Patterns of relatedness and parentage in an asocial, polyandrous striped hyena population

We investigated patterns of relatedness and reproduction in a population of striped hyenas in which individuals are behaviourally solitary but form polyandrous spatial groups consisting of one adult female and multiple adult males. Group-mate males were often close relatives, but were unrelated or distantly related in some cases, indicating that male coalitions are not strictly a result of philopatry or dispersal with cohorts of relatives. Most male-female pairs within spatial groups were unrelated or only distantly related. Considering patterns of relatedness between groups, relatedness was significantly higher among adult males living in non-neighbouring ranges than among neighbouring males. Mean relatedness among male-female dyads was highest for group-mates, but relatedness among non-neighbouring males and females was also significantly higher than among dyads of opposite-sex neighbours. Female-female relatedness also increased significantly with increasing geographic separation. These unusual and unexpected patterns may reflect selection to settle in a nonadjacent manner to reduce inbreeding and/or competition among relatives for resources (both sexes), or mates (males). Finally, resident males fathered the majority of the resident female's cubs, but extra-group paternity was likely in 31% of the cases examined, and multiple paternity was likely in half of the sampled litters.     

Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups

By living in social groups with potential competitors, animals forgo monopolizing access to resources. Consequently, debate continues over how selection might favour sociality among competitors. For example, several models exist to account for the evolution of shared reproduction in groups. The 'concession model' hypothesizes that dominant reproducers benefit from the presence of subordinates, and hence tolerate some reproduction by subordinates. This mutual benefit to both dominants and subordinates may provide a foundation for the formation of social groups in which multiple members reproduce-a necessary step in the evolution of cooperation. To date, however, the concession model has received virtually no support in vertebrates. Instead, the vast majority of vertebrate data support 'limited control models', which posit that dominant reproducers are simply unable to prevent subordinates from reproducing. Here we present the most comprehensive evidence to date in support of the concession model in a vertebrate. We examined natural variation in the number of adult males in gelada (Theropithecus gelada) reproductive units to assess the extent of reproductive skew in multi-male units. Dominant ('leader') males in units that also had subordinate ('follower') males had a 30 per cent longer tenure than leaders in units that did not have followers, mainly because followers actively defended the group against potential immigrants. Follower males also obtained a small amount of reproduction in the unit, which may have functioned as a concession in return for defending the unit. These results suggest that dominants and subordinates may engage in mutually beneficial reproductive transactions, thus favouring male-male tolerance and cooperation.     

Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative mammal

In cooperatively breeding species, subordinates typically suffer strong constraints on within-group reproduction. While numerous studies have highlighted the additional fitness benefits that subordinates might accrue through helping, few have considered the possibility that subordinates may also seek extra-group matings to improve their chances of actually breeding. Here, we show that subordinate males in cooperative meerkat, Suricata suricatta, societies conduct frequent extraterritorial forays, during periods of peak female fertility, which give rise to matings with females in other groups. Genetic analyses reveal that extra-group paternity (EGP) accrued while prospecting contributes substantially to the reproductive success of subordinates: yielding the majority of their offspring (approx. 70%); significantly reducing their age at first reproduction and allowing them to breed without dispersing. We estimate that prospecting subordinates sire 20-25% of all young in the population. While recent studies on cooperative birds indicate that dominant males accrue the majority of EGP, our findings reveal that EGP can also arise from alternative reproductive tactics employed exclusively by subordinates. It is important, therefore, that future attempts to estimate the fitness of subordinate males in animal societies quantify the distribution of extra-group as well as within-group paternity, because a substantial proportion of the reproductive success of subordinates may otherwise go undetected.     

Estimating the proportion of offspring attributable to candidate adults

Statistical methods for estimating genetic parentage are increasingly applied to accommodate limited marker polymorphism and the incomplete sampling of individuals. Neff et al. (2000a, Mol. Ecol. 9, 515–528; 2000b, Mol. Ecol. 9, 529–539) published a method (Pat) that estimates the proportion of next-generation individuals sired by a focal male, taking into account that the male may be genetically compatible, by random chance, with offspring that are not his own. Here we employ this method to reestimate paternity of 68 nest-guarding males from several fish species. The difference between the conventional exclusion-based estimate and Pat was >0.05 in only four of the 68 (5.9%) fish nests analyzed. An analytical formula shows that the difference between the two estimates is expected to be negligible if the focal male is consistent with a large proportion of the genotyped offspring, or if marker polymorphism is high. In addition, computer simulations illustrate how numbers of marker loci and their levels of genetic polymorphism, as well as the mating system of the organism under study, can influence estimates of paternity derived from exclusion-based estimates and Pat. Finally, we discuss various applications of these estimators including cases where additional biological information is present in the form of behavioral observations on parental care.     

