Historical dispersal and host-switching formed the evolutionary history of a globally distributed multi-host parasite – The Ligula intestinalis species complex

Nazarizadeh, Masoud; Nováková, Milena; Loot, Géraldine; Gabagambi, Nestory P.; Fatemizadeh, Faezeh; Osano, Odipo; Presswell, Bronwen; Poulin, Robert; Vitál, Zoltán; Scholz, Tomáš; Halajian, Ali; Trucchi, Emiliano; Kocova, Pavlina; Štefka, Jan

doi:10.1016/j.ympev.2022.107677

Cited by 7 publications

(22 citation statements)

References 114 publications

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“…Genetic evaluation of various populations of L. intestinalis from different fish populations around the world revealed that there are several genetically distinct parasite lineages from different fish hosts and zoogeographical regions that likely represent cryptic species (Bouzid et al, 2008; Štefka et al, 2009). The plerocercoids with the unusual sites of infection reported in the present account belong to lineage A of Nazarizadeh et al (2023) (or clade A of Bouzid et al, 2008), whose members are found in cypriniform fishes of the genera Abramis (including freshwater bream), Alburnus , Blicca , Phoxinus , Rutilus , Scardinius , Squalius (all Leuciscidae), and Carassius (Cyprinidae), and have been found in the Czech Republic, France, Germany, Ireland, Italy, Russia, the United Kingdom, Ukraine, and Tunisia (introduced) (Nazarizadeh et al, 2023).…”

Section: Figuresupporting

confidence: 56%

“…The plerocercoids with the unusual sites of infection reported in the present account belong to lineage A of Nazarizadeh et al (2023) (or clade A of Bouzid et al, 2008), whose members are found in cypriniform fishes of the genera Abramis (including freshwater bream), Alburnus, Blicca, Phoxinus, Rutilus, Scardinius, Squalius (all Leuciscidae), and Carassius (Cyprinidae), and have been found in the Czech Republic, France, Germany, Ireland, Italy, Russia, the United Kingdom, Ukraine, and Tunisia (introduced) (Nazarizadeh et al, 2023).…”

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confidence: 60%

“…These studies have shown that L. intestinalis is indeed a complex of morphologically indistinguishable but genetically distinct lineages (cryptic species) whose members parasitize different groups of fish intermediate hosts and occur in different zoogeographical regions (Štefka et al, 2009; Bouzid et al, 2008). However, a taxonomic revision of the group, in which individual species would be officially named, is still pending, mainly because morphological characters that could be used to delineate individual genetic lineages corresponding to separate species are lacking (Nazarizadeh et al, 2023).…”

Section: Figurementioning

confidence: 99%

“…This response consists predominantly of accumulation of macrophages, vacuolated granulocytes and lymphocytes, occasionally with neutrophils and plasma cells (Taylor & Hoole, 1989b). Plerocercoids of L. intestinalis are commonly found in freshwater fishes of various, often not closely related groups such as Salmonidae, Galaxiidae and Catostomidae, being predominantly found in cyprinoid hosts (Chapman et al, 2006;Dubinina, 1980;Gibson et al, 2005;Groves & Shields, 2001;Museth, 2001;Štefka et al, 2009). In all published reports, plerocercoids were reported to occur almost exclusively in the body cavity of their fish hosts.…”

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confidence: 99%

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Unusual sites of infection of Ligula intestinalis (Cestoda) plerocercoids in an intermediate host, freshwater bream Abramis brama

Adámek¹,

Palíková

Scholz

2023

Journal of Fish Diseases

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Section: Figuresupporting

confidence: 56%

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confidence: 60%

Section: Figurementioning

confidence: 99%

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confidence: 99%

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Unusual sites of infection of Ligula intestinalis (Cestoda) plerocercoids in an intermediate host, freshwater bream Abramis brama

Adámek¹,

Palíková

Scholz

2023

Journal of Fish Diseases

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“…Larval worms can be induced to develop sexually in vitro [18]. The tapeworm has been extensively used in endocrinological, ecological, population genetic, phylogeographic and immunological studies [20][21][22][23].…”

Section: Introductionmentioning

confidence: 99%

Highly resolved genome assembly and comparative transcriptome profiling reveal genes related to developmental stages of tapeworm Ligula intestinalis

Nazarizadeh,

Nováková,

Drábková

et al. 2024

Proc. R. Soc. B.

