Genomic imprinting and evolution of insect societies

Matsuura, Kenji

doi:10.1002/1438-390x.12026

Cited by 33 publications

(25 citation statements)

References 83 publications

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“…Matsuura et al (2018) modelled a genomic imprinting mediated caste determination system in the termite Reticulitermes speratus and found this better explained the influence of parental phenotype on offspring than a purely genetic model. Given the diversity of genes found here showing both maternal and paternal expression bias we believe, along with Matsuura (2019), that further experimental investigation into the role of genomic imprinting in caste determination in social insects is needed.…”

Section: Discussionmentioning

confidence: 91%

Parent of origin gene expression in the bumblebee, Bombus terrestris, supports Haig’s kinship theory for the evolution of genomic imprinting

Marshall

Zweden

Geystelen

et al. 2020

Preprint

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Genomic imprinting is the differential expression of alleles in diploid individuals, with the expression being dependent upon the sex of the parent from which it was inherited. Haig’s kinship theory hypothesizes that genomic imprinting is due to an evolutionary conflict of interest between alleles from the mother and father. In social insects, it has been suggested that genomic imprinting should be widespread. One recent study identified parent-of-origin expression in honeybees and found evidence supporting the kinship theory. However, little is known about genomic imprinting in insects and multiple theoretical predictions must be tested to avoid single-study confirmation bias. We, therefore, tested for parent-of-origin expression in a primitively eusocial bee. We found equal numbers of maternally and paternally biased expressed alleles. The most highly biased alleles were maternally expressed, offering support for the kinship theory. We also found low conservation of potentially imprinted genes with the honeybee, suggesting rapid evolution of genomic imprinting in Hymenoptera.Impact summaryGenomic imprinting is the differential expression of alleles in diploid individuals, with the expression being dependent upon the sex of the parent from which it was inherited. Genomic imprinting is an evolutionary paradox. Natural selection is expected to favour expression of both alleles in order to protect against recessive mutations that render a gene ineffective. What then is the benefit of silencing one copy of a gene, making the organism functionally haploid at that locus? Several explanations for the evolution of genomic imprinting have been proposed. Haig’s kinship theory is the most developed and best supported.Haig’s theory is based on the fact that maternally (matrigene) and paternally (patrigene) inherited genes in the same organism can have different interests. For example, in a species with multiple paternity, a patrigene has a lower probability of being present in siblings that are progeny of the same mother than does a matrigene. As a result, a patrigene will be selected to value the survival of the organism it is in more highly, compared to the survival of siblings. This is not the case for a matrigene.Kinship theory is central to our evolutionary understanding of imprinting effects in human health and plant breeding. Despite this, it still lacks a robust, independent test. Colonies of social bees consist of diploid females (queens and workers) and haploid males created from unfertilised eggs. This along with their social structures allows for novel predictions of Haig’s theory.In this paper, we find parent of origin allele specific expression in the important pollinator, the buff-tailed bumblebee. We also find, as predicted by Haig’s theory, a balanced number of genes showing matrigenic or patrigenic bias with the most extreme bias been found in matrigenically biased genes.

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Section: Discussionmentioning

confidence: 91%

Parent of origin gene expression in the bumblebee, Bombus terrestris, supports Haig’s kinship theory for the evolution of genomic imprinting

Marshall

Zweden

Geystelen

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Matsuura et al (2018) modeled a genomic imprinting mediated caste determination system in the termite R. speratus and found this better explained the influence of parental phenotype on offspring than a purely genetic model. Given the diversity of genes found here showing both maternal and paternal expression bias we believe, along with Matsuura (2019), that further experimental investigation into the role of genomic imprinting in caste determination in social insects is needed.…”

Section: Discussionmentioning

confidence: 91%

Parent of origin gene expression in the bumblebee,Bombus terrestris, supports Haig's kinship theory for the evolution of genomic imprinting

et al. 2020

View full text Add to dashboard Cite

Genomic imprinting is the differential expression alleles in diploid individuals, with the expression being dependent on the sex of the parent from which it was inherited. Haig's kinship theory hypothesizes that genomic imprinting is due to an evolutionary conflict of interest between alleles from the mother and father. In social insects, it has been suggested that genomic imprinting should be widespread. One recent study identified parent-of-origin expression in honey bees and found evidence supporting the kinship theory. However, little is known about genomic imprinting in insects and multiple theoretical predictions must be tested to avoid single-study confirmation bias. We, therefore, tested for parent-of-origin expression in a primitively eusocial bee. We found equal numbers of maternally and paternally biased expressed genes. The most highly biased genes were maternally expressed, offering support for the kinship theory. We also found low conservation of potentially imprinted genes with the honey bee, suggesting rapid evolution of genomic imprinting in Hymenoptera.

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“…In this issue, we provide a special feature “Epigenetic inheritance and a paradigm shift in evolutionary ecology (organized by Kenji Matsuura)” including three papers (Iwasa, ; Matsuura, ; Miryeganeh & Saze, ). This special feature is a spin‐off from the symposium “The era of genome imprinting: epigenetic inheritance and a paradigm shift in evolutionary ecology” at the annual meeting of the Society of Population Ecology in 2017.…”

Section: Special Featuresmentioning

confidence: 99%

Population Ecology 2020 editorial

Noda

2020

Population Ecology

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Genomic imprinting and evolution of insect societies

Cited by 33 publications

References 83 publications

Parent of origin gene expression in the bumblebee, Bombus terrestris, supports Haig’s kinship theory for the evolution of genomic imprinting

Parent of origin gene expression in the bumblebee, Bombus terrestris, supports Haig’s kinship theory for the evolution of genomic imprinting

Parent of origin gene expression in the bumblebee,Bombus terrestris, supports Haig's kinship theory for the evolution of genomic imprinting

Population Ecology 2020 editorial

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