Kin recognition by larval wood frogs (Rana sylvatica): effects of diet and prior exposure to conspecifics

Summary We investigated kin recognition by larval wood frogs (Rana sylvatica) in blind laboratory experiments using spatial affinity as a recognition assay. Tadpoles reared with full-sibs displayed a significant preference for familiar full-sibs over unfamiliar non-kin, but failed to discriminate between unfamiliar full-sibs and unfamiliar paternal half-sibs. Tadpoles reared in social isolation (with or without maternal egg jelly) from the two-celled embryonic stage displayed a significant preference for unfamiliar full-sibs over unfamiliar non-kin. Tadpoles reared on a meat diet with their full-sibs: 1) exhibited a significant preference for unfamiliar full-sibs fed meat over unfamiliar non-kin fed meat, 2) failed to discriminate between unfamiliar full-sibs fed lettuce and unfamiliar non-kin fed meat, 3) exhibited a significant preference for unfamiliar non-kin fed meat over unfamiliar non-lin fed lettuce, 4) failed to discriminate between unfamiliar full-sibs fed meat and unfamiliar full-sibs fed lettuce, and 5) displayed a significant spatial preference for odors associated with meat (a familiar food) over odors associated with lettuce (an unfamiliar food). Our results, together with those of Cornell et al. (1989), indicate that the recognition cue of larval R. sylvatica has both genetic and environmental (dietary) components. Our findings establish that previous exposure to maternal egg jelly, kin, or conspecifics is not necessary for the development of kin recognition ability in larval R. sylvatica. Our results are more consistent with the self-learning of recognition cues (a form of phenotype matching) than with a recognition mechanism that involves a genetically fixed recognition template. Finally, our results indicate that increasing similarity between the recognition template and perceived cue does not necessarily result in increasing spatial affinity for kin.     

The ontogeny of kin recognition in tadpoles of the toadBufo melanostictus (Anura; Bufonidae)

The ontogeny of kin recognition and influence of social environment on the development of kin recognition behaviour was experimentally investigated in tadpoles of Bufo melanostictus that lived in aggregations and showed low larval dispersion. Embryos and tadpoles of the toad were reared as (i) kin only, (ii) with kin and non-kin (separated by a mesh screen), and (iii) in isolation. They were tested for the ability to discriminate between (i) familiar siblings and unfamiliar non-siblings, (ii) familiar siblings and familiar non-siblings and, (iii) unfamiliar siblings and unfamiliar non-siblings. All tadpoles were fed on boiled spinach before conducting trials. Preference of test tadpoles to associate near the end compartments whether empty or containing members of specific stimulus groups was assessed using a rectangular choice tank. When tested in tanks with empty end compartments, the test tadpoles showed random distribution and thus no bias for the apparatus or the procedure. In the presence of kin/non-kin in the end compartments a significantly greater number of test tadpoles spent the majority of the time near familiar or unfamiliar kin rather than near familiar or unfamiliar non-kin. Kin discrimination ability persisted throughout larval development. Familiarity with siblings is not required for discriminating kin from non-kin, and kin discrimination ability is not modified following exposure to non-kin. Also, involvement of dietary cues is unlikely to be the prime mechanism of kin recognition inB. melanostictus unlike in some other anurans.     

Kin recognition by tadpoles and froglets of the wood frog Rana sylvatica

Summary We investigated kin recognition by the wood frog Rana sylvatica in blind laboratory experiments using spatial proximity as a recognition assay. Tadpoles were tested for the ability to discriminate between: 1) familiar full-sibs and unfamiliar non-kin, 2) unfamiliar paternal half-sibs and unfamiliar non-kin, and 3) familiar and unfamiliar full-sibs. Tadpoles discriminated full- and paternal half-sibs from unrelated conspecifics, but did not discriminate between familiar and unfamiliar full-sibs. Froglets from the same laboratory population were tested for the ability to discriminate between 1) familiar full-sibs and unfamiliar non-kin, and 2) unfamiliar paternal half-sibs and unfamiliar non-kin. Froglets preferentially associated with full- and half-sibs over unrelated conspecifics. Our results show that familiarity, i.e., prior association, is not necessary for kin recognition in tadpoles and froglets. The ability of tadpoles and froglets to recognize unfamiliar paternal half-sibs demonstrates that a common maternal factor is not necessary for kin recognition, and indicates that the recognition cue has a genetic component. Our results add to the increasing evidence that a variety of vertebrate and invertebrate animals have the ability to recognize unfamiliar kin by using genetically specified recognition cues.     

