Trematode infection affects shell shape and size in Bulinus tropicus

Trematodes can increase intraspecific variation in the phenotype of their intermediate snail host. However, the extent of such phenotypic changes remains unclear. We investigated the influence of trematode infection on the shell morphology of Bulinus tropicus, a common host of medically important tr...

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Main Authors: Cyril Hammoud, Annelies Kayenbergh, Julius Tumusiime, Dirk Verschuren, Christian Albrecht, Tine Huyse, Bert Van Bocxlaer
Format: Article
Language:English
Published: Elsevier 2022-08-01
Series:International Journal for Parasitology: Parasites and Wildlife
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213224422000657
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author Cyril Hammoud
Annelies Kayenbergh
Julius Tumusiime
Dirk Verschuren
Christian Albrecht
Tine Huyse
Bert Van Bocxlaer
author_facet Cyril Hammoud
Annelies Kayenbergh
Julius Tumusiime
Dirk Verschuren
Christian Albrecht
Tine Huyse
Bert Van Bocxlaer
author_sort Cyril Hammoud
collection DOAJ
description Trematodes can increase intraspecific variation in the phenotype of their intermediate snail host. However, the extent of such phenotypic changes remains unclear. We investigated the influence of trematode infection on the shell morphology of Bulinus tropicus, a common host of medically important trematodes. We focused on a snail population from crater lake Kasenda (Uganda). We sampled a single homogeneous littoral habitat to minimize the influence of environmental variation on shell phenotype, and barcoded snails to document snail genotypic variation. Among the 257 adult snails analysed, 99 tested positive for trematode infection using rapid-diagnostic PCRs. Subsequently we used high-throughput amplicon sequencing to identify the trematode (co-)infections. For 86 out of the 99 positive samples trematode species delineation could discriminate among combinations of (co-)infection by 11 trematode species. To avoid confounding effects, we focused on four prevalent trematode species. We performed landmark-based geometric morphometrics to characterize shell phenotype and used regressions to examine whether shell size and shape were affected by trematode infection and the developmental stage of infection (as inferred from read counts). Snails infected by Petasiger sp. 5, Echinoparyphium sp. or Austrodiplostomum sp. 2 had larger shells than uninfected snails or than those infected by Plagiorchiida sp. Moreover, the shell shape of snails infected solely by Petasiger sp. 5 differed significantly from that of uninfected snails and snails infected with other trematodes, except from Austrodiplostomum sp. 2. Shape changes included a more protuberant apex, an inward-folded outer apertural lip and a more adapically positioned umbilicus. Size differences were more pronounced in snails with ‘late’ infections (>25 days) compared to earlier-stage infections. No phenotypic differences were found between snails infected by a single trematode species and those harbouring co-infections. Further work is required to assess the complex causal links between trematode infections and shell morphological alterations of snail hosts.
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spelling doaj.art-1e3605bb3b5845a793adc826acb217702022-12-22T03:41:35ZengElsevierInternational Journal for Parasitology: Parasites and Wildlife2213-22442022-08-0118300311Trematode infection affects shell shape and size in Bulinus tropicusCyril Hammoud0Annelies Kayenbergh1Julius Tumusiime2Dirk Verschuren3Christian Albrecht4Tine Huyse5Bert Van Bocxlaer6Ghent University, Limnology Unit, Department of Biology, B-9000, Gent, Belgium; Royal Museum for Central Africa, Department of Biology, B-3080, Tervuren, Belgium; Corresponding author. Ghent University, Limnology Unit, Department of Biology, 9000, Gent, Belgium.Royal Museum for Central Africa, Department of Biology, B-3080, Tervuren, BelgiumMbarara University of Science and Technology, Department of Biology, P. O. Box 1410, Mbarara, UgandaGhent University, Limnology Unit, Department of Biology, B-9000, Gent, BelgiumJustus Liebig University, Systematics and Biodiversity Lab, Department of Animal Ecology and Systematics, D-35392, Giessen, Germany; Mbarara University of Science and Technology, Department of Biology, P. O. Box 1410, Mbarara, UgandaRoyal Museum for Central Africa, Department of Biology, B-3080, Tervuren, Belgium; University of Leuven, Laboratory of Biodiversity and Evolutionary Genomics, B-3000, Leuven, BelgiumCNRS, Univ. Lille, UMR 8198 Evo-Eco-Paleo, F-59000, Lille, France; Ghent University, Limnology Unit, Department of Biology, B-9000, Gent, BelgiumTrematodes can increase intraspecific variation in the phenotype of their intermediate snail host. However, the extent of such phenotypic changes remains unclear. We investigated the influence of trematode infection on the shell morphology of Bulinus tropicus, a common host of medically important trematodes. We focused on a snail population from crater lake Kasenda (Uganda). We sampled a single homogeneous littoral habitat to minimize the influence of environmental variation on shell phenotype, and barcoded snails to document snail genotypic variation. Among the 257 adult snails analysed, 99 tested positive for trematode infection using rapid-diagnostic PCRs. Subsequently we used high-throughput amplicon sequencing to identify the trematode (co-)infections. For 86 out of the 99 positive samples trematode species delineation could discriminate among combinations of (co-)infection by 11 trematode species. To avoid confounding effects, we focused on four prevalent trematode species. We performed landmark-based geometric morphometrics to characterize shell phenotype and used regressions to examine whether shell size and shape were affected by trematode infection and the developmental stage of infection (as inferred from read counts). Snails infected by Petasiger sp. 5, Echinoparyphium sp. or Austrodiplostomum sp. 2 had larger shells than uninfected snails or than those infected by Plagiorchiida sp. Moreover, the shell shape of snails infected solely by Petasiger sp. 5 differed significantly from that of uninfected snails and snails infected with other trematodes, except from Austrodiplostomum sp. 2. Shape changes included a more protuberant apex, an inward-folded outer apertural lip and a more adapically positioned umbilicus. Size differences were more pronounced in snails with ‘late’ infections (>25 days) compared to earlier-stage infections. No phenotypic differences were found between snails infected by a single trematode species and those harbouring co-infections. Further work is required to assess the complex causal links between trematode infections and shell morphological alterations of snail hosts.http://www.sciencedirect.com/science/article/pii/S2213224422000657TrematodeGastropodGeometric morphometricsShell morphologyAmplicon sequencingBulinus tropicus
spellingShingle Cyril Hammoud
Annelies Kayenbergh
Julius Tumusiime
Dirk Verschuren
Christian Albrecht
Tine Huyse
Bert Van Bocxlaer
Trematode infection affects shell shape and size in Bulinus tropicus
International Journal for Parasitology: Parasites and Wildlife
Trematode
Gastropod
Geometric morphometrics
Shell morphology
Amplicon sequencing
Bulinus tropicus
title Trematode infection affects shell shape and size in Bulinus tropicus
title_full Trematode infection affects shell shape and size in Bulinus tropicus
title_fullStr Trematode infection affects shell shape and size in Bulinus tropicus
title_full_unstemmed Trematode infection affects shell shape and size in Bulinus tropicus
title_short Trematode infection affects shell shape and size in Bulinus tropicus
title_sort trematode infection affects shell shape and size in bulinus tropicus
topic Trematode
Gastropod
Geometric morphometrics
Shell morphology
Amplicon sequencing
Bulinus tropicus
url http://www.sciencedirect.com/science/article/pii/S2213224422000657
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