Shoaling decisions in three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>)—familiarity,kinship and inbreeding

Shoaling with familiar kin is a well-known phenomenon. It has been described both for adult and for fry of three-spined sticklebacks (Gasterosteus aculeatus). However, evidence of preference for kin independent of familiarity is scarce. Furthermore, inbreeding effects have not been studied for shoaling preferences and there is a lack of studies about changes in individuals’ ability to recognise kin during different phases of life history. We gave inbred and outbred, nonreproductive sticklebacks of different age the choice to shoal with a group of familiar siblings vs unfamiliar non-siblings and with unfamiliar siblings vs unfamiliar non-siblings. Subadult sticklebacks preferred to shoal with familiar kin over unfamiliar non-kin, but inbred and outbred individuals had similar preferences. When given the choice between unfamiliar siblings and unfamiliar non-sibs, adult outbred fish preferred the shoal of kin, while inbred fish behaved indifferently. Body characteristics of the group such as body mass, standard length and condition of its members did not significantly explain the shoaling preferences for kin. Thus, sticklebacks were capable of recognising familiar and unfamiliar kin. The latter capability was lost by inbreeding.     

Do kin always make better neighbours?: The effects of territory quality

Summary The effects of territory quality on kin-biased territorial defence behaviour and fitness of juvenile rainbow trout (Oncorhynchus mykiss) were examined by manipulating food and predation risk levels in an artificial stream channel. Groups of related (full sibling) or unrelated fry were observed in the channel under one of four treatments: (1) high food-low predator (high territory quality); (2) high food-high predator; (3) low food-low predator; and (4) low food-high predator (low territory quality). Fish within kin groups always initiated fewer aggressive interactions, defended smaller territories, exhibited higher proportions of threat type territorial defence behaviours (as opposed to overtly aggressive behaviours) and had a higher mean weight increase than non-kin groups. Within both kin and non-kin groups, decreasing territory quality significantly increased the frequency of aggressive interactions, the size of territories and decreased growth. It is argued that while kin-biased territorial defence behaviours are always present, decreased availability of resources and increased predation risk serve to reduce the magnitude of this kin bias. However, even in low-quality territories, the benefit of associating with kin may increase the probability of overwintering survival (increased fitness) of the young fish by increasing body size.     

Kin discrimination in the spotted hyena (<Emphasis Type="Italic">Crocuta crocuta</Emphasis>): nepotism among siblings

We examined patterns of affiliation, association, and aggression to inquire whether spotted hyenas (Crocuta crocuta) can distinguish among various groups of maternal and paternal siblings. If so, and if these animals conform to predictions of kin selection theory, then behavioral interactions among hyenas should vary with relatedness. We also considered familiarity-based recognition and phenotype matching as mechanisms hyenas might use to recognize kin. Patterns of affiliative behavior indicated that hyenas favored full-sibling littermates over half-sibling littermates or any other group of half-siblings. Rates of dyadic aggression generally did not vary with kinship. Hyenas associated more closely with half-sibling littermates than with non-littermate half-siblings, and hyenas affiliated more with maternal half-siblings than with paternal half-siblings, suggesting that familiarity-based cues might mediate discrimination among these sibling classes. In addition, operation of a phenotype-matching mechanism was suggested by the preference hyenas demonstrated during affiliative interactions for full- over half-sibling littermates, and by their lack of preference in these interactions for half-sibling littermates over non-littermate half-siblings. Phenotype matching was also suggested by our observation that paternal half-siblings cooperated more, and fought less, than did non-kin. Our data indicate that hyenas can discriminate among various types of siblings, that their social behavior conforms to predictions of kin selection theory, and that they recognize kin using mechanisms of both familiarity and phenotype matching.Communicated by S. Alberts     

Differential aggressiveness between fire salamander (<Emphasis Type="Italic">Salamandra infraimmaculata</Emphasis>) larvae covaries with their genetic similarity

Responding differentially to kin and non-kin is known to be adaptive in many species. One example is the inclusive fitness benefits of reducing aggression toward closer relatives. Little is known, however, about the ability of animals to assess differential degrees of genetic relatedness and to respond accordingly with differential levels of aggression. In the present study, we tested whether aggressiveness between body mass-matched pairs of fire salamander (Salamandra infraimmaculata) larvae covaried with the genetic similarity between them. We quantified aggressiveness at three levels of genetic similarity by selecting pairs within and across pools from recently genotyped populations. We also assessed aggression between pairs of siblings. Aggression and associated injuries decreased as genetic similarity increased across the groups. These findings suggest that cannibalistic salamanders can assess their degree of genetic relatedness to conspecifics and vary their behavioral responses depending on the degree of similarity between them along a genetic relatedness continuum.     

