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

Hoedjes, Katja M.; Kruidhof, H.M.; Huigens, Martinus E.; Dicke, Marcel; Vet, Louise E. M.; Smid, Hans M.

doi:10.1098/rspb.2010.2199

Cited by 130 publications

(142 citation statements)

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“…However, either the prey choice of the predator was not frequency-dependent or was not investigated in those studies. Given that parasitoids have evolved variable learning ability depending on ecological requirements (43), host−parasitoid systems attempt to elucidate how their perception, learning rate, and memory dynamics affect their foraging strategies, and host−parasitoid interaction offers a fruitful field for research. Understanding the adaptively flexible behavior of foragers and prey species is critical to understanding the structure of ecological communities, and its effects have become a growing research topic in ecology (44)(45)(46).…”

Section: Discussionmentioning

confidence: 99%

Learning predator promotes coexistence of prey species in host–parasitoid systems

Ishii

Shimada

2012

Proc. Natl. Acad. Sci. U.S.A.

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Ecological theory suggests that frequency-dependent predation, in which more common prey types are disproportionately favored, promotes the coexistence of competing prey species. However, many of the earlier empirical studies that investigated the effect of frequency-dependent predation were short-term and ignored predator-prey dynamics and system persistence. Therefore, we used long-term observation of population dynamics to test how frequency-dependent predation influences the dynamics and coexistence of competing prey species using insect laboratory populations. We established two-host-one-parasitoid populations with two bruchid beetles, Callosobruchus chinensis and C. maculatus, as the hosts and the pteromalid wasp Anisopteromalus calandrae as their common parasitoid. When the parasitoid was absent, C. chinensis was competitively excluded in ∼20 wk. Introducing the parasitoid greatly enhanced the coexistence time to a maximum of 118 wk. In the replicates of long-lasting coexistence, the two host species C. maculatus and C. chinensis exhibited periodic antiphase oscillations. Behavioral experiments showed frequency-dependent predation of A. calandrae that was caused by learning. Females of A. calandrae learned host-related olfactory cues during oviposition and increased their preference for the common host species. Numerical simulations showed that parasitoid learning was the essential mechanism that promoted persistence in this host-parasitoid system. Our study is an empirical demonstration that frequency-dependent predation has an important role in greatly enhancing the coexistence of prey populations, suggesting that predator learning affects predator-prey population dynamics and shapes biological communities in nature.prey switching | flexible foraging | search image O ne of the key challenges of both ecology and evolutionary biology is to understand the mechanisms that maintain biodiversity. In Chesson's terms (1), species coexistence has been explained by two mechanisms: a "stabilizing" mechanism that includes classical niche differentiation, and an "equalizing" mechanism that includes neutral processes (2). Frequency-dependent predation is one of the strong stabilizing mechanisms that are essential for stable species coexistence (1). Since the 1970s, theoretical studies have investigated the effect of frequency-dependent predation on prey coexistence (3-8). Predators that feed on a variety of food items in nature can behaviorally switch to abundant prey types in response to temporal and spatial variations in resource availability. This causes frequency-dependent predation that generally promotes the coexistence of competing prey species because the foraging strategies of predators that switch to more common prey types could prevent rare prey types from being eliminated. However, more recent studies that incorporate prey switching as an optimal diet choice have argued that the effect of switching on the stability of predator-prey systems is quite complex, and sometimes destabilizing, depending on prey c...

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Section: Discussionmentioning

confidence: 99%

Learning predator promotes coexistence of prey species in host–parasitoid systems

Ishii

Shimada

2012

Proc. Natl. Acad. Sci. U.S.A.

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“…Note that a single experience generally results in STM and ARM, whereas LTM requires multiple experiences spaced in time, but some insects already form LTM after a single experience [7]. Repeated experiences, spaced in time, increase the reliability of information and thereby also drive the gating of information towards the right lanes.…”

Section: Figmentioning

confidence: 99%

“…Environmental variation has been proposed as one of the major factors driving the evolution of variation in learning and memory retention [7,[16][17][18]. More variable environments promote short lasting memories, which can be updated continuously.…”

Section: Effects Of Environmental Variation and Spatial Foraging Behamentioning

confidence: 99%

“…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 value of the learned information more readily than other animals, rather their having evolved superior learning and memory abilities [7]. Several factors have been described that play a role in learning and memory including the high energetic costs of memory formation [8,9], the effects of age, physiological state, longevity, stress and the number of lifetime experiences [10][11][12][13][14].…”

Section: Highlightsmentioning

confidence: 99%

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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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“…Some of the smallest insects' entire brains are equivalent in size to only a few human neurons [3]. Nonetheless, these brains contain the full circuitry needed for identification of mates, food and oviposition sites, the motor routines to reach these targets, the control to activate the correct behaviour pattern at the right time, and learning and memory [3,4]. Some functions that in primates are supported by several thousand synchronously active neurons, such as in the dopaminergic reward system [5], can be performed by a single neuron in an insect [6], and miniaturization can be driven further by re-using single neurons as components of multiple circuits [7].…”

Section: Introductionmentioning

confidence: 99%

Information processing in miniature brains

Chittka

Skorupski

2011

Proc. R. Soc. B.

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Since a comprehensive understanding of brain function and evolution in vertebrates is often hobbled by the sheer size of the nervous system, as well as ethical concerns, major research efforts have been made to understand the neural circuitry underpinning behaviour and cognition in invertebrates, and its costs and benefits under natural conditions. This special feature of Proceedings of the Royal Society B contains an idiosyncratic range of current research perspectives on neural underpinnings and adaptive benefits (and costs) of such diverse phenomena as spatial memory, colour vision, attention, spontaneous behaviour initiation, memory dynamics, relational rule learning and sleep, in a range of animals from marine invertebrates with exquisitely simple nervous systems to social insects forming societies with many thousands of individuals working together as a 'superorganism'. This introduction provides context and history to tie the various approaches together, and concludes that there is an urgent need to understand the full neuron-to-neuron circuitry underlying various forms of information processing-not just to explore brain function comprehensively, but also to understand how (and how easily) cognitive capacities might evolve in the face of pertinent selection pressures. In the invertebrates, reaching these goals is becoming increasingly realistic.

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

Cited by 130 publications

References 78 publications

Learning predator promotes coexistence of prey species in host–parasitoid systems

Learning predator promotes coexistence of prey species in host–parasitoid systems

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

Information processing in miniature brains

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