found with mean d2 and with mean d2 outbreeding. This suggests a fitness disadvantage to less heterozygous juveniles. The genetic diversity-fitness correlation (GDFC) was somewhat stronger during years with poor environmental conditions (i.e. wet summers). The stressful environmental conditions of this high mountain population might enhance inbreeding depression and make this association between genetic diversity and fitness detectable. Moreover the mating system, allowing extra pair copulation by occasional immigrants, as well as close inbreeding, favours a wide range of individual genetic diversity (mean H ranges from 0.125 to 1), which also may have facilitated the detection of the GDFC. The results further suggest that the observed GDFC is likely to be explained by the ‘‘local effect’’ hypothesis rather than by the ‘‘general effect’’ hypothesis. Pour en savoir plus
©
Aurélie Cohas
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