Melatonin in the seasonal response of the aphid Acyrthosiphon pisum

Aphids display life cycles largely determined by the photoperiod. During the warm long-day seasons, most aphid species reproduce by viviparous parthenogenesis. The shortening of the photoperiod in autumn induces a switch to sexual reproduction. Males and sexual females mate to produce overwintering resistant eggs. In addition to this full life cycle (holocycle), there are anholocyclic lineages that do not respond to changes in photoperiod and reproduce continuously by parthenogenesis. The molecular or hormonal events that trigger the seasonal response (i.e., induction of the sexual phenotypes) are still unknown. Although circadian synthesis of melatonin is known to play a key role in vertebrate photoperiodism, the involvement of the circadian clock and/or of the hormone melatonin in insect seasonal responses is not so well established. Here we show that melatonin levels in the aphid Acyrthosiphon pisum are significantly higher in holocyclic aphids reared under short days than under long days, while no differences were found between anholocyclic aphids under the same conditions. We also found that melatonin is localized in the aphid suboesophageal ganglion (SOG) and in the thoracic ganglionic mass (TGM). In analogy to vertebrates, insect-type arylalkylamine N-acetyltransferases (i-AANATs) are thought to play a key role in melatonin synthesis. We measured the expression of four i-AANAT genes identified in A. pisum and localized two of them in situ in the insect central nervous systems (CNS). Levels of expression of these genes were compatible with the quantities of melatonin observed. Moreover, like melatonin, expression of these genes was found in the SOG and the TGM.