When birds are faced with a choice of potential recipient nests, helpers preferentially help the breeding pair to whom they are most closely related. This has been documented for the white-fronted bee-eater, Galapagos mockingbird, bell miner, noisy miner and pinyon jay. The only species that doesn’t show kin favouritism is the Mexican jay (Komdeur & Hatchwell 1999)
Female Belding’s ground squirrels mate with one to eight males and most litters are multiply sired (Hanken & Sherman 1981). In the field, females are slightly less likely to attack full sisters than maternal half sisters, and more likely to share territories with full sisters (Holmes & Sherman 1982).
This is all observational evidence and although it is important to study behaviour in its natural surroundings, conducting reliable and repeatable experiments is very difficult without disturbing the animals. There is a clear need for quantitative data in order to lend credibility to the act of kin recognition.
An intraspecific cross-fostering experiment in the Caspian tern showed that parents will accept young substituted for their own within the first week of life. However when given a choice between their own and alien young, in nest scrapes either side of the original nest, they will unfailingly choose their own throughout the nesting period. (Shugart 1977). In this species, the same results were obtained in egg fostering experiments (Shugart 1987).
An experiment on the mating preferences in Japanese quail (Bateson 1982) revealed that the most strongly preferred mates are slightly different from individuals that are familiar from early life. In the experiment which gave the test bird a choice of different members of the opposite sex chose on average to spend more time with novel first cousins than unrelated individuals or closer kin.
These examples do illustrate that animals can exhibit differential behaviour towards closely related kin. Grafen (1990) argues that this may not necessarily be true kin recognition and attributes this differential behaviour as an artefact of other recognition systems. However after reading his paper I am not entirely convinced as Grafen makes too many assumptions and I do not believe in light of current studies that kin recognition is an artefact but a genuine recognition process. However what he does highlight is that although animals may exhibit certain behaviours that are attributed to kin recognition, they may be assigned that definition due to the subjective ness of the observer. For example many anuran tadpoles appear to associate preferentially with siblings. This could be interpreted as nepotism, learning kin phenotypes for optimal out breeding, or simply associating with any conspecifics that smell like the natal site. Researchers must be careful not to make generalisations based on their own preconceptions of the animals’ behaviour.
Komdeur and Hatchwell (1999) illustrate a series of problems concerned with previous studies of kin recognition. The first problem concerns the fact that ethologists in their search for kin recognition or cues have often only used one method of experimentation, which may not be the appropriate one in the first place (Davies &McCaffery 1989 Adelie penguins), whereas different experimental designs will lead to different results. This can often lead to inconclusive results. Also they state that kin recognition has a temporal quality and that data will vary according to the age of the animal, for example juveniles leaving parental territory upon reaching sexual maturity.
Despite the problems listed above there is an overwhelming amount of evidence that nepotunistic behaviours do occur in nature and there has been a lot of work to support their underlying mechanisms. In order to fully understand the mechanisms of kin recognition we must first look at how recognition systems work in general.
All recognition systems require an actor and a recipient, usually in the form of another individual (except in self recognition). The stimulus of the recipient invokes a behavioural response form the actor. Conceptually this process can be split into three parts.
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Production The nature and development of labels (cues) in recipients that actors use to recognise them. (Sherman 1997). In kin recognition the animal should use cues that distinguish the most closely related kin from other individuals, maximising the acceptance threshold. It may be any aspect of the phenotype that signifies kinship reliably, e.g. chemical odours, and may be genetic or environmental in origin.
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Perception The sensory detection of labels by actors and subsequent phenotype matching; i.e. comparison of labels to a template (internal representation) of the phenotypic attributes of desirable (fitness enhancing) or undesirable (fitness reducing) recipients; the ontogeny of templates is also part of this component (Sherman 1997). Recognition occurs when the recipients’ phenotypes match these templates closely enough. There are many origins of these recognition templates. Recognition templates are derived from learning, by associating characteristics of individuals with the consequences of interacting with them directly, observing their interactions with others or learning the characteristics of individuals that are likely, given their representation in time and space, to be desirable or undesirable. In some cases, paper wasps learn recognition odours from their nests and not necessarily from nest mates themselves; this is an example of an environmental factor. The matching process between the cue and the template will be weighted with a bias towards selection, optimising the balance between the cost of making acceptance and rejection errors. For example if acceptance errors are costly then actors should disproportionately weight cues that are possessed exclusively by closely related kin, even if some close kin are rejected.
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Action The nature and determinants of actions performed, depending on the similarity between actor’s templates and recipients cues (Sherman 1997). Given this relationship what action should the animal take, should it be a graduated response correlating precisely with the degree of relatedness or should it be a binary response, all or nothing, for example the decision between attacking or not attacking. When the acceptance threshold (the balance between acceptance and rejection errors) varies in different recognition contexts, organisms should assess environmental cues that distinguish such contexts. These have been termed ‘indirect’ cues in the case of kin recognition, as it doesn’t rely on phenotypic characters.
The process of kin recognition is understood but the mechanisms by which it is enacted are still contentious but each one has a series of supporting experiments and in all likelihood, kin recognition doesn’t solely rely on one mechanism, the same as we do not rely on one form of locomotion.