基于交叉抚育的雄性根田鼠对异性同胞尿气味的识别

通过交叉抚育建立室内繁殖种群,在断奶后（80日龄）分别取这些供体的新鲜尿气味作刺激物,在行为观察箱中观察和记录雄性根田鼠对雌鼠气味的行为反应,以研究根田鼠同胞识别的化学通讯机制。结果表明：①在不同的发育时期（2～70日龄）,雄性同巢同胞与异巢同胞的体重没有显著差异。②雄性根田鼠对雌性同巢非同胞气味的接近潜伏期显著长于对异巢非同胞的接近潜伏期（P〈0．05）,其对异巢非同胞气味的访问时间和嗅舔时间都显著高于同巢非同胞气味（P〈0．05）。③雄性根田鼠对雌性异巢同胞和异巢非同胞气味的不存在明显偏好。其对两者的接近潜伏期、访问频次、访问时间、嗅舔频次和嗅舔时间等行为响应均无显著差异（P〈0．05）。这些结果表明,80日龄时,雄性根田鼠能够识别熟悉和陌生的无亲属关系雌性尿气味,但不能区分陌生的亲属和非亲属,因此,其异性同胞识别的机制为共生熟悉模式。     

Paternal kin discrimination in wild baboons.

Mammals commonly avoid mating with maternal kin, probably as a result of selection for inbreeding avoidance. Mating with paternal kin should be selected against for the same reason. However, identifying paternal kin may be more difficult than identifying maternal kin in species where the mother mates with more than one male. Selection should nonetheless favour a mechanism of paternal kin recognition that allows the same level of discrimination among paternal as among maternal kin, but the hypothesis that paternal kin avoid each other as mates is largely untested in large mammals such as primates. Here I report that among wild baboons, Papio cynocephalus, paternal siblings exhibited lower levels of affiliative and sexual behaviour during sexual consortships than non-kin, although paternal siblings were not significantly less likely to consort than non-kin. I also examined age proximity as a possible social cue of paternal relatedness, because age cohorts are likely to be paternal sibships. Pairs born within two years of each other were less likely to engage in sexual consortships than pairs born at greater intervals, and were less affiliative and sexual when they did consort. Age proximity may thus be an important social cue for paternal relatedness, and phenotype matching based on shared paternal traits may play a role as well.     

Investigating the Effect of Familiarity on Kin Recognition of Three‐Spined Stickleback (Gasterosteus aculeatus)

The ability to discriminate between related and unrelated individuals has been demonstrated in many species. The mechanisms behind this ability might be manifold and depend on the ecological context in which the species lives. In brood‐caring species, both familiarity and phenotype matching are known to be used in kin recognition. However, results of studies disentangling these two phenomena have proved contradictory. We aimed to broaden our knowledge about the mechanisms of kin recognition using shoaling preferences of three‐spined stickleback (Gasterosteus aculeatus) as a model behavior. In our first experiment, focal fish had the choice to shoal either with kin or unfamiliar non‐kin. In half of the trials, kin groups were composed of familiar individuals, while they were unfamiliar in the other half. Focal fish significantly preferred kin as shoaling partner, a result which was not reinforced by familiarity. In our second experiment, focal fish were given the choice between a shoal of familiar kin and a shoal of unfamiliar kin. Here, focal fish did not show any significant preference. These results indicate that familiarity does not impact stickleback's ability to recognize kin. Furthermore, they show that familiarity does not overrule recognition based on phenotype matching or innate recognition, underlining the importance of these mechanisms. Finally, our results lead to the assumption that individual recognition might play a minor role also in non‐kin‐based preferences for familiars.     

