Defensive insect symbiont leads to cascading extinctions and community collapse

Sanders, Dirk; Kehoe, Rachel; Veen, F. J. Frank van; McLean, Ailsa H. C.; Godfray, H. Charles J.; Dicke, Marcel; Gols, Rieta; Frago, Enric

doi:10.1111/ele.12616

Cited by 56 publications

(62 citation statements)

References 41 publications

(99 reference statements)

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“…Their role on communities and ecological network structure through effects on both trophic and non-trophic interactions is now emerging Rothacher et al, 2016;Sanders et al, 2016). They have, until recently, been studied only under laboratory conditions, and have been largely ignored by field ecologists.…”

Section: Role Of Facultative Endosymbiontsmentioning

confidence: 99%

Mechanisms structuring host–parasitoid networks in a global warming context: a review

Thierry

Hrček

Lewis

2019

Ecological Entomology

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1. In natural communities, multiple host and parasitoid species are linked to form complex networks of trophic and non-trophic interactions. Understanding how these networks will respond to global warming is of wide relevance for agriculture and conservation.2. This study synthesises the emerging evidence surrounding host-parasitoid networks in the context of global warming. The suite of direct and indirect interaction types within host-parasitoid networks is summarised, as well as their sensitivity to temperature changes. The study also compiles and reviews studies investigating the responses of whole host-parasitoid networks to increasing temperatures or proxy variables. The findings reveal there is limited evidence overall for the prediction that parasitism will be reduced under global warming: approximately equal numbers of studies show elevated and reduced parasitism.3. Increasingly, endosymbiotic bacteria are recognised as influential mediators of host-parasitoid interactions. These endosymbionts can change how individual species respond to global warming, and their effects can cascade to affect whole host-parasitoid networks. The evidence that symbiotic bacteria are likely to affect the response of host-parasitoid networks to global warming is reviewed. Symbionts can protect hosts from their parasitoids or influence thermal tolerance of their host species. Furthermore, the symbionts themselves can be impacted by global warming.4. Finally, the study considers the most promising avenues for future research into the mechanisms structuring host-parasitoid networks in the context of global warming. Alongside the increasing availability of modern molecular methods to document the structure of real, species-rich host-parasitoid networks, the study highlights the utility of manipulative experiments and mathematical models.

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Section: Role Of Facultative Endosymbiontsmentioning

confidence: 99%

Mechanisms structuring host–parasitoid networks in a global warming context: a review

Thierry

Hrček

Lewis

2019

Ecological Entomology

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“…This has been especially well studied in insects, whose bacterial symbionts can influence traits ranging from mate and diet choice (4,5) to susceptibility to natural enemies (6,7). Bacterial symbionts can also differ in the fidelity of their associations with their insect hosts.…”

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confidence: 99%

Gut Microbiota Colonization and Transmission in the Burying Beetle Nicrophorus vespilloides throughout Development

Wang

Rozen

2017

Appl Environ Microbiol

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Carrion beetles in the genus Nicrophorus rear their offspring on decomposing carcasses where larvae are exposed to a diverse community of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as prehatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as full care). Here, we partition the roles of prehatch and posthatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (full care, prehatch care only, and no care), we found that larvae receiving full care are predominantly colonized by bacteria resident in the maternal gut while larvae receiving no care are colonized with bacteria from the carcass. More importantly, larvae receiving only prehatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo an aposymbiotic stage, after which they are recolonized at eclosion with bacteria similar to those found on the molted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of prehatch parental care for symbiont transmission in Nicrophorus vespilloides and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization.IMPORTANCE Here, we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetle Nicrophorus vespilloides. This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses, where they are exposed to high densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation but are recolonized apparently from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further suggest that competitive interactions mediate the bacterial composition of Nicrophorus larvae together with or apart from the influence of beetle immunity, suggesting that the bacterial communities of these insects may be highly coevolved with those of their host species.KEYWORDS Nicrophorus, parental care, symbiosis, microbiota, transmission A nimals are colonized by a diverse community of bacterial symbionts that play crucial roles in their ecology and evolution (1-3). This has been especially well studied in insects, whose bacterial symbionts can influence traits ranging from mate

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“…These studies have expanded the research focus from simple interactions to complex multi-interaction studies in a community ecology and networks context. Every organism is a community in itself, consisting of a dynamic collection of micro-and macroorganisms (Gilbert et al, 2012) leading to various consequences for multitrophic interactions between plants and their associated community (Frago et al, 2012;Giron et al, 2013Giron et al, , 2017Douglas, 2015;Sugio et al, 2015;Sanders et al, 2016). For example, networks of interacting metabolites within a plant species (e.g., see the previous section) can be linked to networks of interacting arthropods in an entire community to examine how networks at various scales interact in dynamic systems (Richards et al, 2015).…”

Section: Future Promises and Challengesmentioning

confidence: 99%

Promises and challenges in insect–plant interactions

Giron

Dubreuil

Bennett

et al. 2018

Entomologia Exp Applicata

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There is tremendous diversity of interactions between plants and other species. These relationships range from antagonism to mutualism. Interactions of plants with members of their ecological community can lead to a profound metabolic reconfiguration of the plants' physiology. This reconfiguration can favour beneficial organisms and deter antagonists like pathogens or herbivores. Determining the cellular and molecular dialogue between plants, microbes, and insects, and its ecological and evolutionary implications is important for understanding the options for each partner to adopt an adaptive response to its biotic environment. Moving forward, understanding how such ecological interactions are shaped by environmental change and how we potentially mitigate deleterious effects will be increasingly important. The development of integrative multidisciplinary approaches may provide new solutions to the major ecological and societal issues ahead of us. The rapid evolution of technology provides valuable tools and opens up novel ways to test hypotheses that were previously unanswerable, but requires that scientists master these tools, understand potential ethical problems flowing from their implementation, and train new generations of biologists with diverse technical skills. Here, we provide brief perspectives and discuss future promise and challenges for research on insect-plant interactions building on the 16th International Symposium on Insect-Plant interactions (SIP) meeting that was held in Tours, France (2-6 July 2017). Talks, posters, and discussions are distilled into key research areas in insect-plant interactions, highlighting the current state of the field and major challenges, and future directions for both applied and basic research.

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Defensive insect symbiont leads to cascading extinctions and community collapse

Cited by 56 publications

References 41 publications

Mechanisms structuring host–parasitoid networks in a global warming context: a review

Mechanisms structuring host–parasitoid networks in a global warming context: a review

Gut Microbiota Colonization and Transmission in the Burying Beetle Nicrophorus vespilloides throughout Development

Promises and challenges in insect–plant interactions

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