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Ligula intestinalis (Cestoda: Diphyllobothriidae) is an emerging model organism for studies on parasite population biology and host–parasite interactions. However, a well-resolved genome and catalogue of its gene content has not been previously developed. Here, we present the first genome assembly of L. intestinalis , based on Oxford Nanopore Technologies, Illumina and Omni-C sequencing methodologies. We use transcriptome profiling to compare plerocercoid larvae and adult worms and identify differentially expressed genes (DEGs) associated with these life stages. The genome assembly is 775.3 mega (M)bp in size, with scaffold N50 value of 118 Mbp and encodes 27 256 predicted protein-coding sequences. Over 60% of the genome consists of repetitive sequences. Synteny analyses showed that the 10 largest scaffolds representing 75% of the genome display high correspondence to full chromosomes of cyclophyllidean tapeworms. Mapping RNA-seq data to the new reference genome, we identified 3922 differentially expressed genes in adults compared with plerocercoids. Gene ontology analyses revealed over-represented genes involved in reproductive development of the adult stage (e.g. sperm production) and significantly enriched DEGs associated with immune evasion of plerocercoids in their fish host. This study provides the first insights into the molecular biology of L. intestinalis and provides the most highly contiguous assembly to date of a diphyllobothriid tapeworm useful for population and comparative genomic investigations of parasitic flatworms.

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Loss of species and genetic diversity during colonization: Insights from acanthocephalan parasites in northern European seals

Sromek,

Ylinen,

Kunnasranta

et al. 2023

Ecology and Evolution

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Studies on host–parasite systems that have experienced distributional shifts, range fragmentation, and population declines in the past can provide information regarding how parasite community richness and genetic diversity will change as a result of anthropogenic environmental changes in the future. Here, we studied how sequential postglacial colonization, shifts in habitat, and reduced host population sizes have influenced species richness and genetic diversity of Corynosoma (Acanthocephala: Polymorphidae) parasites in northern European marine, brackish, and freshwater seal populations. We collected Corynosoma population samples from Arctic, Baltic, Ladoga, and Saimaa ringed seal subspecies and Baltic gray seals, and then applied COI barcoding and triple‐enzyme restriction‐site associated DNA (3RAD) sequencing to delimit species, clarify their distributions and community structures, and elucidate patterns of intraspecific gene flow and genetic diversity. Our results showed that Corynosoma species diversity reflected host colonization histories and population sizes, with four species being present in the Arctic, three in the Baltic Sea, two in Lake Ladoga, and only one in Lake Saimaa. We found statistically significant population‐genetic differentiation within all three Corynosoma species that occur in more than one seal (sub)species. Genetic diversity tended to be high in Corynosoma populations originating from Arctic ringed seals and low in the landlocked populations. Our results indicate that acanthocephalan communities in landlocked seal populations are impoverished with respect to both species and intraspecific genetic diversity. Interestingly, the loss of genetic diversity within Corynosoma species seems to have been less drastic than in their seal hosts, possibly due to their large local effective population sizes resulting from high infection intensities and effective intra‐host population mixing. Our study highlights the utility of genomic methods in investigations of community composition and genetic diversity of understudied parasites.

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Historical dispersal and host-switching formed the evolutionary history of a globally distributed multi-host parasite – The Ligula intestinalis species complex

Cited by 7 publications

References 114 publications

Unusual sites of infection of Ligula intestinalis (Cestoda) plerocercoids in an intermediate host, freshwater bream Abramis brama

Unusual sites of infection of Ligula intestinalis (Cestoda) plerocercoids in an intermediate host, freshwater bream Abramis brama

Highly resolved genome assembly and comparative transcriptome profiling reveal genes related to developmental stages of tapeworm Ligula intestinalis

Loss of species and genetic diversity during colonization: Insights from acanthocephalan parasites in northern European seals

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