Kin discrimination and female mate choice in the naked mole-rat Heterocephalus glaber

Naked mole-rats are fossorial, eusocial rodents that naturally exhibit high levels of inbreeding. Persistent inbreeding in animals often results in a substantial decline in fitness and, thus, dispersal and avoidance of kin as mates are two common inbreeding avoidance mechanisms. In the naked mole-rat evidence for the former has recently been found. Here we address the latter mechanism by investigating kin recognition and female mate choice using a series of choice tests in which the odour, social and mate preferences of females were determined. Discrimination by females appears to be dependent on their reproductive status. Reproductively active females prefer to associate with unfamiliar males, whereas reproductively inactive females do not discriminate. Females do not discriminate between kin and non-kin suggesting that the criterion for recognition is familiarity, not detection of genetic similarity per se. In the wild, naked mole-rats occupy discrete burrow systems and dispersal and mixing with non-kin is thought to be comparatively rare. Thus, recognition by familiarity may function as a highly efficient kin recognition mechanism in the naked mole-rat. A preference by reproductively active females for unfamiliar males is interpreted as inbreeding avoidance. These findings suggest that, despite an evolutionary history of close inbreeding, naked mole-rats may not be exempt from the effects of inbreeding depression and will attempt to outbreed should the opportunity arise.     

Kin recognition versus familiarity in a solitary mustelid, the European polecat Mustela putorius

The aim of this experimental study was to investigate kin discrimination in the polecat and to analyse the ontogeny of interactions. Juvenile polecats (ten males and nine females) had been raised under four distinct experimental conditions: 1, kin, familiar; 2, kin, unfamiliar; 3, non-kin, familiar; 4, non-kin, unfamiliar. During dyadic encounters between polecats in neutral enclosures, the number of positive (tolerance), negative (aggression), intermediate (intimidation), and neutral interactions (no direct interactions) were recorded at two different ages of the animals (50 and 70 days old). Male-male encounters were characterised by more aggressive behaviour than female-female ones. The proportion of these negative interactions increased with age, while the proportion of positive interactions decreased. Although aggressive behaviours varied among groups, the reaction did never differ with the kinship. Kin selection theory provides successful explanations for a wide range of phenomena, but our results suggest that multiple mechanisms running simultaneously might be involved in social behaviours. Familiarity clearly influenced the social behaviour of polecats and might be involved in a kin facilitation effect favouring interactions. Animals raised together demonstrated more positive and less negative interactions, so that, despite the individualistic way of life of the polecat, familiarisation may result in more tolerance, emphasising that solitary species may provide significant information on social life. Anyway, familiarisation in polecat may be regarded as a cognitive form of recognition.     

Kin recognition in Bufo scaber tadpoles: ontogenetic changes and mechanism

Ontogenetic changes in kin-recognition behavior, effect of social environment on kin-recognition ability, and use of visual and chemical cues in kin recognition have been studied in tadpoles of Bufo scaber after rearing them with kin, in mixed groups, or in isolation from Gosner stage 12 (gastrula). By use of a rectangular choice tank the tadpoles were tested for their ability to choose between (a) familiar siblings and unfamiliar non-siblings, (b) unfamiliar siblings and familiar non-siblings, and (c) unfamiliar siblings and unfamiliar non-siblings. When tested without any stimulus groups in the end compartments of the tank, random distribution was observed for the tadpoles and no bias for the apparatus or the procedure. In the presence of kin and non-kin in the end compartments, significantly more tadpoles spent most of their time near kin (familiar or unfamiliar) rather than near non-kin during early larval stages, up to stage 37. After stage 37 (characterized by the differentiation of toes), test tadpoles showed no preference to associate with kin, suggesting an ontogenetic shift in the kin-recognition ability in B. scaber. In experiments involving selective blockade of visual or chemical cues the test tadpoles preferentially associated near their kin on the basis of chemical rather than visual cues. These findings suggest that familiarity with siblings is not necessary for kin recognition and that kin-recognition ability is not modified after exposure to non-kin by mixed rearing. The findings for B. scaber indicate a self referent phenotype matching mechanism of kin recognition which is predominantly aided by chemical rather than visual cues.     

