Termite queens have disproportionately more <scp>DNA</scp> in their fat body cells: reproductive division of labor and endoreduplication

Nozaki, Tomonari; Matsuura, Kenji

doi:10.1111/ens.12156

Cited by 16 publications

(28 citation statements)

References 22 publications

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“…With utmost care and attention to avoid contamination by other tissues such as Malpighian tubules and tracheoles, we dissected the fat body from the abdomen of insects. In addition, we used the heads of all analyzed individuals as diploid tissue (Nozaki & Matsuura, ). Tissue for flow cytometric analysis was processed with a Cycletest PLUS DNA Reagent Kit (Becton Dickinson).…”

Section: Methodsmentioning

confidence: 99%

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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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Section: Methodsmentioning

confidence: 99%

“…Tissue for flow cytometric analysis was processed with a Cycletest PLUS DNA Reagent Kit (Becton Dickinson). All procedures were performed according to Nozaki and Matsuura (). Stained nuclei were analyzed for DNA‐PI fluorescence using an Accuri C6 Flow Cytometer (Becton Dickinson) at an excitation wavelength of 488 nm.…”

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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“…Any parent-specific gene expression of the genes involved in secondary queen differentiation [e.g. queen pheromone receptor, juvenile hormone, hexamerin, fat body endoreduplication (Nozaki and Matsuura, 2016) or vitellogenin synthesis] can explain the parthenogens' developmental priority to be secondary queens. For simplicity, let us assume maternal imprinting (silencing) of the queen pheromone receptor gene (Fig.…”

Section: Genomic Imprinting Model For Aqsmentioning

confidence: 99%

Evolution of the asexual queen succession system and its underlying mechanisms in termites

Matsuura

2017

Journal of Experimental Biology

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One major advantage of sexual reproduction over asexual reproduction is its promotion of genetic variation, although it reduces the genetic contribution to offspring. Queens of social insects double their contribution to the gene pool, while overuse of asexual reproduction may reduce the ability of the colony to adapt to environmental stress because of the loss of genetic diversity. Recent studies have revealed that queens of some termite species can solve this tradeoff by using parthenogenesis to produce the next generation of queens and sexual reproduction to produce other colony members. This reproductive system, known as asexual queen succession (AQS), has been identified in the subterranean termites Reticulitermes speratus, Reticulitermes virginicus and Reticulitermes lucifugus and in the Neotropical higher termites Embiratermes neotenicus and Cavitermes tuberosus. The studies presented here have uncovered the unusual modes of reproduction in termites and have aimed to identify their underlying mechanisms. The study of AQS, the mixed use of sexual and asexual reproduction, is of fundamental importance as it may provide a key to solve the evolutionary paradox of sex.

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“…Vitellogenic oocytes only occur after a reproductive molt, associated with increased Vg expression in female reproductives in many species (Saiki et al, 2015;reviewed in Korb, 2015). Strikingly, a doubling of DNA content through endoploidy in the fat body (i.e., the main tissue for vitellogenesis) was found in queens, but not other castes, in R. speratus (Nozaki and Matsuura, 2016). This may be an adaption to enable the high fecundity of termite queens, although similar duplications also exist in females of some solitary insects (e.g., Dittmann et al, 1989).…”

Section: Frontiers In Ecology and Evolution | Wwwfrontiersinorgmentioning

confidence: 90%

Genes Underlying Reproductive Division of Labor in Termites, with Comparisons to Social Hymenoptera

Korb

2016

Front. Ecol. Evol.

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All social insects are characterized by a reproductive division of labor. Within a colony only a few individuals reproduce (queens and in termites, also a king) while the large majority (workers and soldiers) forgo reproduction, at least temporarily. The evolution of such reproductive altruism can ultimately be explained by inclusive fitness theory. Here, I will review the proximate genetic mechanisms underlying this altruism in termites. As social cockroaches they evolved eusociality independently from the social Hymenoptera, which makes them interesting test cases to look for common underlying mechanisms of eusociality and lineage specific idiosyncrasies. First, I will provide a summary of the genes and their function that have been identified to underlie reproductive division of labor-so called "queen genes,"-in the drywood termite Cryptotermes secundus, an emerging model to study termite social evolution. Second, I outline how widespread these queen genes are across the termite phylogeny, using also evidence from recent genome analyses. I will provide hypotheses about the evolutionary origin of these queen genes, aiming to link proximate mechanisms with ultimate functions. Finally, I will draw comparisons to social Hymenoptera to indicate potential common underpinnings that warrant further testing.

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Termite queens have disproportionately more DNA in their fat body cells: reproductive division of labor and endoreduplication

Cited by 16 publications

References 22 publications

Evolutionary relationship of fat body endoreduplication and queen fecundity in termites

Evolutionary relationship of fat body endoreduplication and queen fecundity in termites

Evolution of the asexual queen succession system and its underlying mechanisms in termites

Genes Underlying Reproductive Division of Labor in Termites, with Comparisons to Social Hymenoptera

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