Evolutionary relationship of fat body endoreduplication and queen fecundity in termites

Abstract

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.

Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite

“…We observed a first upregulation of the vg gene. As recently suggested for other termite species 39 , polyploidy in the fat body of M. natalensis queens can boost their egg production by increasing protein synthesis, notably VG. In Drosophila, seven out of eight insulin-like peptides (DILPs) are mainly produced in the brain insulin-producing cells except for DILP6, which is produced in the fat body.…”

Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite

“…Concomitantly with the growth of colonies and coinciding with their development of physogastry, the imaginal fat body of virgin queens (QT0) with its canonical fat storage function becomes replaced by a royal fat body (QT4), which is highly oriented towards specific protein synthesis and secretion 40 . A comparative analysis of different termite species recently suggested that endopolyploidy (or nuclear genome replication without cell division) permits the rate of vitellogenin synthesis to increase 41 . Developmental changes in oogenesis might rely on endopolyploidy and we therefore determine the percentages of the nuclei count at each ploidy level (2C, 4C, and 8C) in the fat bodies of adult queens in five stages.…”

Long-lived termite kings and queens activate telomerase in somatic organs

“…Although adult fat body cells of termite queens (and sometimes also kings) undergo endoreduplications [ 53 ], these are expected to be infrequent in Pr. simplex , belonging to termites with low fecundity and low adult abdominal growth [ 54 ]. In other words, in both the honeybee and termites, the telomerase activation in long-lived reproductives appears as independent of the actual rate of nuclear divisions, at least in some of the studied organs.…”