Multiple paternity in an aggregate breeding amphibian: the effect of reproductive skew on estimates of male reproductive success

Aggregate, or explosive, breeding is widespread among vertebrates and likely increases the probability of multiple paternity. We assessed paternity in seven field-collected clutches of the explosively breeding spotted salamander (Ambystoma maculatum) using 10 microsatellite loci to determine the frequency of multiple paternity and the number of males contributing to a female's clutch. Using the Minimum Method of allele counts, multiple paternity was evident in 70% of these egg masses. Simple allele counts underestimate the number of contributing males because this method cannot distinguish multiple fathers with common or similar alleles. Therefore, we used computer simulations to estimate from the offspring genotypes the most likely number of contributing fathers given the distributions of allele frequencies in this population. We determined that two to eight males may contribute to A. maculatum clutches; therefore, multiple paternity is a common strategy in this aggregate breeding species. In aggregate mating systems competition for mates can be intense, thus differential reproductive success (reproductive skew) among males contributing to a female's clutch could be a probable outcome. We use our data to evaluate the potential effect of reproductive skew on estimates of the number of contributing males. We simulated varying scenarios of differential male reproductive success, ranging from equal contribution to high reproductive skew among contributing sires in multiply sired clutches. Our data suggest that even intermediate levels of reproductive skew decrease confidence substantially in estimates of the number of contributing sires when parental genotypes are unknown.     

Queen mating and paternity variation in the ant Lasius niger

We have electrophoretically analysed the variation in queen mating and worker paternity across and within seven populations of the ant Lasius niger in northwestern Europe. Populations were panmictic and not genetically differentiated ( F _ST = 0.003 ± 0.004; range c. 1000 km). Queens ( n = 535) were shown to mostly mate with a single male, but double mating occurred in all populations and triple mating was found in one case (the total number of worker offspring analysed for paternity was 4825). The genetically effective queen mating frequency was 1.16 on average across populations (range 1.04–1.42). Double sampling of six out of the seven populations showed that most of the variation in queen mating occurred among populations and not within populations among years. Also, paternity skew in colonies with double-mated queens was relatively constant per site but varied across populations. Paternity skew was high in populations with low frequencies of double queen-mating, low in populations with intermediate frequencies of double queen mating and ambiguous in a single population where more than half of the queens mated multiply. Double-mated queens were only collected halfway through a nuptial flight, suggesting that double mating is time consuming and that the mating swarm sex ratio may affect the likelihood of multiple mating towards the end of a flight. No difference in fresh weight between single- and double-mated queens from the same population was found.     

Familiarity breeds progeny: sociality increases reproductive success in adult male ring-tailed coatis (Nasua nasua)

The ring-tailed coati (Nasua nasua) is the only coati species in which social groups contain an adult male year round, although most males live solitarily. We compared reproductive success of group living and solitary adult male coatis to determine the degree to which sociality affects reproductive success. Coati mating is highly seasonal and groups of female coatis come into oestrus during the same 1-2 week period. During the mating season, solitary adult males followed groups and fought with the group living male. This aggression was presumably to gain access to receptive females. We expected that high reproductive synchrony would make it difficult or impossible for the one group living male to monopolize and defend the group of oestrous females. However, we found that group living males sired between 67-91% of the offspring in their groups. This reproductive monopolization is much higher than other species of mammals with comparably short mating seasons. Clearly, living in a group greatly enhanced a male's reproductive success. At the same time, at least 50% of coati litters contained offspring sired by extra-group males (usually only one offspring per litter); thus, resident males could not prevent extra-group matings. The resident male's reproductive advantage may reflect female preference for a resident male strong enough to fend off competing males.     

