Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta)

When agonistic interventions are nepotistic, individuals are expected to side more often with kin but less often against kin in comparison with non-kin. As yet, however, few mammal studies have been in a position to test the validity of this assertion with respect to paternal relatedness. We therefore used molecular genetic kinship testing to assess whether adult female rhesus macaques (Macaca mulatta) from the free-ranging colony of Cayo Santiago (Puerto Rico) bias their interventions in ongoing dyadic aggressive interactions towards maternal and paternal half-sisters compared with unrelated females. It turned out that females supported maternal half-sisters significantly more often than paternal half-sisters or non-kin regardless of the costs associated with such interventions. Similarly, females targeted maternal half-sisters significantly less often than non-kin when this was associated with high costs. Unrelated females provided significantly higher mean rates of both high- and low-cost support to each other than did paternal half-sisters. However, females targeted paternal half-sisters significantly less often than non-kin when targeting was at low cost, suggesting that females refrain from intervening against paternal half-sisters. Our data confirm the general view that coalition formation in female mammals is a function of both the level of maternal relatedness and of the costs of intervention. The patterns of coalition formation among paternal kin were found to be more complex, and may also differ across species, but clear evidence for paternal kin discrimination was observed in female rhesus as predicted by kin selection theory.     

The association of female kin in the arctic ground squirrel Spermophilus parryii

Summary The association of kin in arctic ground squirrels (Spermophilus parryii) was studied near Haines Junction, Yukon Territory, during the summers of 1977, 1978, and 1979. Males dispersed in this population, thus only females were likely to live near relatives.Close female kin (sisters, mothers/daughters) had greater overlap of home ranges and interacted more amicably and less agonistically than did less closely related females. Closely related females clumped their young at emergence, whereas more distantly related females did not; there was little indication of clumping of pre-emerged young. The overlap of home ranges of distant relatives (known genetic relatives that had not associated in a natal burrow) was intermediate to that of close relatives and non-relatives. The types of interactions between distant relatives were more similar to those between non-relatives than between close relatives.I conclude that female arctic ground squirrels exhibit nepotism. Females may benefit from associations with relatives by sharing watching for predators once juveniles become conspicuous. Male arctic ground squirrels commit infanticide and several females may be more effective at protecting their young from infanticidal males than females living alone. I suggest that clumping of young by close relatives may provide a mechanism allowing distantly related females to identify each other.Address for offprint requests     

Genetic relatedness and space use in a behaviorally flexible species of marmot, the woodchuck (Marmota monax)

Solitary species show several patterns of space use and relatedness. Individuals may associate randomly or may live near female or male kin, often as a result of natal philopatry or dispersal patterns. Although usually described as solitary or asocial, woodchucks (Marmota monax) are behaviorally flexible marmots that exhibit greater sociality in some populations than others. I examined relationships between kinship, geographic distance, and home range overlap, as well as dispersal and philopatry, to determine the extent to which kin associated spatially. I used a combination of microsatellite DNA analysis, long-term behavioral observations, and radiotelemetry to test predictions that females, but not males, would associate with kin. Indeed, woodchucks lived closer and shared a greater proportion of their home range with more closely related animals. Overlap of females' and males' home ranges was positively correlated with kinship, and male–female dyads shared more area with closer kin. Most juveniles delayed dispersal beyond their first summer. Females often remained philopatric and settled near their natal range. Although males often dispersed as yearlings, some males also established territories within or immediately adjacent to their natal home ranges. A combination of factors can explain these spatial patterns, including high population density associated with the study site's location within a suburban environment, high dispersal costs, and abundant food. Thus, despite their asocial and solitary reputation, woodchucks displayed spatial patterns seen in other, more social species of ground-dwelling sciurids.     

Kinship,reproductive strategies and social dynamics of yellow-bellied marmots

Summary Social behavior of yellow-bellied marmots was observed for three years in colonies where kinship was known and for one year in a high elevation colony where harems were contiguous. Social dynamics of yellow-bellied marmots is dependent on kinship, group composition, and age-sex classes. This pattern is a consequence of the reproductive strategies of males and females. Females behave cohesively toward sisters or daughters, but not with sons and agonistically toward other females. Males generally behave amicably toward females and agonistically toward males, including their sons. Thus, reproductive strategies limit nepotism. This behavior is consistent with a population process in which sons typically disperse as yearlings. At least some of the variation in the expected patterns of social behaviors is attributable to individual differences. Because male and female reproductive strategies differ, a marmot population consists of two social subsystems. The female unit is the closely-related kin group which may also be a burrow group. The male unit is a harem which usually consists of two or more competing female kin groups.     