Kin and non-kin interventions in the aggressive disputes of vervet monkeys

Summary Interventions in aggressive disputes were investigated in a free-living troop of vervets (Cercopithecus aethiops sabaeus) in Barbados. Interventions on behalf of kin were more frequent than on behalf of non-kin. Both types of interventions were more likely when the intervening animal outranked the opponent; presumably because retaliation probability, and hence cost of intervening, is low against low ranking opponents. The number of interventions given on behalf of both kin and non-kin increased with the number of disputes in which they were involved. In contrast to kin interventions, the number of interventions given on behalf of non-kin was correlated with that received by non-kin, suggesting that reciprocation is a necessary component of non-kin interventions. Non-kin interventions were more likely when the recipient outranked the opponent, presumably because reciprocation probability is high. Pairs of non-kin form structured reciprocal relationships based on the proportion of interventions allocated to each other, and most non-kin interventions flowed through these relationships. Males intervened on behalf of non-kin more frequently than did females. The implications of the results for the evolution of kin and reciprocal altruism were discussed.     

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     

Kin and population recognition in sympatric Lake Constance perch (Perca fluviatilis L.): can assortative shoaling drive population divergence?

Prior studies have shown that perch (Perca fluviatilis L.) of Lake Constance belong to two genetically different but sympatric populations and that local aggregations of juveniles and adults contain closely related kin. In this study, we analysed the genetic structure of pelagic perch larvae to investigate if kin-structured shoals already exist during early ontogenetic development or might be the result of homing to natal sites. Analysis of the gene frequencies at five microsatellite loci revealed that three out of five pelagic aggregations of larvae showed significant accumulation of kin. To investigate possible mechanisms of shoal formation, we tested if perch use olfactory cues to recognize their kin. Choice tests in a fluviarium showed preference for odours of unfamiliar kin vs unfamiliar non-kin. Additionally, we showed that perch could differentiate between the odours of the two sympatric populations and significantly preferred unfamiliar and unrelated conspecifics of their own over the foreign population. Our results present a behavioural mechanism that can lead to the observed formation of kin-structured shoals in perch. We further discuss if the ability to discriminate between their own and a foreign population can result in assortative mating within populations and thus form the basis of “socially mediated speciation” in perch.     

Kinship and food availability influence cannibalism tendency in early-instar wolf spiders (Araneae: Lycosidae)

For potentially cannibalistic animals such as spiders, the ability to recognize and avoid kin and/or preferentially cannibalize non-relatives would permit exploiting conspecifics as prey while minimizing loss of inclusive fitness. We investigated the effects of relatedness and availability of alternative food on cannibalism tendency in pairs of juvenile Hogna helluo (Walckenaer), a North American wolf spider (Araneae: Lycosidae). For second-instar spiderlings (dispersing stage), cannibalism was more likely among pairs of non-sibs than pairs of sibs and, interestingly, was also more likely when other prey were available. We found no evidence of increased cannibalism in pairings involving broods of greatest average size disparity, indicating that size differences are unlikely to explain differences in cannibalism tendency. Additionally, the relative number of deaths from cannibalism or other causes did not increase with increasing risk of starvation. For third-instar spiderlings, which had lived independently of their mother and sibs following dispersal, cannibalism rates were very high in all treatments and there were no significant effects of relatedness or food availability. Our results suggest that spiders with predominantly solitary lifestyles may bias cannibalism toward non-kin during the juvenile associative period, and that this effect is lost in the subsequent instar. Results are discussed in the context of several potential mechanisms that might result in differential cannibalism.Communicated by M. Elgar     

The predatory mite Phytoseiulus persimilis manipulates imprinting among offspring through egg placement