Recognition Alleles.
This mechanism requires that a gene (complex) confer an identifiable phenotype on its carrier, which also enables the carrier to perceive that phenotypic trait and discriminate accordingly. Hamilton (1964) originally posed the idea for recognition alleles, and Dawkins (1982) took this model one step further by suggesting that such genes also conveyed a behavioural response as well. Such “green beard genes” as Dawkins put it, although an attractive idea at the time are flawed in three main ways. The green beard genes would tend to be genetic outlaws, replicating themselves at the expense of the genome. They would also be open to cheating as mutant alleles would arise that had the recognition phenotype but none of the altruistic behaviour, and that green beard genes tend to be complex and how can a single gene encode for this type of behaviour. An example of a recognition allele would be the use of the Major Histocompatibility Complex (MHC) in laboratory rodents to confer specific odours in the urine that allows for individualistic discrimination. This was determined by breeding lines of mice that differ only in the MHC. Several lines of evidence have established that mice and rodents are able to establish individuals based only on the difference of their MHC’s. (Brown & Ekland 1994). However this doesn’t prove that the MHC contains recognition alleles as this would also require the carrier to perceive the phenotype using products of the allele itself and this has been discredited due to the fact that mating preferences can be reversed due to cross fostering, implying that although the MHC is used for recognition, the act of recognition is not determined by the MHC. Another example would be Bateson’s (2000) Japanese quail but the reasons for discrimination has been found to be due to phenotypic character as unrelated birds that look the same are more preferable to first cousins who differ. These experiments discredit the existence of recognition allele, so there must be another mechanism for kin recognition.
Phenotype Matching
Kin recognition through phenotype matching involves the learning and assessment of phenotypes of particular animals. As described before it is based on template reference, created by reference to self or by another closely related conspecific. An example of template creation with reference to self, the so called ‘armpit effect’ (Dawkins 1982) can be seen in the honeybees. The queens mate with up to 17 different drones, leading to mixed paternity. Isolated workers can use their own phenotype as a kin recognition template, and may be able to discriminate between full and half sisters. Whether this is used in relation to nepotism is controversial (see Visscher 1986). The likelihood of a self-matching mechanism in nepotunistic contexts is under content. Alexander (1990, 1991) argued against the evolution of self-matching because of the alleles behind would be genetic outlaws as described before. Dawkins however argues that it is not just one allele that gets passed down to the next generation but the entire genome and so it is beneficial to all genes. There is extreme difficulty in distinguishing recognition alleles from matching with phenotype as no empirical data has been produced to suggest the distinction. Therefore although preferential treatment is seen we cannot yet attribute it to either of the above mechanisms.
Associative Learning
This is a widespread mechanism for discriminating kin form non-kin, and is probably effective in any situation where there is a reliable correlation between genetic relatedness and association. Imprinting of offspring onto parents or vice versa, where recognition results from a period of association, is an obvious manifestation of this mechanism, for example Lorenz’s geese displayed imprinting behaviour on Lorenz himself. Another example are female great tit chicks that learn their father’s songs and, as adults, females avoid pairing with males whose songs match this template (McGregor & Krebs 1982). Although associative learning can be problematic because during the period of association the animal learns the cues of its kin but it can also learn the cues of a strangers kin and mistake it for kin, Lorenz’s geese feature again but a better example is brood parasitism by cuckoos. Normally first time parents learn what their eggs look like, however if their nest contains a cuckoo’s egg then they are forever doomed to recognise the foreign egg as their own in that and subsequent nests.
Spatially Based Recognition
This is probably the simplest mechanism of kin recognition and one for which there is good evidence among birds. When relatives are predictively distributed in space, i.e. the offspring are located at the nest site, location can offer an accurate and consistent cue to genetic relatedness. For example, breeders providing parental care may use the simple rule “feed anything in my nest”. Because of its simplicity however it is also the most open to exploitation.
Conclusions
What we have seen here is a host of mechanisms for kin recognition. I personally believe that kin recognition exists, due to the huge amount of observational evidence available. However what the real problem ethologists face is one that seems to echo in all other aspects of their field, that is that because behaviour is such a complex, difficult and subjective thing to analyse there is not enough empirical data to support many of these theories, leaving the floor open to criticism by others due to opinions based on what the animal perceives, something that we cannot accurately know. The mechanisms described here act on many different levels, from simple behaviours to complex gene orientated ones. It will take time to gather the evidence to arrange these mechanisms and the most important thing to point out is that these mechanisms are not mutually exclusive, behaviours are so complex and based on a range of environmental and genetic factors it would be foolish to assume that the whole process of kin recognition is attributable to one mechanism alone.
Bibliography
Bateson (1982) Nature 295, 236
Fletcher & Michener (1987) Kin Recognition in Animals
Grafen (1990) Animal Behaviour 39, 42-54
Brown & Ekland (1994) Kin recognition and MHC - a review
Komdeur & Hatchwell (1999) Kin recognition: function and n in Ecology & Evolution, 1999, Vol. 14, No.6, pp.237-24114, 2
Sherman et al. (1997) In Krebs, J.R. & Davies, N.B. Behavioural ecology