A field test of the effects of familiarity and relatedness on social associations and reproduction in prairie voles

Inbreeding depression is a well-documented phenomenon. In animals, one means of avoiding the costs of inbreeding is through the recognition and avoidance of kin as mates. Prairie voles (Microtus ochrogaster) are short-lived, socially monogamous rodents that demonstrate inbreeding depression in the laboratory. Field data indicate that pair formation in nature is opportunistic but pairing among close relatives seems uncommon. We examined the role of relatedness and familiarity on prairie vole social associations and reproduction by placing adult voles into 0.1-ha enclosures with familiar siblings, unfamiliar siblings, and unrelated, unfamiliar conspecifics. Live-trapping data indicated that indices of social pair bonding were random with respect to relatedness and familiarity. Among females whose litters were sired by a single male, litters were significantly more likely to be sired by unfamiliar than familiar males, but the number of litters sired by males that were unrelated to their partner was not different from the number of litters sired by males that were related to their partner. Additionally, females that produced offspring with familiar siblings were significantly more likely to have litters with multiple paternity than females not producing offspring with familiar siblings. However, multiple paternity was not influenced by relatedness of sires. Finally, older individuals were more likely to produce offspring with each other than with younger individuals. Our findings suggest that prior association is a more important mechanism of inbreeding avoidance than phenotype matching for prairie voles mating under ecologically relevant conditions.     

The effects of age and relatedness on mating patterns in thornbug treehoppers: inbreeding avoidance or inbreeding tolerance?

The social environment of many species includes synchronous maturation of siblings in family groups, followed by limited dispersal of adults from their natal site. Under these conditions, females may experience high encounter rates with same-age siblings during mate searching, increasing their risk of inbreeding. If inbreeding depression occurs, mating with a sibling is often considered maladaptive; however, in some contexts, the inclusive fitness benefits of inbreeding may outweigh the costs, favoring females that tolerate some level of inbreeding depression. We evaluated mating patterns in the treehopper Umbonia crassicornis, a semelparous species in which females encounter same-age siblings during mate searching. A female U. crassicornis that mates with a brother suffers from inbreeding depression. We used a free-choice mating design that offered females simultaneous mating opportunities with three groups of males: siblings, same-age nonsiblings, and older nonsiblings. These groups represent the types of males typically encountered by females during mate searching. Our goal was to assess whether mating patterns were influenced by inbreeding avoidance by evaluating two hypotheses: kin discrimination and age-based mating (older males cannot be siblings in this species). There was no difference in the proportions of females mating with siblings vs nonsiblings, suggesting an absence of kin discrimination. However, females mated with a greater proportion of older vs younger males. Given that females do not avoid siblings as mates despite a cost to inbreeding, our results provide a possible example of inbreeding tolerance. We also discuss some factors that may have contributed to the mating advantage of older males.     

Kin recognition in rainbowfish (Melanotaenia eachamensis): sex, sibs and shoaling

Living with relatives can be beneficial to individuals via the evolution of kin-directed altruism, but this is tempered by the increased risk of inbreeding. Therefore, in social species, the ability to recognise relatives can be highly advantageous. This study focuses on kin discrimination in the Lake Eacham rainbowfish, Melanotaenia eachamensis, an endangered freshwater species from north-east Queensland, Australia. First, I examined kin recognition abilities when a combination of both chemical and visual recognition cues was available. When given a choice of shoaling with same-sex groups, females spent significantly longer with full-sibs rather than half-sibs, full-sibs rather than non-relatives and half-sibs rather than non-relatives. Males spent significantly longer shoaling with full-brothers versus half-brothers, but showed no other shoalmate preferences. Second, in the presence of only chemical cues, females did not discriminate among groups of different levels of relatedness, but males showed a non-significant tendency to associate with full-sibs rather than non-relatives. Male shoaling behaviour seemed to be more influenced by factors other than relatedness, e.g. intra-sexual competition. Finally, I found that the shoaling preferences of females changed when exposed to groups of males. Females preferred to associate with non-relatives rather than half-brothers and non-relatives rather than full-brothers. There was no significant difference in the time spent with half-brothers versus full-brothers. Taken together, my results suggest that females have very good kin recognition abilities. They prefer to shoal with female relatives but avoid male relatives, and so are able to balance the benefits of nepotism and the costs of incest. Received: 2 May 2000 / Revised: 26 July 2000 / Accepted: 30 July 2000     