Kin discrimination and altruism in the larvae of a solitary insect

Kin selection theory predicts altruism between related individuals, which requires the ability to recognize kin from non-kin. In insects, kin discrimination associated with altruistic behaviour is well-known in clonal and social species but in very few solitary insects. Here, we report that the solitary larvae of a non-social insect Aleochara bilineata Gyll. (Coleoptera; Staphylinidae) show kin discrimination and sibling-directed altruistic behaviour. Larvae superparasitize more frequently the hosts parasitized by non-kin individuals than those hosts parasitized by siblings. Kin discrimination probably occurs by self-referent phenotype matching, where an individual compares its own phenotype with that of a non-familiar related individual, a mechanism rarely demonstrated in animals. The label used to recognize kin from non-kin corresponds to substances contained in the plug placed on the hosts by the resident larvae during the parasitization process. Kin competition induced by a limited larval dispersion may have favoured the evolution of kin recognition in this solitary species.     

Olfactory kin recognition in a songbird

The ability to recognize close relatives in order to cooperate or to avoid inbreeding is widespread across all taxa. One accepted mechanism for kin recognition in birds is associative learning of visual or acoustic cues. However, how could individuals ever learn to recognize unfamiliar kin? Here, we provide the first evidence for a novel mechanism of kin recognition in birds. Zebra finch (Taeniopygia guttata) fledglings are able to distinguish between kin and non-kin based on olfactory cues alone. Since olfactory cues are likely to be genetically based, this finding establishes a neglected mechanism of kin recognition in birds, particularly in songbirds, with potentially far-reaching consequences for both kin selection and inbreeding avoidance.     

Kin discrimination in sticklebacks is mediated by social learning rather than innate recognition

Theory predicts several advantages for animals to recognize kin. These include inbreeding avoidance and an increase in inclusive fitness. In shoaling species, kin recognition may lead to an increased amount of altruism among shoal members. Adult, non‐reproductive three‐spined sticklebacks, Gasterosteus aculeatus, prefer to shoal with kin. This preference was shown for familiar as well as for unfamiliar individuals. However, whether it is based on learned cues of familiar individuals or on innate mechanisms like self‐referent phenotype matching or ‘true’ kin recognition through recognition alleles remains unknown. In our experiments, juvenile fish were given the choice between shoals that differed in relatedness and familiarity. The number of testfish who joined each group indicated that sticklebacks prefer to shoal with familiar kin when the alternative shoal was composed of unfamiliar non‐kin. When one shoal consisted of familiar kin while the second consisted of familiar non‐kin testfish did not show any preference. Kin recognition in sticklebacks is thus most likely mediated by social learning.     

Kin recognition and the 'armpit effect': evidence of self-referent phenotype matching

In species with multiple paternity or maternity, animals may best assess their relatedness to unfamiliar conspecifics by comparing their own phenotype(s) with those of unidentified individuals. Yet whether animals can recognize kin through self-matching is controversial. Because golden hamsters (Mesocricetus auratus) mate multiply and can produce multiply sired litters, they were tested for their ability to use self-matching for kin recognition. Hamsters that were reared only with non-kin since birth responded differentially to odours of unfamiliar relatives and non-relatives. Postnatal association with kin was not necessary for this discrimination. Prenatal learning was unlikely because of delayed production and perception of social odours. To our knowledge, this is the first demonstration that a vertebrate can use its own phenotype for kin-recognition purposes without prior experience with kin. By using itself as a referent, rather than its siblings or parents, a golden hamster may be better able to direct nepotism towards the most appropriate individuals. Kin discrimination via self-inspection may be especially important in nepotistic contexts (to identify most closely related conspecifics), whereas inclusion of the phenotypes of close kin as referents may be favoured in mate-choice contexts (to identify all related individuals).     

