across a very broad taxonomic range animals frequently respond differentially to close kin , even if those kin were previously unfamiliar . logically , this differentiation between individuals according to kinship requires well - defined mechanisms to allow recognition . and whereas animals may learn the cues of familiar individual kin during rearing , recognition of unfamiliar kin must really be recognition of genetic similarity - either to self or to other known kin .
a challenge in this area lies in discovering the cues that animals use for genetic recognition of kin , and the genetic encoding of such cues . in many vertebrates , odors are key to the recognition process , and have been widely implicated as cues that allow genetic kin recognition in many species of fish , reptiles and mammals ( figure 1 ) . however , vertebrate scents are generally complex , and there have been few attempts to identify the specific scent components used in kin recognition or their genetic basis .
in work published recently in bmc evolutionary biology , boulet and colleagues   have advanced this field by demonstrating a significant correlation between genetic similarity ( estimated from 11 - 14 microsatellite loci ) in a captive population of ring - tailed lemurs ( lemur catta ) and similarity of volatile chemicals in their genital gland secretions , as assessed by gas - chromatography mass - spectrometry .
the genetic similarity of two individuals is thus manifest in the odor profile ( sometimes referred to as an ' odortype ' ) . even more intriguing , although the genital glands of the two sexes are anatomically distinct ( scrotal glands in the male , labial glands in the female ) , this covariance between genetic and chemical similarity is evident even between individuals of the opposite sex . while some components are expressed only by animals of one sex , more than half ( about 170 )
were expressed by individuals of both sexes . to provide a simple estimate of chemical distance between a pair of individuals , boulet et al . used the relative abundance of each of these shared compounds to calculate the euclidean distance between the pair ( derived from the pythagorean theorem , this sums the pairwise difference ,  , in abundance of all 170 compounds , such that chemical distance = sqrt(1 + 2 + 3 + .... 170 ) .
while there was a broad spread of chemical distances between male - female dyads that had intermediate genetic distance , dyads with low genetic similarity had low chemical similarity whereas those with a high genetic similarity had a higher chemical similarity .
this relationship is consistent with the hypothesis that odors from genital secretions can be used to assess genetic relatedness , and maybe close kinship .
of particular interest , these relationships were significant both within and between the sexes during the breeding season , but were much weaker or nonsignificant during the non - breeding season .
odortype may be particularly important during the competitive breeding season to prevent inbreeding and/or to direct nepotistic behavior towards more closely related individuals .
however , this study is still only a first step in establishing whether such odor signals could offer a reliable means of recognizing kinship among ring - tailed lemurs and the genetic basis of the cues used .
if lemurs used a measure of chemical distance based on all volatile compounds that are shared within or between the sexes , it would only be of very limited value in assessing kinship because of the considerable range in that measure between individuals of intermediate genetic relatedness .
although very closely related animals have similar odortypes , so do many individuals that are much less closely related .
if odortype were used to avoid inbreeding , for example , the consequence would be exclusion as mates of many individuals that are not closely related , reducing choice without gaining any genetic benefit .
it is likely , therefore , that animals use more specific markers within the odortype to distinguish close relatives reliably ( figure 2 ) .
chemical distance between pairs of animals based on all volatile compounds in a scent correlates with genetic distance ( a ) , but variance will be high for any particular genetic distance because some compounds are likely to be strongly influenced by non - genetic factors such as current hormone levels and bacterial flora .
instead , selective assessment of specific semiochemicals within the scent that correlate strongly with genotype ( b ) will provide a much more reliable assessment of kinship .
there has been surprisingly little progress in establishing the genetic and molecular markers used to recognize kin through scents in vertebrates . in part
, this may be due to the molecular complexity of vertebrate scents , which are the product not only of an individual 's genes but also of hormonal and metabolic status , diet and microflora .
for the past 30 years , the focus on genetic mechanisms underlying vertebrate kin recognition through odors has been on the major histocompatibility complex ( mhc ) , which is often held to be the major genetic component apparently determining an individual 's scent .
inbred laboratory mice have been a key model organism for manipulating mhc genes on a constant genetic background as proof that animals can detect mhc type through scent . as mhc
is so highly polymorphic in natural populations , those that share the same mhc type ( and mhc - based scent ) are very likely to be closely related - mhc odors could be used as a marker of genetic relatedness . yet , despite the precise genetic control offered by laboratory rodent strains , chemical analyses of volatile profiles have found correlations of some volatile components with mhc type but have not yet discovered consistent differences in compounds that are regulated by mhc type [ 3 - 6 ] . in reality ,
complex interactions are found with genetic background , microflora and diet , all of which alter the odor profile [ 3,5 - 7 ] .
