Natural variation in learning and memory dynamics studied by artificial selection on learning rate in parasitic wasps

Berg, Michael van den; Duivenvoorde, Loes P. M.; Tribuhl, S.V.; Bukovinszky, Tibor; Vet, Louise E. M.; Dicke, Marcel; Smid, Hans M.

doi:10.1016/j.anbehav.2010.11.002

Cited by 41 publications

(54 citation statements)

References 41 publications

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“…Interestingly, this finding correlates well with reports that ARM and LTM are mutually exclusive in flies; the formation of ARM prevents LTM consolidation and vice versa [41]. The dependency of LTM and ARM was also investigated by bidirectional artificial selection over nine generations in C. glomerata [42]. As explained above, this species forms LTM for plant odors after a single oviposition experience when oviposition on P. brassicae is used as a reward.…”

Section: Evolutionary Aspects Of Prepared Learningsupporting

confidence: 72%

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

Smid

Vet

2016

Current Opinion in Insect Science

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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

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Section: Evolutionary Aspects Of Prepared Learningsupporting

confidence: 72%

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

Smid

Vet

2016

Current Opinion in Insect Science

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“…For instance, Smid et al [12] hypothesized that C. glomerata does not form ARM after a single learning trial, but only LTM. An artificial selection experiment with this parasitoid species, aimed to decrease learning rate, resulted in a low learning rate line in less than 10 generations [13]. Wasps of this low learning-rate line formed normal LTM after spaced conditioning, but formed only ASM after single trial conditioning, instead of LTM, which is formed in unselected wasps.…”

Section: (D) Learning and Memory Dynamics In Parasitoid Waspsmentioning

confidence: 99%

“…Recent research unveiled remarkable natural variation in learning rate and in the dynamics of memory formation between closely related parasitoid wasp species [9][10][11][12][13]. These studies suggested that this variation reflects adaptations to species-specific ecological constraints.…”

Section: Introductionmentioning

confidence: 99%

“…These types of memory can be disrupted with anaesthesia, such as a brief exposure to a cold shock in insects, and are known as forms of anaesthesia-sensitive memory (ASM) [36,37]. ASM lasts, depending on the investigated species, for several minutes up to a few hours [13,36,37]. During the ASM phase, the formation of long-lasting memory types starts, a process called memory consolidation [34].…”

Section: Variation In Learning Rate and Memory Dynamicsmentioning

confidence: 99%

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Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience

et al. 2010

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Although the neural and genetic pathways underlying learning and memory formation seem strikingly similar among species of distant animal phyla, several more subtle inter-and intraspecific differences become evident from studies on model organisms. The true significance of such variation can only be understood when integrating this with information on the ecological relevance. Here, we argue that parasitoid wasps provide an excellent opportunity for multi-disciplinary studies that integrate ultimate and proximate approaches. These insects display interspecific variation in learning rate and memory dynamics that reflects natural variation in a daunting foraging task that largely determines their fitness: finding the inconspicuous hosts to which they will assign their offspring to develop. We review bioassays used for oviposition learning, the ecological factors that are considered to underlie the observed differences in learning rate and memory dynamics, and the opportunities for convergence of ecology and neuroscience that are offered by using parasitoid wasps as model species. We advocate that variation in learning and memory traits has evolved to suit an insect's lifestyle within its ecological niche.

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“…Strain-specific differences in the ability to learn and remember are not unique to Lymnaea as they have been observed for many years across phyla (Ings et al, 2009;Healy et al, 2009;van den Berg et al, 2011). Why some Lymnaea strains are smarter than others is not clear.…”

Section: Introductionmentioning

confidence: 99%

Juveniles ofLymnaeasmart snails do not perseverate and have the capacity to form LTM

Shymansky

Protheroe

Hughes

et al. 2016

Journal of Experimental Biology

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Previously, it was concluded that the nervous systems of juvenile snails were not capable of mediating long-term memory (LTM). However, exposure and training of those juvenile snails in the presence of a predator cue significantly altered their ability to learn and form LTM. In addition, there are some strains of Lymnaea which have been identified as 'smart'. These snails form LTM significantly better than the lab-bred strain. Here, we show that juveniles of two smart snail strains not only are capable of associative learning but also have the capacity to form LTM following a single 0.5 h training session. We also show that freshly collected 'wild' 'average' juveniles are also not able to form LTM. Thus, the smart snail phenotype in these strains is expressed in juveniles.

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Natural variation in learning and memory dynamics studied by artificial selection on learning rate in parasitic wasps

Cited by 41 publications

References 41 publications

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

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

Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience

Juveniles ofLymnaeasmart snails do not perseverate and have the capacity to form LTM

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