Endopolyploidy Changes with Age-Related Polyethism in the Honey Bee, Apis mellifera

Abstract

Honey bees (Apis mellifera) exhibit age polyethism, whereby female workers assume increasingly complex colony tasks as they age. While changes in DNA methylation accompany age polyethism, other DNA modifications accompanying age polyethism are less known. Changes in endopolyploidy (DNA amplification in the absence of cell division) with increased larval age are typical in many insect cells and are essential in adults for creating larger cells, more copies of essential loci, or greater storage capacity in secretory cells. However, changes in endopolyploidy with increased adult worker age and polyethism are unstudied. In this study, we examined endopolyploidy in honey bee workers ranging in age from newly emerged up to 55 days old. We found a nonsignificant increase in ploidy levels with age (P < 0.1) in the most highly endopolyploid secretory cells, the Malpighian tubules. All other cell types decreased ploidy levels with age. Endopolyploidy decreased the least amount (nonsignificant) in neural (brain) cells and the stinger (P < 0.1). There was a significant reduction of endopolyploidy with age in leg (P < 0.05) and thoracic (P < 0.001) muscles. Ploidy in thoracic muscle dropped from an average of 0.5 rounds of replication in newly emerged workers to essentially no rounds of replication (0.125) in the oldest workers. Ploidy reduction in flight muscle cells is likely due to the production of G1 (2C) nuclei by amitotic division in the multinucleate striated flight muscles that are essential to foragers, the oldest workers. We suggest that ploidy is constrained by the shape, size and makeup of the multinucleate striated muscle cells. Furthermore, the presence of multiple 2C nuclei might be optimal for cell function, while higher ploidy levels might be a dead-end strategy of some aging adult tissues, likely used to increase cell size and storage capacity in secretory cells.

Comparative physiology of Malpighian tubules: form and function

“…9 In Dinoponera australis, organs related to digestion and excretion present the much higher levels of endopolyploidy when compared with other organs such as brain and muscle. 31 This was also observed in Apis mellifera by Rangel et al, 32 although no statistically significant differences were observed. In addition to differences with regard to other organs, in Apis mellifera, MT showed higher ploidy values in an age-dependent manner.…”

Evolutionary relationship of fat body endoreduplication and queen fecundity in termites

“…Because age-related endopolyploidy has been reported in worker honeybees (Rangel et al, 2015), it is probably reasonable to expect that the fat body of long-lived individuals will have more endopolyploid cells than others in termites. In fact, queens in eusocial insects including termites exhibit long lives; their lifespan is more than 10-fold longer than that of workers and soldiers (Jemielity et al, 2005;Keller, 1998;Thorne, Breisch, & Haverty, 2002).…”

“…Endoreduplication is often attributed to increasing cellular size, metabolism, and gene expression owing to the increasing availability of DNA templates for transcription (Bourdon et al, ; Claycomb, Benasutti, Bosco, Fenger, & Orr‐Weaver, ; Edgar et al, ; Galitski, Saldanha, Styles, Lander, & Fink, ; Nagl, ). In social hymenopterans, several studies have shown the intriguing linkage between caste specialization and endopolyploidy (Rangel, Strauss, Seedorf, Hjelmen, & Johnston, ; Scholes, Suarez, & Paige, ; Scholes, Suarez, Smith, Johnston, & Paige, ). Scholes et al () investigated the degree of polyploidy within and among castes of four ant species with worker polymorphism and observed variation in ploidy levels among workers with different body sizes.…”

Flying High—Muscle-Specific Underreplication in Drosophila

“…Also to be determined are environmental effects on the parameters. Flight performance in honeybees is associated with a reduction in polyploidy with age [19]. Further, while it is known that endocyclic cells are large and metabolically active, have multiple sites of origin firing, and variable levels of transcription [10,14,15], it remains to be seen whether underreplication is a mechanism to meet the metabolic demands of flight with a minimal increase in nuclear size.…”

“…The thorax is comprised of a variety of different tissues, including cuticle, gut, tergal depressor of the trochanter (TDT) muscle, and the direct and indirect flight muscle [18]. Of these, only the gut is expected to have any polyploid nuclei, according to data collected from a bee and an ant [19,20]. Yet, gut nuclei are expected to be rare relative to the nuclei from other thoracic tissues, as the thorax is filled by muscle [21].…”