The kinship theory of genomic imprinting
Encyclopedia
The kinship theory of genomic imprinting is an evolution
ary account of the origin and evolution of imprinted genes. When two allele
s at a diploid locus differ in their optimal gene expression
level depending on their parent of origin, the theory predicts the evolutionary outcome to be imprinted gene expression. The development of the theory is due mostly to David Haig
and is an outgrowth and extension of the theories of kin selection
and parent-offspring conflict
.
kinship theory is a gene-centered
extension of Trivers'
theory of parent-offspring conflict
. Where parent-offspring conflict theory sees the genotype of the offspring as a single agent with a cohesive interest in the negotiation between mother and child for resources, the kinship theory of genomic imprinting sees each allele
at a diploid locus in the offspring as having its own separate interest in that negotiation. In Trivers' original formulation of parent-offspring conflict, genes in the offspring are predicted to demand more resources from the mother than the mother is selected to provide. In Haig’s extension of parent-offspring conflict, a prediction is made for each of the two alleles at a diploid locus for their optimal level of demand on maternal resources.
Because the relatedness of the two alleles at a locus in an offspring to other siblings will differ when the mother is multiply mated, so too will the inclusive fitness
of each allele differ. Therefore what maximizes inclusive fitness for one allele may not be what maximizes inclusive fitness for the other. This form of conflicting selection pressure is called parental antagonism and is necessary for the evolution of imprinted genetic expression. It is not a conflict between the two parents - as the name might suggest - but is more carefully described as a conflict within individuals between the two alleles at a diploid locus that depends on their parent of origin. The fundamental breakthrough in Haig's theory is the identification of this additional intra-individual conflict over resource allocation from the mother. That is, while the parent and the offspring are in conflict (parent-offspring conflict), so too can the two alleles at a locus within the offspring be in conflict (parental antagonism).
When a genetic locus experiences parentally antagonistic selection pressure and alleles are capable of adopting conditional expression
strategies depending on their parent of origin context, Haig
shows that all-or-none expression is an evolutionarily stable strategy
(ESS). Further, the parent of origin context that favors a higher level of expression of the gene
is predicted to be expressed at equilibrium and the parent of origin context that favors a lower level of expression is predicted to silence itself at equilibrium.
Because the relatedness of a genetic locus to siblings and half siblings is predicted to be higher on the maternal side than the paternal side of an offspring in utero, the kinship theory predicts that genes whose expression increase demands on the mother will be paternally expressed and genes that inhibit demand on mothers will be maternally expressed.
Haig's kinship theory extends beyond the maternal-fetal relationship, though. Under female-biased dispersal, the relatedness for paternally derived genes in a social kin group will be higher than maternally derived genes. As such, genes that promote cooperative
or altruistic behaviors are expected to be paternally expressed while genes that promote selfish behavior will be expressed when maternally derived.
Evolution
Evolution is any change across successive generations in the heritable characteristics of biological populations. Evolutionary processes give rise to diversity at every level of biological organisation, including species, individual organisms and molecules such as DNA and proteins.Life on Earth...
ary account of the origin and evolution of imprinted genes. When two allele
Allele
An allele is one of two or more forms of a gene or a genetic locus . "Allel" is an abbreviation of allelomorph. Sometimes, different alleles can result in different observable phenotypic traits, such as different pigmentation...
s at a diploid locus differ in their optimal gene expression
Gene expression
Gene expression is the process by which information from a gene is used in the synthesis of a functional gene product. These products are often proteins, but in non-protein coding genes such as ribosomal RNA , transfer RNA or small nuclear RNA genes, the product is a functional RNA...
level depending on their parent of origin, the theory predicts the evolutionary outcome to be imprinted gene expression. The development of the theory is due mostly to David Haig
David Haig (biologist)
David Haig, is an Australian evolutionary biologist and geneticist, professor in Harvard Department of Organismic and Evolutionary Biology. He is interested in intragenomic conflict, genomic imprinting and parent-offspring conflict, and wrote the book Genomic Imprinting and Kinship...
and is an outgrowth and extension of the theories of kin selection
Kin selection
Kin selection refers to apparent strategies in evolution that favor the reproductive success of an organism's relatives, even at a cost to the organism's own survival and reproduction. Charles Darwin was the first to discuss the concept of group/kin selection...
and parent-offspring conflict
Parent-offspring conflict
Parent–offspring conflict is a term coined in 1974 by Robert Trivers. It is used to signify the evolutionary conflict arising from differences in optimal parental investment to an offspring from the standpoint of the parent and the offspring...
.
