Studies of both vertebrates and invertebrates have shown that memory is composed of different phases that differ in duration and time of onset. Two distinct forms of memory—labile, short-term memory and robust, long-term memory—were defined in original studies of memory. These two forms appear to be highly conserved from invertebrates to vertebrates [1
]. Long-term memory is typically defined as memory that is resistant to anaesthesia and that depends on new protein synthesis. However, genetic dissection of the memory phases has revealed that, at least in Drosophila
] and some parasitoid species [3
], these two criteria may define two different forms of memory. In Drosophila
, anaesthesia-resistant memory (ARM) and long-term memory (LTM) can be independently formed using Pavlovian aversive olfactory conditioning [4
]. ARM forms when repeated conditioning sessions immediately follow one another; LTM forms when repeated conditioning sessions are separated by a time interval. These two memory phases differ in their durability and by whether they depend on new protein synthesis. LTM lasts longer than ARM and its formation requires de novo protein synthesis [3
]. These findings raise questions about the pattern of genetic correlations between different memory phases, and about how these correlations could influence cognitive evolution.
Previous studies have focused on the functional differences between these long-lasting memory phases [2
]. Only recently has research begun to address how they are specifically adapted to the needs of an animal behaving in its natural environment and how they respond to natural selection [3
]. The capacity for learning and memory is known to trade-off with other fitness-related traits [12
]. At the functional level, a recent study established that the formation of ARM gates the formation of LTM via specific oscillations of two pairs of dopaminergic neurons that project to the mushroom body [16
]. This study confirmed that the spacing between conditioning events determines whether ARM or LRM will form [17
] and that there is a functional trade-off between these consolidated memory phases. Less is known about the evolutionary significance of this functional trade-off and whether evolution acts on ARM and LTM independently.
Although the existence of evolutionary trade-offs is widely assumed, it can be difficult to demonstrate them. Several approaches have been used, including comparative studies on different taxa, phenotypic manipulation, analysis of genetic correlations and selection experiments; however, most of these have interpretive limitations [18
]. In the present study, we directly addressed how a functional trade-off may affect the evolutionary relationship between ARM and LTM. We artificially selected populations of Drosophila
either for improved ARM or LTM, and determined the extent to which selection on one memory phase affects the formation of the other memory phase. Unlike ARM, LTM formation is known to be costly and linked to decreased longevity in conditioned flies [20
]. Knowing that learning ability trades off with other traits [13
], we quantified longevity, fecundity, stress resistance and development time to demonstrate the ultimate constitutive cost of improved LTM.