Why do males tolerate sneakers? Tests with the European bitterling, Rhodeus sericeus

In most species, males attack other males that attempt to gain fertilizations through sneak copulations. Here we report on a system where dominant males show a low level of aggression against sneakers at the initial stages of territory establishment. Females of the European bitterling, Rhodeus sericeus, lay their eggs in living mussels and males fertilize the eggs by releasing sperm over the mussels both before and after egg laying. When we allowed males to court females to a mussel containing no eggs at different male densities - one, two, four, or six males - the dominant male showed a low level of aggression against other males that released sperm. The dominant male became aggressive toward the other males only after eggs had been laid. This unusual pattern could be due to either some benefit of accepting sneakers or a high cost of aggression. We found support for both possibilities. The presence of several males decreased the time until a female spawned, whereas increased aggression by the dominant male against other males during a second female presentation, when the male was more territorial, interrupted courtship and increased the time until spawning. Females appeared to be attracted by both the presence of several males around a mussel and increased courtship under male competition. The bitterling mating system possibly differs from that of other species due to lack of investment in nest building and parental care, and high costs of defending the spawning site against sneakers.     

Female-biased immigration and male peace-keeping in groups of the shell-dwelling cichlid fish Neolamprologus multifasciatus

The small cichlid fish Neolamprologus multifasciatus is endemic to Lake Tanganyika and is unique among fish because it lives in complex social groups with several reproductive males and females, all of which participate in defending their territory against neighbors and intruders. Individuals use empty snail shells for breeding and shelter. Previous parentage analysis using microsatellites suggested occasional exchange of individuals between groups. In field experiments, we found that females showed a higher tendency than males to migrate into territories already occupied by a resident pair. The phenomenon and causes of female-biased immigration were further investigated in aquarium experiments: Nine of 15 females, but only 2 of 15 equally sized males, settled in territories of established pairs. Territorial males exhibited more aggression toward strange males (potential reproductive competitors) than toward strange females (potential additional mates); their females were more aggressive toward strange females (probably competitors for shells) than toward strange males. Apparently, a conflict exists between the sexes regarding the immigration of additional females. This conflict seems to be the selective basis for observed active male interference in aggressive disputes between females in the territory. Interfemale tolerance in a group was greater in the male’s presence than in his absence. Received: 1 February 2000 / Received in revised form: 2 May 2000 / Accepted: 5 May 2000     

Scent communication by female Columbian ground squirrels, Urocitellus columbianus

Scent-marking is a frequent behaviour of highly social ground squirrels and might play an important role in their social dynamics. Female Columbian ground squirrels exhibit considerable scent-marking during the reproductive period. We examined how gestating and lactating females responded to jugal gland scent-marks of same-sexed and opposite-sexed conspecifics with attention to genetic relatedness and the geographical location of the territory of individuals. We tested the dear-enemy, threat-level and kin-discrimination hypotheses to explain patterns of scent-marking. Females sniffed the scent of non-neighbouring males significantly longer than other types of scent categories and tended to over mark the scent of females more than the scent of males. Furthermore, females sniffed significantly longer at scents during gestation than during lactation. We concluded that scent-marking mainly functioned in the defence of female territories and for protection of pups against infanticidal females (threat-level hypothesis). Our results were also in accordance with the kin-discrimination hypothesis, because greater attention was paid to the marks of non-kin females. Kin females might not pose an infanticidal threat, perhaps explaining greater tolerance among related reproductive females. We concluded that scent-marking may be a relatively low-cost means of territorial defence, as well as a means of communication of aspects of individual identity.     