Age- and tactic-related paternity success in male African elephants

Information on age- and tactic-related paternity success isessential for understanding the lifetime reproductive strategyof males and constitutes an important component of the fitnesstrade-offs that shape the life-history traits of a species.The degree of reproductive skew impacts the genetic structureof a population and should be considered when developing conservationstrategies for threatened species. The behavior and geneticstructure of species with large reproductive skew may be disproportionatelyimpacted by anthropogenic actions affecting reproductively dominantindividuals. Our results on age- and tactic-specific paternitysuccess in male African elephants are the first from a free-rangingpopulation and demonstrate that paternity success increasesdramatically with age, with the small number of older bullsin the competitive state of musth being the most successfulsires. However, nonmusth males sired 20% of genotyped calves,and 60% of mature bulls (>20 years old) were estimated tohave sired offspring during the 5-year study period. The 3 mostsuccessful males sired less than 20% of the genotyped offspring.Hence, contrary to prediction from behavior and life-historytraits, reproduction was not heavily skewed compared with manyother mammalian systems with a similar breeding system. Nevertheless,these results indicate that trophy hunting and ivory poaching,both of which target older bulls, may have substantial behavioraland genetic effects on elephant populations. In addition, theseresults are critical to the current debate on methods for managingand controlling increasing populations of this species.     

Helping opportunities and space segregation in cooperatively breeding cichlids

Studies of cooperative breeding have largely ignored the roleof conflict among helpers and how it shapes group dynamics andhelping behavior. In the present study, performing laboratoryexperiments with cooperatively breeding cichlids from Lake Tanganyika,we show that secondary group members (potential helpers) occupyhome ranges within the group territory and may be aggressiveto one another. Experimental removal of secondary group membersallowed the individual next in rank to move closer to the removedindividual's home range. In the field, dominant secondary groupmembers stayed closer to the brood chamber than did subordinategroup members of similar size, and proximity to the brood chamberwas related to the length of time spent inside. We suggest thatspace segregation and competition among secondary group membersis common in these cichlids, and may limit the opportunitiesto provide help.     

Insights into the mating habits of the tiger salamander (Ambystoma tigrinum tigrinum) as revealed by genetic parentage analyses

Among urodeles, ambystomatid salamanders are particularly amenable to genetic parentage analyses because they are explosive aggregate breeders that typically have large progeny arrays. Such analyses can lead to direct inferences about otherwise cryptic aspects of salamander natural history, including the rate of multiple mating, individual reproductive success, and the spatial distribution of clutches. In 2002, we collected eastern tiger salamander (Ambystoma tigrinum tigrinum) egg masses (> 1000 embryos) from a approximately 80 m linear transect in Indiana, USA. Embryos were genotyped at four variable microsatellite loci and the resulting progeny array data were used to reconstruct multilocus genotypes of the parental dams and sires for each egg mass. UPGMA analysis of genetic distances among embryos resolved four instances of egg mass admixture, where two or more females had oviposited at exactly the same site resulting in the mixing of independent cohorts. In total, 41 discrete egg masses were available for parentage analyses. Twenty-three egg masses (56%) consisted exclusively of full-siblings (i.e. were singly sired) and 18 (44%) were multiply sired (mean 2.6 males/clutch). Parentage could be genetically assigned to one of 17 distinct parent pairs involving at least 15 females and 14 different males. Reproductive skew was evident among males who sired multiply sired clutches. Additional evidence of the effects of sexual selection on male reproductive success was apparent via significant positive correlations between male mating and reproductive success. Females frequently partitioned their clutches into multiple discrete egg masses that were separated from one another by as many as 43 m. Collectively, these data provide the first direct evidence for polygynandry in a wild population of tiger salamanders.     

Constraints on control: factors influencing reproductive success in male mandrills (Mandrillus sphinx)

