Segmentation of the subcuticular fat body in Apis mellifera females with different reproductive potentials

Abstract

Evolution has created different castes of females in eusocial haplodiploids. The difference between them lies in their functions and vulnerability but above all in their reproductive potentials. Honeybee queens are highly fertile. On the other hand, the workers are facultatively sterile. However, rebel workers, i.e. workers that develop in a queenless colony, reproduce more often than normal workers. As a result, the fat body of these bees, which apart from acting as the energy reserve, is also the site of numerous metabolic processes, had to specialize in different functions perfected over millions of years of eusocial evolution. Assuming that the variety of functions manifests itself in the pleomorphic structure of the fat body cells, we predicted that also different parts of the fat body, e.g. from different segments of the abdomen, contain different sets of cells. Such differences could be expected between queens, rebels and normal workers, i.e. females with dramatically different reproductive potentials. We confirmed all these expectations. Although all bees had the same types of cells, their proportion and segmental character corresponded with the caste reproductive potential and physiological characteristics shaped in the evolutionary process. The females with an increased reproductive potential were characterized by the presence of oenocytes in the third tergite and high concentrations of compounds responsible for energy reserves, like glucose, glycogen and triglycerides. Queens had very large trophocytes, especially in the third tergite. Only in workers did we observe intercellular spaces in all the segments of the fat body, as well as high protein concentrations—especially in the sternite. As expected, the rebels combined many features of the queens and normal workers, what with other findings can help understand the ways that led to the origin of different castes in females of eusocial Hymenoptera.

Humoral and Cellular Defense Mechanisms in Rebel Workers of Apis mellifera

“…We also confirmed that oenocytes located in the fat body in the third tergite did not occur in normal worker bees, only in the females with an increased reproductive potential [4]. Previous research by Strachecka et al [4] showed that the fat body is segmental. The present paper analyses further parameters (e.g., the numbers and sizes of oenocytes in specific segments/localizations of this tissue).…”

“…Moreover, as suggested by Koubová et al [ 59 ], this decreased fat body cell size is associated with a lower rate of DNA synthesis and lower telomerase activity. These changes result in the release of energy reserves contained in the cells [ 4 , 5 ]. We also confirmed that oenocytes located in the fat body in the third tergite did not occur in normal worker bees, only in the females with an increased reproductive potential [ 4 ].…”

“…These concentrate on the outer surface of the dorsal vessel and, mainly, in specific foci in the heart; they are typically connected to abdominal segments [ 3 ]. As a result, the fat body has a segmental character and functions as a multifunctional system made up of many organs/segments where each segment works separately and they all contribute to a common metabolism [ 4 ]. This segmental nature of the two cooperating tissues/cell types (hemocytes in hemolymph and fat body cells) is crucial in the cascading processes related to immunity and aging of honeybee workers.…”

“…Ecdysteroids act on vitellogenin (Vg; a zinc-binding glycolipoprotein) uptake from the hemolymph [ 8 ], therefore its levels are reduced with age [ 9 ]. Vg is synthesized in the trophocytes [ 10 ] (most likely in the third tergite of the fat body) and is immediately directed to the appropriate tissues by the circulatory system [ 4 ]. The changes of these hormones as a result of aging induce hemocyte death [ 6 ].…”

“…Thus, workers developing at larval stage in a queenless colony become relatively selfish individuals with higher reproductive potential than those that develop in a colony with a queen. These workers called rebel workers are characterized not only by their increased reproductive potential but also other altered anatomical features (e.g., less developed HGs, larger mandibular glands; [ 20 ]), shortened preimaginal development [ 22 ], prolonged life [ 23 ], different foraging preferences [ 24 ], tendency to drift to other colonies [ 25 ], increased sucrose sensitivity [ 26 ], energy reserves and protein concentrations in fat body [ 4 ], and increased learning ability [ 27 ].…”