Multiple paternity in the cooperatively breeding fish <Emphasis Type="Italic">Neolamprologus pulcher</Emphasis>

In cooperative breeders, mature males may compete for fertilizations. In this study, we measured the degree of multiple paternity in a natural population of a cooperatively breeding fish. Neolamprologus pulcher (Perciformes: Cichlidae) is a highly social cichlid endemic to Lake Tanganyika. We used highly variable microsatellite loci to survey 12 groups with an average number of 10.6 brood care helpers per group and a total of 43 offspring (mean 3.6 per brood). In 11 of 12 groups, all young were assigned to the dominant female. The dominant male sired all offspring in three groups, part of the offspring in four groups, and in five groups, he had no paternity at all. In total, 44.2% of young were not fathered by the current male territory owner. Multiple paternity was found in 5 of 12 broods (41.7 %), with 8 of 35 young (22.9 %) being sired by males other than the respective territory owners. This is an exceptionally high rate of extra-pair paternity among cooperatively breeding vertebrates. Neither helpers present in these territories during collection nor neighbouring males were unequivocally assigned to have sired these extra-pair young. However, behavioural observations suggest that male helpers may have produced these young before being expelled from the territory in response to this reproductive parasitism. We discuss these results in the light of reproductive skew theory, cooperative breeding in vertebrates and alternative reproductive tactics in fish.     

Female aggression and male peace-keeping in a cichlid fish harem: conflict between and within the sexes in Lamprologus ocellatus

Summary Conflicts of interest within and between the sexes are important processes leading to variability in mating systems. The behavioral interactions mediating conflict are little documented. We studied pairs and harems of the snail-shell inhabiting cichlid fish Lamprologus ocellatus in the laboratory. Due to their larger size, males controlled the resource that limited breeding: snail shells. Males were able to choose among females ready to spawn. Females were only accepted if they produced a clutch within a few days of settling. When several females attempted to settle simultaneously the larger female settled first. Females were least aggressive when guarding eggs. Secondary females were more likely to settle when the primary female was guarding eggs. In established harems females continued to be aggressive against each other. The male intervened in about 80% of female aggressive interactions. Male intervention activity correlated with the frequency of aggression among the females in his harem. The male usually attacked the aggressor and chased her back to her own snail shell. When a male was removed from his harem, aggression between females increased immediately and usually the secondary female was expelled by the primary female within a few days. Time to harem break-up was shorter the more mobile the primary females' young were and did not correlate with the size difference between harem females. Male L. ocellatus interfere actively in female conflict and keep the harem together against female interests. Female conflict presumably relates to the cost of sharing male parental investment and to the potential of predation by another female's large juveniles on a female's own small juveniles.Correspondence to: F. Trillmich     

Olfactory cues,genetic relatedness and female mate choice in the agile antechinus (<Emphasis Type="Italic">Antechinus agilis</Emphasis>)

Females show mate preferences for males that are genetically dissimilar to themselves in a variety of taxa, but how females choose these males is not clearly understood. In this study, we examined the effects of olfactory stimuli and genetic relatedness on female mate choice in a small carnivorous marsupial, the agile antechinus (Antechinus agilis), during two breeding seasons. Captive female antechinus in oestrus were provided with a combination of male urine and body scent from two novel males, one more genetically similar and one more dissimilar to the females, in a Y-maze olfactometer. Genetic relatedness between females and pairs of males was determined using highly polymorphic, species-specific, microsatellite markers. Females consistently chose to visit the scents of males that were genetically dissimilar to themselves first, spent significantly more time near the source of those scents and showed more sexual and non-exploratory behaviours near those scents. These data demonstrate that chemosensory cues are important in mate choice in the agile antechinus and that females prefer males that are genetically dissimilar to themselves.     

Female aggressive response and hormonal correlates—an intrusion experiment in a free-living passerine

The optimal mating system is rarely the same for males and females—whereas males usually benefit from attracting additional females to the territory, this could incur costs for the resident female. Females should therefore prevent prospecting females from settling on the territory. We studied the male and female behavioral and hormonal responses to simulated female territorial intrusions in free-living bluethroats during the pre-laying period. In the study population, polygyny occurs with potential fitness costs for the resident female. We recorded different aspects of aggressive behavior before and after presentation of a live female decoy and playback of female song. These behaviors were compared with a set of intrusions using a male decoy. At the end of a trial, the birds were captured, and blood samples were analyzed for androstenedione, testosterone, estradiol and corticosterone. During the pre-intrusion period, none of the females were observed. Females generally responded strongly to the female decoy by increased flight rate, vocalizations, and by conspicuous perching. Nearly half of the males displayed to the female decoy but never while the resident female was present. We suggest that resident female aggression in bluethroats prevents courtship by her mate and signals her mating status to the female intruder. Female aggression could therefore prevent additional females to settle on the territory and shape the mating system. Females that responded with song had higher levels of estradiol. These findings suggest that estradiol may support aggression in breeding female birds.     

