Drosophila hemocytes, like those of mammals, are given rise from two distinctive phases
during both the embryonic and larval hematopoiesis. Embryonically derived hemocytes,
mostly composed of macrophage-like plasmatocytes, are largely identified by genetic
markers. However, the cellular diversity and distinct functions of possible subpopulations
within plasmatocytes have not been explored in Drosophila larvae. Here, we show that
larval plasmatocytes exhibit differential expressions of Hemolectin (Hml) and Peroxidasin
(Pxn) during development. Moreover, removal of plasmatocytes by overexpressing pro-apoptotic
genes, hid and reaper in Hml-positive plasmatocytes, feeding high sucrose diet, or
wasp infestation results in increased circulating hemocytes that are Hml-negative.
Interestingly these Hml-negative plasmatocytes retain Pxn expression, and animals
expressing Hml-negative and Pxn-positive subtype largely attenuate growth and abrogate
metabolism. Furthermore, elevated levels of a cytokine, unpaired 3, are detected when
Hml-positive hemocytes are ablated, which in turn activates JAK/STAT activity in several
tissues including the fat body. Finally, we observed that insulin signaling is inhibited
in this background, which can be recovered by concurrent loss of upd3. Overall, this
study highlights heterogeneity in Drosophila plasmatocytes and a functional plasticity
of each subtype, which reaffirms extension of their role beyond immunity into metabolic
regulation for cooperatively maintaining internal homeostatic balance.