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A temporal trophic shift from primary parasitism to facultative hyperparasitism during interspecific competition between two coevolved scelionid egg parasitoids.

ABSTRACT: Understanding competition between scelionid parasitoids that exploit the same host may provide insight into strategies that allow coexistence on a shared resource. Competition studies typically focus on interactions between native and exotic parasitoids that do not share an evolutionary history; however, coevolved parasitoids may be more likely to demonstrate strategies to avoid or exploit a shared resource. We examined intrinsic and extrinsic competition between Asian Trissolcus japonicus (Ashmead) and T. cultratus (Mayr) (Hymenoptera: Scelionidae) associated with Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) that share an evolutionary history. Interspecific interactions were assessed by providing parasitized egg masses to each species at various intervals post-parasitism, and measuring host acceptance, developmental suitability, and guarding behaviour. Trissolcus japonicus showed high acceptance of parasitized hosts up to 72 h following oviposition by T. cultratus, despite a very poor developmental outcome. In contrast, T. cultratus generally avoided ovipositing in H. halys eggs containing T. japonicus early-instar larvae but did not avoid parasitizing H. halys that contained eggs and third instar larvae. The adaptive value of this behaviour was supported by developmental outcome: T. cultratus outcompeted T. japonicus eggs but not early-instar larvae, and a trophic shift occurred wherein T. cultratus developed as a facultative hyperparasitoid on third instar T. japonicus larvae. Trissolcus japonicus guarded egg masses 8-12× longer and displayed more aggressive interactions than T. cultratus, suggesting T. japonicus is the superior extrinsic competitor. Development as a facultative hyperparasitoid provided a competitive niche for Asian T. cultratus and confirms its instrinsic competitive superiority. This also occurs in a biologically distinct European population of T. cultratus, suggesting that facultative hyperparasitism as a competitive strategy is retained in geographically separated populations that have not coevolved with H. halys or T. japonicus.

SUBMITTER: Haye T

PROVIDER: S-EPMC8717335 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:When a guild of species exploit the same limited resources, interspecific competition induces the exclusion of inferior competitors, in which case, interspecific recognition mechanisms are needed. Here, we address resource partitioning and interspecific competition among three main solitary parasitoid species attacking the same host resource, the aphid Sitobion avenae in wheat fields. Optimal host acceptance models predict that parasitoid species should prefer attacking unparasitized hosts when they are available in order to maximize their fitness, as already parasitized hosts are less valuable for laying eggs, especially for inferior competitors. Therefore, we expected the level of competition (multiparasitism) in the field to increase at low host density. By using a combination of taxonomical (determination) and molecular (PCR-based) approaches, we assessed the species of all parasitoid adults and immature stages within aphid hosts. Our results demonstrate that, early in the season, the multiparasitism rates were low, whereas they were high in the mid-late season, corresponding to an aphid density decrease over time. Moreover, parasitoid species could not have been exploiting host resources randomly and the better competitor, Aphidius ervi, seemed to be foraging preferentially on hosts already parasitized by the inferior competitor A. rhopalosiphi, even when unparasitized hosts were still available. This could be due to differences in their host detection capability, as species with a narrow host range may be better at detecting their hosts in comparison with species with a greater host range, such as A. ervi, with a greater host range within the guild. Our study suggests differences in the host exploitation of two prevalent parasitoid species through the main period of aphid colonization, which still allowed the coexistence of a third inferior competitor (A. rhopalosiphi) within the assemblage, in spite of some negative interactions (multiparasitism) and redundancies.

Project description:The bacterial predator Bdellovibrio bacteriovorus is considered to be obligatorily prey (host)-dependent (H-D), and thus unable to form biofilms. However, spontaneous host-independent (H-I) variants grow axenically and can form robust biofilms. A screen of 350 H-I mutants revealed that single mutations in stator genes fliL or motA were sufficient to generate flagellar motility-defective H-I strains able to adhere to surfaces but unable to develop biofilms. The variants showed large transcriptional shifts in genes related to flagella, prey-invasion, and cyclic-di-GMP (CdG), as well as large changes in CdG cellular concentration relative to the H-D parent. The introduction of the parental fliL allele resulted in a full reversion to the H-D phenotype, but we propose that specific interactions between stator proteins prevented functional complementation by fliL paralogs. In contrast, specific mutations in a pilus-associated protein (Bd0108) mutant background were necessary for biofilm formation, including secretion of extracellular DNA (eDNA), proteins, and polysaccharides matrix components. Remarkably, fliL disruption strongly reduced biofilm development. All H-I variants grew similarly without prey, showed a strain-specific reduction in predatory ability in prey suspensions, but maintained similar high efficiency in prey biofilms. Population-wide allele sequencing suggested additional routes to host independence. Thus, stator and invasion pole-dependent signaling control the H-D and the H-I biofilm-forming phenotypes, with single mutations overriding prey requirements, and enabling shifts from obligate to facultative predation, with potential consequences on community dynamics. Our findings on the facility and variety of changes leading to facultative predation also challenge the concept of Bdellovibrio and like organisms being obligate predators.ImportanceThe ability of bacteria to form biofilms is a central research theme in biology, medicine, and the environment. We show that cultures of the obligate (host-dependent) "solitary" predatory bacterium Bdellovibrio bacteriovorus, which cannot replicate without prey, can use various genetic routes to spontaneously yield host-independent (H-I) variants that grow axenically (as a single species, in the absence of prey) and exhibit various surface attachment phenotypes, including biofilm formation. These routes include single mutations in flagellar stator genes that affect biofilm formation, provoke motor instability and large motility defects, and disrupt cyclic-di-GMP intracellular signaling. H-I strains also exhibit reduced predatory efficiency in suspension but high efficiency in prey biofilms. These changes override the requirements for prey, enabling a shift from obligate to facultative predation, with potential consequences on community dynamics.

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A temporal trophic shift from primary parasitism to facultative hyperparasitism during interspecific competition between two coevolved scelionid egg parasitoids.

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