this plasticity of mhc - derived odortype creates a conundrum . to be useful in natural populations , kin markers must be stable and readily recognized against the variable genetic and environmental background of normal outbred animals .
our own studies of wild - derived mice with normal genetic variation in semi - natural populations provided clear evidence that wild mice do not use mhc to avoid inbreeding .
in fact , mice showed a very strong avoidance of inbreeding with those sharing another very highly polymorphic marker in mouse scent , the major urinary proteins ( mups ) , which have a strong influence on an individual 's scent profile regardless of other genetic and non - genetic variation .
sharing of a single highly polymorphic marker , like mup or mhc type , can provide a reliable indicator of relatedness because only close relatives are likely to inherit both of the same alleles at a particular locus ( or both of the same haplotypes in the case of clusters of closely linked genes like mup or mhc ) .
however , this type of mechanism can only be partially effective for kin recognition . for any single locus , the number of alleles shared between two relatives is a matter of chance ; even very close relatives such as full siblings are as likely to share no alleles as they are to share both alleles at a particular locus .
modeling alternative genetic mechanisms that could be used to discriminate full sibs from unrelated animals   reveals that reliance on a single genetic locus will either fail to identify many relatives ( if the requirement is that both alleles are shared ) or will mistake many unrelated animals as sibs ( if sharing of any allele is used ) .
notwithstanding the theory , house mice do use sharing of mup type , encoded by a single tightly linked cluster of genes , to avoid inbreeding .
this may be specific to house mice - there are insufficient data to assess whether such simple recognition systems are widespread .
an alternative model is that instead of directly comparing the similarity of scents to self , imprinting on maternal scent encoded by several independent loci is employed to provide reliable recognition of all siblings and maternal half - sibs , because all offspring share with their mother one allele at every locus .
laboratory cross - fostering studies in which newborn mouse pups were fostered onto a mother of different mhc type to their own have suggested that animals might imprint on the genotype of their mother and subsequently avoid ' inbreeding ' with those sharing the foster mother 's genotype rather than avoiding mates that match their own mhc type .
however , maternal imprinting does not require recognition of the mother 's genotype for kin recognition ; instead animals must be able to recognize the separate haplotypes carried by the mother when these are combined with other unknown haplotypes .
this recognition task is likely to be considerably more difficult given the complex effects that mhc type has on odors , particularly as the odors of mhc heterozygotes are not an additive combination of the two homozygous profiles .
a key test would be whether mice ( or other animals ) can recognize the separate mhc haplotypes carried by a heterozygous animal when combined with other mhc haplotypes ( for example , animals imprinted on the mhchaplotype must be able to recognize mhcor mhc ) ; they also need to be able to do this on the randomly assorting genetic background of outbred animals .
a recent study using inbred laboratory mice found that animals recognized non - genetic similarities in offspring from the same mother compared to those from another genetically identical female due to their shared maternal ( in utero and postnatal ) environment .
the approach of relating genetic similarity to the global volatile profile of scent glands   is a step towards the systems biology of complex behaviors .
indeed , the application of global profiling methodologies to scents could be said to introduce the concept ( but preferably not the term ! ) of ' semiomics ' . as with many studies of this nature ,
the analyte mixtures are complex , and a major challenge is in unbundling the important semiochemicals from the entire volatile profile - although boulet and colleagues   refer to a ' semiochemical profile ' , it is likely that many of the constituent compounds will be ' silent ' in kin recognition .
an attractive way forward is to use the combined datasets to identify those chemicals that show the greatest correlation with relatedness , focusing on differences in relatedness that can be discriminated behaviorally .
the candidates can be examined in ' kin - shifting ' experiments such that when they are spiked into a distant sample , they elicit a response more ' akin ' to a close relative .
indeed , similar experiments could be conducted using humans to establish the extent to which we too can discriminate our own kin based on genetically determined scents .
the development of these ideas was supported by research grants from bbsrc ( s19816 , bbc603897 ) and nerc ( neg018650 ) .
 a recent study in bmc evolutionary biology has shown that genetically similar individual ring - tailed lemurs are also more similar in their scent composition , suggesting a possible mechanism of kin recognition . 
 theoretical and experimental studies reveal challenges ahead in achieving a true systems - level understanding of this process and its outcomes.see research article http://www.biomedcentral.com/1471-2148/9/281 . 
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Gene-odor covariance
Genetic and molecular mechanisms used to assess kinship
The way forward
Acknowledgements