The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation

I re-examine the four most widely proposed mechanisms of kin discrimination among vertebrates and conclude that the current categorization of kin discrimination mechanisms has been counterproductive because it has a hindered a clear understanding of the basic mechanisms by which animals discriminate kin. I suggest that there likely is only one authentic mechanism of kin discrimination and that this mechanism is learning, particularly associative learning and habituation. Observed differences in the way animals discriminate between kin and non-kin are due only to the cues (e.g., individually-distinctive, family-distinctive, or self) that are used, and not to different mechanisms per se. I also consider whether kin discrimination is mediated by specially evolved kin recognition systems, defined as neural mechanisms that allow animals to directly classify conspecifics as either kin or non-kin. A preliminary analysis of vertebrate recognition systems suggests that specialized neural, endocrine, and developmental mechanisms specifically for recognizing kin have not evolved. Rather, kin discrimination results from an extension of other, non-specialized sensory and cognitive abilities of animals, and may be derived from other forms of social recognition, such as individual, group, or species recognition.     

Familiarity adds to attractiveness in matters of siskin mate choice

There is currently considerable controversy in evolutionary ecology revolving around whether social familiarity brings attraction when a female chooses a mate. The topic of familiarity is significant because by avoiding or preferring familiar individuals as mates, the potential for local adaptation may be reduced or favoured. The topic becomes even more interesting if we simultaneously analyse preferences for familiarity and sexual ornaments, because when familiarity influences female mating preferences, this could very significantly affect the strength of sexual selection on male ornamentation. Here, we have used mate-choice experiments in siskins Carduelis spinus to analyse how familiarity and patterns of ornamentation (i.e. the size of wing patches) interact to influence mating success. Our results show that females clearly prefer familiar individuals when choosing between familiar and unfamiliar males with similar-sized wing patches. Furthermore, when females were given the choice between a highly ornamented unfamiliar male and a less ornamented familiar male, half of the females still preferred the socially familiar birds as mates. Our finding suggests that male familiarity may be as important as sexual ornaments in affecting female behaviour in mate choice. Given that the potential for local adaptation may be favoured by preferring familiar individuals as mates, social familiarity as a mate-choice criterion may become a potential area of fruitful research on sympatric speciation processes.     

Major histocompatibility complex and kin discrimination in Atlantic salmon and brook trout

Many species of salmonids can discriminate kin from unrelated conspecifics using olfactory cues. In this study, we determined the role of the major histocompatibility complex (MHC) in kin discrimination by juvenile Atlantic salmon (Salmo salar) and brook trout (Salvelinus fontinalis). Genetic variation at the highly polymorphic exon coding for peptide-binding region of an MHC class II gene was studied using polymerase chain reaction and denaturing gradient gel electrophoresis. Experiments compared discrimination ability based on MHC haplotypes both within and among kin and non-kin groups. Juveniles chose kin sharing both alleles over kin sharing no alleles. Juveniles also preferred non-kin sharing both alleles to non-kin sharing no alleles. These data suggest that the MHC class II gene influence kin discrimination in juvenile Atlantic salmon and brook trout. The influence of additional genes was also apparent in trials where juveniles were able to recognize kin sharing no alleles over non-kin sharing no alleles. However, the inability of juveniles to discriminate between kin sharing no alleles and non-kin sharing either one or both alleles indicates that MHC is as potent as the rest of the genome in producing distinguishable odours.     

Kin discrimination in salmonids

Summary The data presented here suggest that significant selection pressures towards kin discrimination behaviour patterns result from kin-biased territorial defence behaviour patterns. Salmonids employ a phenotype matching recognition mechanism allowing individuals to discriminate unfamiliar kin. Kin discrimination abilities allow individuals to reduce the levels of aggression associated with territorial defence towards related conspecifics and to defend smaller territories near kin versus non-kin. This kin-biased territorial defence behaviour is observed in at least one species under a wide range of territorial quality conditions. Within kin groups, subordinate individuals obtain a greater number of foraging attempts, resulting in kin-biased foraging within the social group. As a result of this kin-bias, individuals within kin groups show significantly higher mean weight increases (increased direct fitness benefits) and reduced variance in these increases (increased indirect benefits). Since all individuals within the kin groups obtained higher, less variable weight increases, we can argue that individuals are increasing their inclusive fitness as a result of these kin-biased behaviour patterns.Based on these results, and on what is known about the life history of a variety of salmonid and non-salmonid species, we can formulate a number of testable predictions. By testing these predictions, we may be better able to understand both the proximate and ultimate causation of kin discrimination abilities in a variety of fishes.     

