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Neofunctionalization of an ancient domain allows parasites to avoid intraspecific competition by manipulating host behaviour.

ABSTRACT: Intraspecific competition is a major force in mediating population dynamics, fuelling adaptation, and potentially leading to evolutionary diversification. Among the evolutionary arms races between parasites, one of the most fundamental and intriguing behavioural adaptations and counter-adaptations are superparasitism and superparasitism avoidance. However, the underlying mechanisms and ecological contexts of these phenomena remain underexplored. Here, we apply the Drosophila parasite Leptopilina boulardi as a study system and find that this solitary endoparasitic wasp provokes a host escape response for superparasitism avoidance. We combine multi-omics and in vivo functional studies to characterize a small set of RhoGAP domain-containing genes that mediate the parasite's manipulation of host escape behaviour by inducing reactive oxygen species in the host central nervous system. We further uncover an evolutionary scenario in which neofunctionalization and specialization gave rise to the novel role of RhoGAP domain in avoiding superparasitism, with an ancestral origin prior to the divergence between Leptopilina specialist and generalist species. Our study suggests that superparasitism avoidance is adaptive for a parasite and adds to our understanding of how the molecular manipulation of host behaviour has evolved in this system.

SUBMITTER: Chen J

PROVIDER: S-EPMC8446075 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Neofunctionalization of an ancient domain allows parasites to avoid intraspecific competition by manipulating host behaviour.

Chen Jiani J Fang Gangqi G Pang Lan L Sheng Yifeng Y Zhang Qichao Q Zhou Yuenan Y Zhou Sicong S Lu Yueqi Y Liu Zhiguo Z Zhang Yixiang Y Li Guiyun G Shi Min M Chen Xuexin X Zhan Shuai S Huang Jianhua J

Nature communications 20210916 1

Intraspecific competition is a major force in mediating population dynamics, fuelling adaptation, and potentially leading to evolutionary diversification. Among the evolutionary arms races between parasites, one of the most fundamental and intriguing behavioural adaptations and counter-adaptations are superparasitism and superparasitism avoidance. However, the underlying mechanisms and ecological contexts of these phenomena remain underexplored. Here, we apply the Drosophila parasite Leptopilina ...[more]

PMID: 34531391

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Project description:Urbanization has reshaped ecosystems and changed natural processes, driving an intense transformation of biomes, biotic community composition and diversity. Despite the growing interest in studying urban ecology over the last decades, the consequences of these changes on species occupying these ecosystems are not yet fully understood. Trophic generalism and tolerance to human disturbance have been proposed as two key traits in the colonization of urban environments. However, most studies focused on species' average traits, paying less attention to the potential role of inter-individual variability. Here, we examined diet specialization in urban and rural breeding pairs, as well as its relationship with individual behaviour and intraspecific competition, using the burrowing owl as a study model. Our results show that both urban and rural breeding pairs behaved as trophic specialists. The diet of burrowing owl breeding pairs followed a gradient from coleopteran- to micromammal-dominated, which is related to individual behaviour (bolder individuals consuming more coleopterans than shyer ones). Besides, pairs distant from others showed a more diverse diet than those experiencing higher levels of intraspecific competition. Models fitted separately for each habitat showed that the proportion of micromammals in the diet of urban breeding pairs was related to their behavior, while the diet of rural pairs was not affected by individual behavior but by intraspecific competition. However, despite the strong selection of tame and more explorative individuals in urban environments and the higher density they reach in this habitat type, they did not differ in their degree of diet specialization from rural conspecifics. Although it would be necessary to evaluate prey availability on a small scale, our results suggest that burrowing owl breeding pairs behave as specialists, despite the generalist character of the species, and that this specialization is not affected by the occupation of urban environments but to individual behaviour and intraspecific competition.

Dataset Information

Neofunctionalization of an ancient domain allows parasites to avoid intraspecific competition by manipulating host behaviour.

Publications

Neofunctionalization of an ancient domain allows parasites to avoid intraspecific competition by manipulating host behaviour.

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