Endopolyploidy changes with age-related polyethism in the honey bee, Apis mellifera.

Juliana Rangel,Kim Strauss,J Spencer Johnston,Carl E Hjelmen,Kaileah Seedorf,Stephen C Pratt

doi:10.1371/journal.pone.0122208

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.

Highlights

Endopolyploidy is the cellular process of nuclear DNA amplification in the absence of typical mitotic cell division during the endocycle [1,2]
Ploidy levels were determined for 84 samples from 9 age classes (0- to 55-day-old honey bee workers) for five tissue types: brain, thoracic muscle, leg muscle, Malpighian tubules, and stinger with 1 to 3 replicates depending on the number of workers recovered for each age class (Table 1)
We report the first estimates of endopolyploidy levels for tissues in newly emerged honey bee workers and provide the first evidence that endopolyploidy levels change significantly as workers age

Summary

Introduction

Endopolyploidy is the cellular process of nuclear DNA amplification in the absence of typical mitotic cell division during the endocycle [1,2]. Endoreduplication is commonly observed in specialized plant and animal tissues, including a number of tissues in arthropods [3,4,5,6,7,8,9]. Age-related changes in endopolyploidy are often of interest because of their association with tumorogenesis [10]. The extent to which endopolyploidy levels change as a natural cell process related to aging is largely unstudied [11].

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Results

Conclusion