Laser-based selective killing of a manipulative parasite reveals partial reversibility of phenotypic alterations in its intermediate host

Various parasites alter their intermediate hostʼs phenotype in ways that increase parasite transmission to definitive hosts. To what extent infected intermediate hosts can recover from such “manipulation” is poorly documented, thus limiting our understanding of its proximate and ultimate causes. Her...

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Main Authors: Marie-Jeanne Perrot-Minnot, Frank Cézilly, Olivier Musset
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:Current Research in Parasitology and Vector-Borne Diseases
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Online Access:http://www.sciencedirect.com/science/article/pii/S2667114X24000529
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author Marie-Jeanne Perrot-Minnot
Frank Cézilly
Olivier Musset
author_facet Marie-Jeanne Perrot-Minnot
Frank Cézilly
Olivier Musset
author_sort Marie-Jeanne Perrot-Minnot
collection DOAJ
description Various parasites alter their intermediate hostʼs phenotype in ways that increase parasite transmission to definitive hosts. To what extent infected intermediate hosts can recover from such “manipulation” is poorly documented, thus limiting our understanding of its proximate and ultimate causes. Here, we address the reversibility of several phenotypic alterations induced by the acanthocephalan Polymorphus minutus, a trophically-transmitted bird parasite, in its amphipod intermediate host. Using a recently developed laser-based technology, we selectively killed parasite larvae inside the body cavity of Gammarus fossarum, while preserving host viability. Following behavioral tests, parasite death was confirmed using DNA integrity assays. Alterations of geotaxis, locomotor activity and resting metabolic rate in infected gammarids remained unchanged one month after parasiteʼs death. In contrast, elevated brain lactate concentration and hemolymph total phenoloxidase activity of treated gammarids hosting a dead cystacanth returned to control (uninfected) levels. Interestingly, melanotic encapsulation response to dead cystacanths was rare up to two months after treatment, with only 5.6% of cystacanths being fully or partially melanized, thus suggesting long-lasting protection from the acellular outer envelope. Irreversible behavioral but reversible physiological alterations appear to be a cost-effective strategy of host manipulation, and point to a putative role of epigenetic alterations in parasite manipulation.
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series Current Research in Parasitology and Vector-Borne Diseases
spelling doaj-art-e5858fe4f8c34e26aed2a366adfa8b9f2025-08-20T02:07:31ZengElsevierCurrent Research in Parasitology and Vector-Borne Diseases2667-114X2024-01-01610022110.1016/j.crpvbd.2024.100221Laser-based selective killing of a manipulative parasite reveals partial reversibility of phenotypic alterations in its intermediate hostMarie-Jeanne Perrot-Minnot0Frank Cézilly1Olivier Musset2Biogéosciences, UMR 6282 CNRS Université de Bourgogne, 6 Boulevard Gabriel, 21000, Dijon, France; Corresponding author.Université de Bourgogne, 6 Boulevard Gabriel, 21000, Dijon, FranceLaboratoire Interdisciplinaire Carnot de Bourgogne, UMR 6303 CNRS, Université Bourgogne Franche-Comté, 9 Avenue Alain Savary, 21078, Dijon, FranceVarious parasites alter their intermediate hostʼs phenotype in ways that increase parasite transmission to definitive hosts. To what extent infected intermediate hosts can recover from such “manipulation” is poorly documented, thus limiting our understanding of its proximate and ultimate causes. Here, we address the reversibility of several phenotypic alterations induced by the acanthocephalan Polymorphus minutus, a trophically-transmitted bird parasite, in its amphipod intermediate host. Using a recently developed laser-based technology, we selectively killed parasite larvae inside the body cavity of Gammarus fossarum, while preserving host viability. Following behavioral tests, parasite death was confirmed using DNA integrity assays. Alterations of geotaxis, locomotor activity and resting metabolic rate in infected gammarids remained unchanged one month after parasiteʼs death. In contrast, elevated brain lactate concentration and hemolymph total phenoloxidase activity of treated gammarids hosting a dead cystacanth returned to control (uninfected) levels. Interestingly, melanotic encapsulation response to dead cystacanths was rare up to two months after treatment, with only 5.6% of cystacanths being fully or partially melanized, thus suggesting long-lasting protection from the acellular outer envelope. Irreversible behavioral but reversible physiological alterations appear to be a cost-effective strategy of host manipulation, and point to a putative role of epigenetic alterations in parasite manipulation.http://www.sciencedirect.com/science/article/pii/S2667114X24000529Complex life-cycleCostsCrustaceaImmunityRecovery
spellingShingle Marie-Jeanne Perrot-Minnot
Frank Cézilly
Olivier Musset
Laser-based selective killing of a manipulative parasite reveals partial reversibility of phenotypic alterations in its intermediate host
Current Research in Parasitology and Vector-Borne Diseases
Complex life-cycle
Costs
Crustacea
Immunity
Recovery
title Laser-based selective killing of a manipulative parasite reveals partial reversibility of phenotypic alterations in its intermediate host
title_full Laser-based selective killing of a manipulative parasite reveals partial reversibility of phenotypic alterations in its intermediate host
title_fullStr Laser-based selective killing of a manipulative parasite reveals partial reversibility of phenotypic alterations in its intermediate host
title_full_unstemmed Laser-based selective killing of a manipulative parasite reveals partial reversibility of phenotypic alterations in its intermediate host
title_short Laser-based selective killing of a manipulative parasite reveals partial reversibility of phenotypic alterations in its intermediate host
title_sort laser based selective killing of a manipulative parasite reveals partial reversibility of phenotypic alterations in its intermediate host
topic Complex life-cycle
Costs
Crustacea
Immunity
Recovery
url http://www.sciencedirect.com/science/article/pii/S2667114X24000529
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AT frankcezilly laserbasedselectivekillingofamanipulativeparasiterevealspartialreversibilityofphenotypicalterationsinitsintermediatehost
AT oliviermusset laserbasedselectivekillingofamanipulativeparasiterevealspartialreversibilityofphenotypicalterationsinitsintermediatehost