A crucial question with respect to imprinting is how animals ensure that kin imprint on kin but not on non-kin. Imprinting takes place in a sensitive ontogenetic phase, usually in an early period of life or when offspring are produced, at which time the recipient imprints on the first referents met. In the predatory mite Phytoseiulus persimilis, imprinting among immature individuals happens in the larval stage immediately after hatching. I tested the hypothesis that adult P. persimilis females manipulate offspring imprinting by influencing the likelihood of encounters among recipients and referents via egg placement and egg aggregation. I conducted two experiments, one of which addressed imprinting and cannibalism, and the other addressed egg placement and egg aggregation. The imprinting experiment suggests that larvae imprint on any conspecific individual met in a sensitive ontogenetic phase and later on treat this individual as kin, irrespective of relatedness. After molting to protonymphs, imprinted individuals preferentially cannibalized unfamiliar to familiar larvae. Irrespective of familiarity, kin were cannibalized earlier than non-kin, suggesting the involvement of self-referent phenotype matching. The egg-placement experiment provides evidence that females adjust the aggregation level of their own eggs according to the degree of relatedness to present eggs from a previously ovipositing female. Both experiments in concert suggest that egg placement is a maternal strategy influencing imprinting among immature individuals. Apart from avoiding kin cannibalism, egg placement and imprinting by larvae may have relevance to other behaviors influenced by kin recognition, such as mate choice, prey-patch choice and dispersal.Communicated by L. Simmons     

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.     

Kinship and social tolerance among female and juvenile wild house mice: kin bias but not kin discrimination

Kin-biased social tolerance among house mice has been interpreted in terms of kin discrimination. However, several lines of evidence suggest it may instead be an incidental artifact of group member discrimination. This leads to very different predictions about the social consequences of relatedness within and between social groups. Social interactions between wild-stock adult female and juvenile house mice (Mus domesticus) established in neighbouring territorial groups within enclosures reveal relatedness to dominant males within groups as the major factor determining social tolerance of juveniles by females. Relatedness to the female herself had no significant independent effect on responses indicating tolerance. Females were generally more aggressive toward neighbouring-group juveniles (all unrelated to females) compared with those from their own group (all related to females), but were most aggressive toward neighbouring juveniles sired by the neighbouring dominant male. They were also more aggressive toward their own-group juveniles that had been sired by the neighbouring dominant but only when encountered in the neighbouring territory and with a greater bias against female juveniles. Females were least aggressive toward own-group juveniles sired by their own-group dominant male. The sire-bias in tolerance among females is similar to that reported among the dominant males themselves in an earlier study. As a result of the combined sire-bias in tolerance by adult males and females, juveniles sired by their own-group dominant males become less likely to intrude into a neighbouring territory with time. Overall, the results suggest that differences in social tolerance reflect discrimination on the basis of social group membership rather than relatedness between interactants and thus provide strong experimental evidence in support of incidental kin bias rather than kin discrimination.     

Vocal alliances in Chacma baboons (<Emphasis Type="Italic">Papio hamadryas ursinus</Emphasis>)

Theory predicts that females in species with matrilineal dominance hierarchies should use nepotistic support systems to maintain their family’s rank. Female Old World monkeys, however, form alliances against other females at surprisingly low rates. Nonetheless, in many species, females utter threat vocalizations when observing others’ disputes, suggesting that these vocalizations may function as ‘vocal alliances’. We describe a playback experiment testing the efficacy of vocal alliances in free-ranging female baboons. Subjects were played the same female’s threat-grunts under three separate conditions: after being threatened by the signaller’s close relative to mimic kin support, after being threatened by a female maternally unrelated to the signaller to mimic non-kin support, and after a friendly interaction with the signaller’s close relative as a control. Subjects responded more strongly to the playback and avoided the signaller and her matrilineal relatives for a longer period of time in kin support trials than in either non-kin support or no aggression trials. In contrast, there was no difference in subjects’ behaviour between non-kin support and no aggression trials. These results corroborate observational data showing that vocal support occurs at a higher rate than physical support in female baboons, and that kin are more likely to provide vocal support than non-kin. We conclude that vocal support plays a similar role as physical support in the alliances of female baboons.     