Over the last decade, paternity analysis using molecular markershas revealed that observed mating systems do not necessarilycorrelate with reproductive systems and thus cannot providereliable information about male reproductive success (RS). Thisis especially true for primate species with a complex multimale-multifemalesocial organization, such as mandrills (Mandrillus sphinx).Using molecular markers for the measurement of individual RSand a comprehensive data set comprising 193 offspring from 27birth cohorts over a 20-year period of sampling, we investigatedthe social, genetic, and demographic factors that may influencethe probability of paternity by dominant male mandrills, livingin a semi–free-ranging colony. We observed a significantskew in RS towards dominant males, with their probability ofpaternity increasing as the number of adult males in the groupincreased, and when they were closely related to subordinateadolescent males. Conversely, the probability of dominant malessiring infants decreased when the number of simultaneously tumescentfemales increased. Fewer offspring were sired by dominant maleswhen female partners were closely related to them and when therelatedness between dominant and subordinate adult males increased.These two last points suggests particularly that mechanismsof kin recognition are operating to avoid the costs of inbreedingand may also reflect the lower costs to dominant males of losingconception opportunities to more closely related subordinateadult males. This study is, to our knowledge, one of the firstin primates to use an integrative approach and multivariateanalysis to show that multiple factors are involved in determiningthe probability of paternity by dominant males.     

Long-term paternity skew and the opportunity for selection in a mammal with reversed sexual size dimorphism

Most mammalian groups are characterized by male-biased sexual size dimorphism, in which size-dependent male-male competition and reproductive skew are tightly linked. By comparison, little is known about the opportunity for sexual selection in mammalian systems without male-biased dimorphism, where the traits under sexual selection might be less obvious. We examined 10 years of parentage data in a colony of greater horseshoe bats (Rhinolophus ferrumequinum) to determine the magnitude of male reproductive skew and the opportunity for sexual selection in a mammal in which females are the larger sex. Annual paternity success was weakly skewed but consistent patterns led to strong longitudinal paternity skew among breeders. Just three males accounted for a third of all paternity assignments, representing at least a fifth of all colony offspring born in a decade. Paternity success was in part determined by age but was not influenced by dispersal status. Our results show that paternity skew and the opportunity for sexual selection in a species with reversed sexual size dimorphism can approach levels reported for classical examples of species with polygyny and male-biased dimorphism, even where the traits under sexual selection are not known.     

Inter-population variation in multiple paternity and reproductive skew in the guppy

We use microsatellite loci to detail the multiple paternity patterns in broods from 10 wild populations of the guppy ( Poecilia reticulata ) found in Northern Trinidad. The populations span two major drainages comprising the Caroni and the Oropouche, and include sites that are characterized by either high or low predation. Across the populations the frequency of multiple paternity is high with 95% (range: 70%–100%) of broods having multiple sires. Broods have an average of 3.5 sires (range: 1–9) and a mixed-model analysis suggests that broods from high predation sites have marginally more sires than do those from low predation sites, but this is true only in the Oropouche drainage. There is no difference in sire number between predation sites in the Caroni drainage. Brood size, but not female body length, is correlated with the number of sires and the correlation cannot be attributed solely to the stochastic process associated with sperm competition and a 'fair raffle'. Within broods there is significant skew in reproductive success among males, which may reflect variation in sperm competitiveness or female choice. There is, however, no difference in the skew among populations from different predation regimes or drainages. Finally, high predation populations were characterized by increased genetic variability at the microsatellite loci, suggesting a larger effective population size. We discuss explanations for the high degree of multiple paternity but the general lack of any major differences among broods from ecologically different populations.     

Polyandry and paternity skew in natural and experimental populations of Drosophila serrata

Many species engage in polyandry, resulting in the potential for sexual selection to continue post-copulation through sperm competition and/or cryptic female choice. The relative importance of pre- vs. post-copulatory processes remains unknown for most species despite this information being fundamental for understanding the evolutionary consequences of sexual selection. The Australian fruit fly Drosophila serrata has become a prominent model system for studying precopulatory sexual selection, such as mating preferences and their influence on the evolution of sexually selected traits. Here, we investigated polyandry and the potential for post-copulatory sexual selection in this species using indirect paternity analysis. We genotyped 21 wild-caught and 19 laboratory-reared mothers and their offspring (a total of 787 flies) at six microsatellite loci and found extensive polyandry, with all broods surveyed having at least two sires. Female remating rates were higher than in other Drosophila surveyed to date and no significant differences were found between laboratory and field populations. Additionally, we found evidence for biased sperm usage in several broods of D. serrata . Paternity skew occurred more frequently in broods from the field population than the laboratory one, suggesting differences between the two environments in the level of post-copulatory sexual selection. Our data suggest that D. serrata represents a promising system for studying the interaction between pre- and post-copulatory sexual selection in driving the evolution of sexually selected phenotypes.