Interactions among females in polygynous yellow-headed blackbirds

Summary Two alternative hypotheses which attempt to predict how females within harems in polygynous species should behave toward one another were examined in a population of yellow-headed blackbirds (Xanthocephalus xanthocephalus). The hypothesis that females within a harem are co-operative was not supported. Females in large harems did not enjoy higher reproductive success than those in smaller harems and females within a territory did not initiate their nests close in time or space. The alternative hypothesis that females within a harem are competitive was also not supported. Nest density did not have a negative effect on female reproductive success, females within a territory did not initiate their nests far apart in time or space, and resident females were not very aggressive toward intruding female mounts during the settling period. The data support the idea that females settled independently of one another and had no effect on one another's reproductive success.     

Young-boy networks without kin clusters in a lek-mating manakin

I use 10 years of data from a long-term study of lek-mating long-tailed manakins to relate the social network among males to their spatial and genetic structure. Previously, I showed that the network connectivity of young males predicts their future success. Here, I ask whether kinship might shape the organization of this “young-boy network”. Not surprisingly, males that were more socially distant (linked by longer network paths) were affiliated with perch zones (lek arenas) that were further apart. Relatedness (r) among males within the network decreased as social distance increased, as might be expected under kin selection. Nevertheless, any role for indirect inclusive fitness benefits is refuted by the slightly negative mean relatedness among males at all social distances within the network (overall mean r = −0.06). That is, relatedness ranged from slightly negative (−0.04) to more negative (−0.2). In contrast, relatedness in dyads for which at least one of the males was outside the social network (involving at least one blood-sampled male not documented to have interacted with other banded males) was slightly above the random expectation (mean r = 0.05). The slight variations around r = 0 among males of different categories likely reflect dispersal dynamics, rather than any influence of kinship on social organization. Relatedness did not covary with the age difference between males. These results, together with previous results for lack of relatedness between alpha and beta male partners, refute any role for kin selection in the evolution of cooperative display in this lek-mating system. This contribution is part of the special issue “Social Networks: new perspectives” (Guest Editors: J. Krause, D. Lusseau, and R. James).     

Positive association between social and extra-pair mating in a polygynous songbird, the dickcissel (Spiza americana)

In polygynous species, males appear to gain additional offspring by pairing with multiple females simultaneously. However, this may not be true if some females copulate outside of the social pair bond. Polygynous males could experience lower paternity because of trade-offs among gaining multiple social mates, guarding fertility with these mates, and pursuing extra-pair matings. Alternatively, polygynous males could simultaneously gain extra social mates and have high paternity, either because of female preferences or because of male competitive attributes. We tested four predictions stemming from these hypotheses in a facultatively polygynous songbird, the dickcissel (Spiza americana). Unlike most previous studies, we found that males with higher social mating success (harem size) also tended to have higher within-pair paternity and that the number of extra-pair young a male sired increased significantly with his social mating success. Females that paired with mated males were not more likely to produce extra-pair young. In contrast, extra-pair paternity was significantly lower in the nests of females whose nesting activity overlapped that of another female on the same territory. This pattern of mating was robust to differences in breeding density. Indeed, breeding density had no effect on either extra-pair mating or on the association between polygyny and paternity. Finally, nest survival increased with harem size. This result, combined with the positive association between polygyny and paternity, contributed to significantly higher realized reproductive success by polygynous male dickcissels.     

