A Genomic Imprinting Model of Termite Caste Determination: Not Genetic but Epigenetic Inheritance Influences Offspring Caste Fate

Matsuura, Kenji; Mizumoto, Nobuaki; Kobayashi, Keiko; Nozaki, Tomonari; Fujita, Tadahide; Yashiro, Toshihisa; Fuchikawa, Taro; Mitaka, Yuki; Vargo, Edward L.

doi:10.1086/697238

Cited by 52 publications

(75 citation statements)

References 42 publications

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“…In some species this is genetically determined (Mott et al, 2015), however there is growing evidence epigenetic factors may play a role in caste determination in some species (Lyko et al, 2010; Bonasio et al, 2012; Marshall et al, 2019). 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: 99%

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: 99%

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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“…Rotten woods containing their colonies were transported to the laboratory, and the extracted termites were immediately used for ploidy analysis. Each colony contained multiple queens, which were nymph‐derived neotenics, and one adult king, as reported in this species (Matsuura et al, ).…”

Section: Methodsmentioning

confidence: 99%

Evolutionary relationship of fat body endoreduplication and queen fecundity in termites

Nozaki

Matsuura

2019

Ecology and Evolution

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Endoreduplication or nuclear genome replication without cell division is widely observed in the metabolically active tissues of plants and animals. The fat body cells of adult female insects produce abundant yolk proteins and become polyploid, which is assumed to accelerate egg production. Recently, it was reported that in termites, endopolyploidy in the fat body occurs only in queens but not in the other females; however, the relationship between the fecundity and ploidy level in the fat body remains unclear. Termite queens exhibit a huge variation in their egg‐producing capacity among different species; queens in the species with a foraging lifestyle, in which workers leave the nest to forage outside, are much more fecund than those in the species living in a single piece of wood. In this study, we conducted ploidy analyses on three foragings and three wood‐dwelling termites via flow cytometry. In all the species, the fat body of queens contained significantly more polyploid cells than that of other nonreproductive females, considering their body size effect. However, the male fat body, which is not involved in yolk production, did not show consistency in polyploid cell numbers among the species studied. Moreover, highly fecund queens in foraging termites exhibit higher levels of endopolyploidy in their fat body than those with less fecundity in wood‐dwelling termites. These results suggest that endopolyploidy in the fat body of termite queens can boost their egg production, and the level of endopolyploidy in their fat body is linked to their fecundity. Our study provides a novel insight into the evolutionary relationship between endoreduplication and caste specialization in social insects.

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“…Social insects exhibit sometimes extreme morphological and behavioral differences within a single colony, known as castes. The mechanisms by which species develop differences between castes are diverse; some species use only environmental cues, whereas others rely only on inherited changes, with many species falling somewhere in between these two extremes (Matsuura et al 2018). For example, some ant species from the Pogonomyrmex genus have purely genetic caste determination (Mott et al 2015).…”

Section: Impact Summarymentioning

confidence: 99%

Methylation and gene expression differences between reproductive and sterile bumblebee workers

2019

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Phenotypic plasticity is the production of multiple phenotypes from a single genome and is notably observed in social insects. Multiple epigenetic mechanisms have been associated with social insect plasticity, with DNA methylation being explored to the greatest extent. DNA methylation is thought to play a role in caste determination in Apis mellifera, and other social insects, but there is limited knowledge on its role in other bee species. In this study, we analyzed whole genome bisulfite sequencing and RNA‐seq data sets from head tissue of reproductive and sterile castes of the eusocial bumblebee Bombus terrestris. We found that genome‐wide methylation in B. terrestris is similar to other holometabolous insects and does not differ between reproductive castes. We did, however, find differentially methylated genes between castes, which are enriched for multiple biological processes including reproduction. However, we found no relationship between differential methylation and differential gene expression or differential exon usage between castes. Our results also indicate high intercolony variation in methylation. These findings suggest that methylation is associated with caste differences but may serve an alternate function, other than direct caste determination in this species. This study provides the first insights into the nature of a bumblebee caste‐specific methylome as well as its interaction with gene expression and caste‐specific alternative splicing, providing greater understanding of the role of methylation in phenotypic plasticity within social bee species. Future experimental work is needed to determine the function of methylation and other epigenetic mechanisms in insects.

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A Genomic Imprinting Model of Termite Caste Determination: Not Genetic but Epigenetic Inheritance Influences Offspring Caste Fate

Cited by 52 publications

References 42 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

Evolutionary relationship of fat body endoreduplication and queen fecundity in termites

Methylation and gene expression differences between reproductive and sterile bumblebee workers

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