基于交叉抚育的雌性根田鼠对雄鼠尿气味的识别

通过交叉抚育建立同巢同胞、同巢非同胞、异巢同胞和异巢非同胞个体组成的室内繁殖种群,在断奶后（80日龄）分别取这些供体的新鲜尿作刺激物,在吕字型观察箱中观察和记录雌性根田鼠对雄鼠气味的行为响应,以研究根田鼠同胞识别的化学通讯机制。结果表明：（1）成年雌性根田鼠对雄性同巢同胞气味的接近潜伏期极显著短于对同巢非同胞气味的接近潜伏期（P〈0.01）,而其对两者的访问时间和嗅舔时间之间的差异并不显著（P〉0.05）;（2）雌鼠对雄性异巢同胞和异巢非同胞气味无明显偏好。其对两者的接近潜伏期、访问时间和嗅舔时间等行为响应均无显著差异（P〉0.05）;（3）雌鼠对雄性同巢非同胞和异巢非同胞的接近潜伏期差异并不明显（P〉0.05）,对两者访问时间和嗅舔时间的差别不大（P〉0.05）;（4）比较雌鼠对异巢同胞和同巢同胞气味的行为响应发现,其对后者的接近潜伏期显著短于前者（P〈0.05）,其对两者访问时间、嗅舔时间之间的差异未达到显著水平（P〉0.05）。这些结果表明,80日龄时,雌性根田鼠具有亲属识别能力,其同胞识别的机制可能为共生熟悉和表型匹配两种模式协同作用。     

Association preference and mechanism of kin recognition in tadpoles of the toad <Emphasis Type="Italic">Bufo melanostictus</Emphasis>

In experiments with specially designed choice tanks, tadpoles of Bufo melanostictus spend significantly greater amounts of time near kin than near non-kin. However, in the absence of kin members, they prefer to spend more time near non-kin rather than stay away in isolation in the opposite blank zone with no company. This implies that association of toad tadpoles with their kin is due to attraction rather than repulsion from non-kin. Experiments designed to elucidate the sensory basis of kin recognition showed that toad tadpoles recognize their kin based on chemical cues rather than visual cues. They can also discriminate between homospecific non-kin and heterospecific (Sphaerotheca breviceps) tadpoles since the tadpoles spent significantly greater amounts of time near the former than near the latter. These findings suggest that where kin members are unavailable, selection may have favoured living with non-kin so as to derive benefits from group living and that a phenotype-matching mechanism may operate for both kin and species discrimination in B. melanostictus.     

A test of alternative hypotheses for kin recognition in cannibalistic tiger salamanders

The function of kin recognition is controversial. We investigatedthe adaptive significance of kin discrimination in cannibalistictiger salamander larvae, Ambystoma tigrinum. Previous laboratoryexperiments show that cannibals preferentially consume lessrelated individuals. We hypothesized that this example of kinrecognition (1) is a laboratory artifact, (2) is a by-productof sibship-specific variation in escape responses, because cannibalsfrom families with rapid responses may be more likely to cannibalize slowlyescaping non-kin, (3) is an epiphenomenon of species recognition,(4) functions in disease avoidance, because kin may be moreinfectious than non-kin, or (5) is favored by kin selection.We evaluated these five hypotheses by using laboratory and fieldexperiments to test specific predictions made by each hypothesis.We rejected hypotheses 1-4 above because (1) kin recognitionwas expressed in the wild, (2) escape responses did not reliablypredict whether a cannibal would ingest kin or non-kin, (3)kin recognition was not most pronounced in populations wheretiger salamanders co-occur with other species of salamanders,and (4) non-kin prey were more likely than kin to transmit pathogensto cannibals. However, we established that the necessary conditionfor kin selection, Hamilton's rule, was met. Thus, our resultsimplicate kin selection as the overriding reason that cannibalistictiger salamanders discriminate kin.