Parent-offspring conflict and parental antagonism
Haig’sDavid Haig (biologist)
David Haig, is an Australian evolutionary biologist and geneticist, professor in Harvard Department of Organismic and Evolutionary Biology. He is interested in intragenomic conflict, genomic imprinting and parent-offspring conflict, and wrote the book Genomic Imprinting and Kinship...
kinship theory is a gene-centered
Gene-centered view of evolution
The gene-centered view of evolution, gene selection theory or selfish gene theory holds that evolution occurs through the differential survival of competing genes, increasing the frequency of those alleles whose phenotypic effects successfully promote their own propagation, with gene defined as...
extension of Trivers'
Robert Trivers
Robert L. Trivers is an American evolutionary biologist and sociobiologist and Professor of Anthropology and Biological Sciences at Rutgers University. Trivers is most noted for proposing the theories of reciprocal altruism , parental investment , facultative sex ratio determination , and...
theory of parent-offspring conflict
Parent-offspring conflict
Parent–offspring conflict is a term coined in 1974 by Robert Trivers. It is used to signify the evolutionary conflict arising from differences in optimal parental investment to an offspring from the standpoint of the parent and the offspring...
. Where parent-offspring conflict theory sees the genotype of the offspring as a single agent with a cohesive interest in the negotiation between mother and child for resources, the kinship theory of genomic imprinting sees each allele
Allele
An allele is one of two or more forms of a gene or a genetic locus . "Allel" is an abbreviation of allelomorph. Sometimes, different alleles can result in different observable phenotypic traits, such as different pigmentation...
at a diploid locus in the offspring as having its own separate interest in that negotiation. In Trivers' original formulation of parent-offspring conflict, genes in the offspring are predicted to demand more resources from the mother than the mother is selected to provide. In Haig’s extension of parent-offspring conflict, a prediction is made for each of the two alleles at a diploid locus for their optimal level of demand on maternal resources.
Because the relatedness of the two alleles at a locus in an offspring to other siblings will differ when the mother is multiply mated, so too will the inclusive fitness
Inclusive fitness
In evolutionary biology and evolutionary psychology, the inclusive fitness of an organism is the sum of its classical fitness and the number of equivalents of its own offspring it can add to the population by supporting others...
of each allele differ. Therefore what maximizes inclusive fitness for one allele may not be what maximizes inclusive fitness for the other. This form of conflicting selection pressure is called parental antagonism and is necessary for the evolution of imprinted genetic expression. It is not a conflict between the two parents - as the name might suggest - but is more carefully described as a conflict within individuals between the two alleles at a diploid locus that depends on their parent of origin. The fundamental breakthrough in Haig's theory is the identification of this additional intra-individual conflict over resource allocation from the mother. That is, while the parent and the offspring are in conflict (parent-offspring conflict), so too can the two alleles at a locus within the offspring be in conflict (parental antagonism).
When a genetic locus experiences parentally antagonistic selection pressure and alleles are capable of adopting conditional expression
Gene expression
Gene expression is the process by which information from a gene is used in the synthesis of a functional gene product. These products are often proteins, but in non-protein coding genes such as ribosomal RNA , transfer RNA or small nuclear RNA genes, the product is a functional RNA...
strategies depending on their parent of origin context, Haig
David Haig (biologist)
David Haig, is an Australian evolutionary biologist and geneticist, professor in Harvard Department of Organismic and Evolutionary Biology. He is interested in intragenomic conflict, genomic imprinting and parent-offspring conflict, and wrote the book Genomic Imprinting and Kinship...
shows that all-or-none expression is an evolutionarily stable strategy
Evolutionarily stable strategy
In game theory and behavioural ecology, an evolutionarily stable strategy , which is sometimes also called an evolutionary stable strategy, is a strategy which, if adopted by a population of players, cannot be invaded by any alternative strategy that is initially rare. An ESS is an equilibrium...
(ESS). Further, the parent of origin context that favors a higher level of expression of the gene
Gene
A gene is a molecular unit of heredity of a living organism. It is a name given to some stretches of DNA and RNA that code for a type of protein or for an RNA chain that has a function in the organism. Living beings depend on genes, as they specify all proteins and functional RNA chains...
is predicted to be expressed at equilibrium and the parent of origin context that favors a lower level of expression is predicted to silence itself at equilibrium.
Because the relatedness of a genetic locus to siblings and half siblings is predicted to be higher on the maternal side than the paternal side of an offspring in utero, the kinship theory predicts that genes whose expression increase demands on the mother will be paternally expressed and genes that inhibit demand on mothers will be maternally expressed.
Haig's kinship theory extends beyond the maternal-fetal relationship, though. Under female-biased dispersal, the relatedness for paternally derived genes in a social kin group will be higher than maternally derived genes. As such, genes that promote cooperative
Cooperation
Cooperation or co-operation is the process of working or acting together. In its simplest form it involves things working in harmony, side by side, while in its more complicated forms, it can involve something as complex as the inner workings of a human being or even the social patterns of a...
or altruistic behaviors are expected to be paternally expressed while genes that promote selfish behavior will be expressed when maternally derived.