Effects of kinship on territorial conflicts among groups of lions,<Emphasis Type="Italic"> Panthera leo</Emphasis>

Inclusive fitness theory predicts that cost of tolerant behaviour during competitive interactions is lower for relatives than for nonrelatives. Many studies have examined the effect of relatedness on behaviour within social groups. In contrast, kin selection acting among groups has received less attention. The genetic structure of African lion (Panthera leo) populations creates a strong possibility that kin selection among groups modifies behaviour during group conflicts. We used playback experiments and genetic data to investigate the importance of relatedness during simulated territorial disputes in lions. However, we found no effect of relatedness on territorial behaviour. Degree of relatedness did not affect the decision to approach simulated intrusions, nor did it affect the behaviour during approaches. The decision to approach was instead affected by position within the territory and consecutive playback number (a measure of habituation). For playbacks that did elicit an approach, the speed of response was not detectably affected by relatedness, but was affected by odds (the ratio of residents to intruders), number of intruders, number of bouts, presence of cubs, position within the territory, temperature and playback number. Although responses were unaffected by relatedness, it remains possible that other aspects of behaviour during natural encounters among prides are affected by kin selection.Communicated by L. Sterck     

Kinship and aggression: do house sparrows spare their relatives?

Kin-selection theory predicts that relatedness may reduce the level of aggression among competing group members, leading to indirect fitness benefits for kin-favoring individuals. To test this hypothesis, we investigated whether relatedness affects aggressive behavior during social activities in captive house sparrow (Passer domesticus) flocks. We found that sparrows did not reduce their aggression towards kin, as neither the frequency nor the intensity of fights differed between close kin and unrelated flock-mates. Fighting success was also unrelated to kinship and the presence of relatives in the flock did not influence the birds’ dominance rank. These results suggest that the pay-offs of reduced aggression towards kin may be low in non-breeding flocks of sparrows, e.g. due to competition among relatives as predicted by a recent refinement of kin-selection theory. Our findings indicate that the significance of kin selection may be restricted in some social systems such as winter aggregations of birds. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The kin recognition system of carpenter ants (Camponotus spp.)

Summary Hamilton's (1964) hypothesis linking haplodiploidy and eusociality in the Hymenoptera could be reconciled with the occurrence of polygyny and multiple insemination if workers are able to distinguish full (3/4 related) sisters from other familiar matri- and patrilines within the colony, and direct altruistic behavior toward them preferentially. We examined this possibility in small genetically mixed nests of the carpenter ant Camponotus floridanus, formed by the transfer of worker pupae from two unrelated source colonies. In 120 h of observation on 12 queenright and 12 queenless nests, more than 15,000 behavioral interactions were recorded. Workers antennated familiar nonkin significantly more frequently than familiar sisters. However, they failed to discriminate consistently between kin and non-kin in food exchanges and grooming. Aggressive behavior was occasionally observed in some queenless nests, but almost never in the presence of a queen. When aggression did occur, it was directed significantly more often toward non-kin. Though related adult workers did not cooperate preferentially, the biases in antennation and aggression do indicate an ability to discriminate familiar kin from familiar nonkin, which may be employed in other contexts such as the rearing of reproductive brood.     

Kin recognition by juvenile predatory mites: prior association or phenotype matching?

Kin recognition, the biased treatment of conspecific individuals based on genetic relatedness, is a widespread phenomenon in animals. The most common mechanisms mediating kin recognition are prior association (familiarity) and phenotype matching. Recognition based on prior association allows identifying familiar individuals. Recognition based on phenotype matching is an extension of prior-association-based recognition and allows identifying familiar and unfamiliar individuals due to a shared phenotypic trait. I investigated which of the two mechanisms is used by cannibalistic juvenile predatory mites, Phytoseiulus persimilis. Protonymphs that were associated with either siblings or non-kin discriminated familiar and unfamiliar larvae and preferentially cannibalized the latter irrespective of genetic relatedness. In contrast, despite previous association with either siblings or non-kin, protonymphs did not discriminate unfamiliar sibling and unfamiliar non-kin larvae. Association in the larval stage therefore mediated kin recognition based on familiarity, but not phenotype matching in cannibalistic P. persimilis protonymphs. Furthermore, in the presence of a familiar prey individual, sibling cannibalism occurred significantly sooner than non-kin cannibalism. This quick sibling cannibalism may have been the consequence of preferential association of siblings and/or may indicate the occurrence of an alternative cannibal phenotype. I discuss the adaptive significance of prior-association-based recognition for P. persimilis juveniles and emphasize the ability of P. persimilis to use multiple recognition mechanisms in dependence of the ontogeny and the ecological context.     