Kin-preferential cooperation,dominance-dependent reproductive skew,and competition for mates in communally nesting female house mice

Little is known about the behavioural mechanisms facilitating kin-preferential communal breeding in wild house mice (Mus domesticus). We evaluated the effect of kinship and male availability on aggression, social structure and reproductive skew in groups of female mice freely interacting and reproducing in semi-natural indoor enclosures. Triplets of either sisters or non-sisters were established in enclosures provided with either one or three littermate males, which were unrelated and unfamiliar to the females. Sisters were more spatially associated and less aggressive than non-sisters, leading to higher incidences of communal breeding and reproduction. This is in agreement with theoretical considerations on kin selection in house mice. Reproductive success was highly skewed in favour of dominant females due to subordinate infertility or complete loss of first litters, which might have been caused by dominant females. In spite of this, subordinates only rarely dispersed from the enclosures, suggesting that perceived dispersal risk generally outweighed relatively reduced reproductive potentials. Aggression levels among females were significantly higher when one male was available, compared to when three males were available. We suggest that this might result from higher female-female competition for mates, due to the risk of missing fertilisation when synchronously oestrous females encounter limited numbers of males in a deme. Our results indicate that, first, communal nursing in house mice might have evolved to make the best out of a bad job rather than to enhance offspring fitness; and, second, that female-female mate-competition might play an important role in shaping female social structure in this polygynous mammal.Electronic Supplementary Material Supplementary material is available in the online version of this article at Communicated by F. Trillmich     

The influence of kinship on foraging competition in Siberian jays

Foraging competition in Siberian jay groups was examined in relation to dominance and kinship to determine whether juvenile offspring, by associating with adults, gained in food acquisition relative to juvenile immigrants. Members of the adult pair were dominant over juvenile cohort members and males were dominant to females, although an inter-sexual hierarchy, with male juveniles occasionally overlapping adult females, was suggested. Few competitive asymmetries were found between adults and retained offspring or adults and immigrant juveniles when they were competing for food together, but in kin and non-kin foraging groups, respectively. Male offspring visited the bait site more frequently than adult males, and female immigrants spent less time at the bait site than adult females. Under these circumstances, hoarding activities may limit the ability of alpha members to control resources. In mixed groups containing both juvenile offspring and juvenile immigrants, no difference was found in the number of visits made to the bait site, although load sizes and foraging rates were lower for immigrant birds. Retained juveniles obtained greater load sizes and foraging rates when associating with adults. The social dominance of parents suggests that they control juvenile foraging. Although offspring benefit in the presence of adults, adults may incur a cost to their restraint by spending more time at the bait site when competing with immigrants. These results extend conclusions from previous work describing the role of selective tolerance by adults which relaxes competition with retained offspring in Siberian jay winter groups. The present findings suggest that offspring benefit in both immediate and future energy gains, which may have a direct influence on survival. Received: 18 September 1996 / Accepted after revision: 26 January 1997     

Relatedness, polyandry and extra-group paternity in the cooperatively-breeding white-browed scrubwren (Sericornis frontalis )

We used DNA fingerprinting to examine the genetic parentage and mating system of the cooperatively breeding white-browed scrubwren, Sericornis frontalis, in Canberra, Australia. Our analyses revealed a remarkable variety of mating tactics and social organization. Scrubwrens bred in pairs or multi-male groups that consisted of a female and two or more males. Females were always unrelated to the pair male or alpha (dominant) male. Among multi-male groups we found three different mating tactics. Firstly, when alpha and beta (subordinate) males were unrelated, they usually shared paternity in the brood. This resulted in both males gaining reproductive benefits directly. Secondly, when beta males were not related to the female but were related to the alpha males, beta males sired offspring in some broods. In this situation, beta males gained reproductive benefits both directly and potentially indirectly (through the related alpha male). Thirdly, when beta males were related to the female or both the female and alpha male, they remained on their natal territory and did not sire any offspring. Thus beta males gained only indirect reproductive benefits. Overall, when group members were related closely, the dominant male monopolized reproductive success, whereas when the members were not related closely the two males shared paternity equally. This positive association between monopolization of reproduction and relatedness is predicted by models of reproductive skew, but has not been reported previously within a single population of birds. Other cooperatively breeding birds with both closely related and unrelated helpers may show a similar variety of mating tactics. Finally, we found that extra-group paternity was more common in pairs (24% of young) than in multi-male groups (6%), and we discuss three possible reasons for this difference. Received: 21 May 1996 / Accepted after revision: 14 December 1996