The complexity of learning, memory and neural processes in an evolutionary ecological context

Abstract

The ability to learn and form memories is widespread among insects, but there exists considerable natural variation between species and populations in these traits. Variation manifests itself in the way information is stored in different memory forms. This review focuses on ecological factors such as environmental information, spatial aspects of foraging behavior and resource distribution that drive the evolution of this natural variation and discusses the role of different genes and neural networks. We conclude that at the level of individual, population or species, insect learning and memory cannot be described as good or bad. Rather, we argue that insects evolve tailor-made learning and memory types; they gate learned information into memories with high or low persistence. This way, they are prepared to learn and form memory to optimally deal with the specific ecologies of their foraging environments. Highlights:• Environmental variation, spatial foraging behavior and the distribution of resources are factors that drive the evolution of differences in prepared learning • Considerable heritable variation exists in numerous learning and memory traits • Insects have evolved tailor-made memory types, adapted to the specific ecology of their foraging environment • The foraging gene is an important gene underlying natural variation in learning and memory • Dopaminergic signaling may drive the adaptive gating of information into different memory formsThe use of previous experience to optimize behavior in an adaptive manner is obviously of great benefit to all animals, including insects [1,2]. However, this does not mean that insects should learn and remember information from all possible experiences they encounter. Studies on diverse insect species have revealed the daunting complexity of different forms of memory each with different stabilities, including short-, mid-, anesthesia resistant-and long term memory (STM, MTM, ARM and LTM), e.g. [3][4][5][6]. In Fig. 1 we provide a basic description of these memory forms and their abbreviations. Why does learning not always result in the formation of LTM? To ensure the reliability of learned information, most animals require multiple, spaced experiences before information is stored as LTM. Nevertheless, some animals form LTM after a single experience suggesting that they may have evolved to rely on the Accepted in Current Opinion in Insect Science, CC-BY-NC-ND

Multiple genetic loci affect place learning and memory performance in Drosophila melanogaster

“…There is a growing appreciation for the complexity of learning and memory and the need to study these traits in realistic settings 4,116 . Recently there has been a shift from investigating single genes to identifying the sets of neurons and circuits involved in learning and memory 54,87,117,118 .…”

Flexible memory controls sperm competition responses in maleDrosophila melanogaster

“…Similar examples of ecologically relevant memory are referred to as "Tailor made memory", defined as the properties and temporal dynamics of acquisition, consolidation and retrieval of memory after learning specific for an ecological context [37,38]. For example, parasitoid wasps (Cotesia glomerata) differ in the spatial memory pathway (ARM or ASM)…”

Multiple genetic loci affect place learning and memory performance in Drosophila melanogaster

“…4,116 Recently there has been a shift from investigating single genes to identifying the sets of neurons and circuits involved in learning and memory. 4,116 Recently there has been a shift from investigating single genes to identifying the sets of neurons and circuits involved in learning and memory.…”

“…There is a growing appreciation for the complexity of learning and memory and the need to study these traits in realistic settings. 4,116 Recently there has been a shift from investigating single genes to identifying the sets of neurons and circuits involved in learning and memory. 54,87,117,118 In addition, mapping studies in humans are beginning to uncover the natural genetic variants influencing learning and memory.…”