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.     

Consequences of communal gall occupation and a test for kin discrimination in the aphid Tamalia coweni (Cockerell) (Homoptera: Aphididae)

This study investigated the consequences of communal gall induction on individual and group fitness in the aphid Tamaliacoweni. The possibilities that kin discrimination and foundress density are factors favoring communal gall occupation were examined. Clonally produced aphid foundresses were collected to create two treatments: clonal groups and groups of less closely related individuals. These were confined on suitable host plant tissue to compare their respective propensities towards communal behavior. There were no significant differences in the frequencies of communal gall occupation; therefore, active kin discrimination by T.coweni foundresses apparently does not play a role in their communal behavior, within the context of this experiment. In a second experiment, aphid foundress density on the host plant was manipulated in three treatments and was correlated with the frequency of communal gall occupation. Individual fitness was inversely related to the mean number of foundresses per gall. These results suggest that communal gall occupation does not necessarily represent mutual cooperation but may instead be the outcome of competition for limited gall sites on the host plant. However, natural selection at the clonal level may favor communal gall occupation under the conditions of resource limitation and high within-group relatedness. Received: 26 September 1997 / Accepted after revision: 28 March 1998     

Genetic relatedness and eusociality: parasite-mediated selection on the genetic composition of groups

Summary Contrary to the expectations of kin selection theory, intracolony relatedness in eusocial insects is often low. We examined the idea that associations of low relatedness (high genetic variability) may be advantageous because of negative frequency-dependent selection on common host phenotypes by rapidly evolving parasites and pathogens. Using the natural host-parasite system of the bumble bee Bombus terrestris and its intestinal trypanosome Crithidia bombi, we investigated the transmission properties of parasites in host groups. Within naturally infested nests and in artificially constructed groups of workers, prevalence of infestation increased with time of exposure (Table 1). The susceptibility of isolated groups of workers to the parasites to which they were exposed differed with identity and natural infestation of their nest of origin (Table 2). In addition, those workers that were related to the individual introducing an infection to their group were more likely to become infested than were unrelated workers (Table 3). Although the bumble bee workers in experimental boxes appeared to differ in behavior toward kin and non-kin, making more physical contacts with kin, we found no discernible relationship between number of physical contacts and prevalence of infestation in a group. Therefore, we conclude that differences in parasite transmission reflected interactions among different host and parasite phenotypes. This system thus demonstrates the factors necessary for negative frequency-dependent selection by parasites on common host phenotypes - variability for susceptibility and infectiousness in host and parasite populations and similarity for these traits among related individuals. If, as we show here, high genetic relatedness within groups enhances parasite transmission, kin directed altruism may increase the risk of contracting parasites and infectious diseases. Therefore, parasites and pathogens may be an important force moderating the genetic structure of social groups. Offprint requests to: J.A. Shykoff at the present address     

Infant handling and mortality in yellow baboons (<Emphasis Type="Italic">Papio cynocephalus</Emphasis>): evidence for female reproductive competition?

This study examines negative and positive infant handling behavior in 24 free-ranging yellow baboon infants (Papio cynocephalus) studied over a 5-year period in Mikumi National Park, Tanzania. We test predictions of the female reproductive competition hypothesis to explain patterns of infant handling behavior by adult females (excluding the infants mother) in relation to observed cases of infant mortality by age 3 months (25% of infants in this study). Results show that: (1) low-ranking infants received more negative infant handling than high-ranking infants; conversely high-ranking infants received more positive infant handling; (2) female kin engaged in higher levels of positive infant handling than did non-kin, whereas non-kin showed higher levels of negative infant handling; (3) rates of negative infant handling varied by season, with high levels at the onset of the rainy season; and (4) high level of negative infant handling was a significant predictor of infant mortality by age 3 months (infant rank and sex did not predict survival). We discuss how the occurrence and interpretation of infant handling behavior in the literature has likely been confused by different definitions of this behavior, as well as differences in the socio-ecological context in which this behavior occurs.Communicated by C. Nunn